Feb 7, 2015 - tour de France, du pistolet à billes et à fléchettes, du chamboule-tout d'échantillons et même un ...... mobility in soil and water systems (Beesley et al., 2010). Indeed, its ...... the Wadley Sb district (San Luis, PotosÃ, Mexico), Sci.
` THESE En vue de l’obtention du
´ DE TOULOUSE DOCTORAT DE L’UNIVERSITE D´ elivr´ e par : l’Universit´e Toulouse 3 Paul Sabatier (UT3 Paul Sabatier)
Pr´ esent´ ee et soutenue le 26/10/2016 par :
Antoine PIERART Rˆ ole des champignons mycorhiziens ` a arbuscules et des bioamendements dans le transfert et la bioaccessibilit´ e de Cd, Pb et Sb vers les v´ eg´ etaux cultiv´ es en milieu urbain.
JURY M. Mikael MOTELICA-HEINO Mme. Camille DUMAT Mme. Corinne LEYVAL M. Christophe NGUYEN M. Juan-Carlos SANCHEZ-HERNANDEZ Mme. Eva SCHRECK Mme. Nathalie SEJALON-DELMAS
Professeur - Pr´esident Professeur Directeur de Recherche Directeur de Recherche Professeur Maitre de Conf´erences Maitre de Conf´erences
´ Ecole doctorale et sp´ ecialit´ e: ´ SDU2E : Ecologie fonctionnelle Unit´ e de Recherche : Laboratoire d’´ecologie fonctionnelle et environnement - EcoLab (UMR 5245) Directeur(s) de Th` ese : Mme. Camille DUMAT et Mme. Nathalie SEJALON-DELMAS Rapporteurs : Mme. Corinne LEYVAL, M. Christophe NGUYEN
Orl´eans Toulouse Nancy Bordeaux Tol`ede Toulouse Toulouse
i
NOTE TO READERS
To follow the charter of thesis from the University Paul Sabatier of Toulouse, the following thesis is written in the form of classical chapters and scientific publications (accepted, submitted or in preparation) in their edited form. For accepted and submitted articles, section, page, figure and table numbering was adapted to the manuscript. For the same reason, the abstract was written both in French and English. A summarized French version of the introduction and a full conclusion were also added.
Inspired from 9gag
If your brain just came in coma, Les orteils barbus, 2011
You can consult all the research scientific articles, posters from international congress, and research projects of my PhD with the following QR code:
ii CITATIONS
“Knowledge generates ignorance” Stuart Firestein, The pursuit of ignorance (TEDx conference)
“El ser humano puede ser el único animal capaz de destruirse si mismo. Ese es el dilema que tenemos por adelante” Jose Muica, Uruguay former president (2010-2015)
“Much to learn, you still have…” Yoda, Star Wars – attack of the clones
iii THANKS
Oops, I did it again… Britney Spears, 2000 On va commencer par une petite confession. Parce que oui, dans les remerciements on dit merci, mais on se confesse aussi : Au début, je n’avais pas envie ! ‘’Prends le temps d’y réfléchir Antoine, tu devrais faire une thèse.’’, m’a dit le couple de chercheurs de choc David & Marie-Hélène Macherel, un de ces (nombreux) jours pluvieux d’automne angevine pendant un stage au laboratoire IRHS il y a 5 ans. Ma réponse, ‘’La thèse, ça n’est pas pour moi, j’ai déjà fait bien assez de laboratoire’’. J’étais catégorique, plus jamais, décidé à bosser pour de bon. Finalement, je reste dans le monde de la recherche : stage de fin d’études en laboratoire, premier emploi en station d’expérimentation ; ça s’accroche, comme ce petit caillou sur lequel on marche et qui reste coincé dans la semelle pendant des semaines. Je crois que c’est cette petite phrase, à une époque où je ne savais finalement pas vraiment quoi faire de mon avenir, qui a trottée dans ma tête et m’a conduite ici ! Peut-être que vous n’aviez pas tort finalement ? Alors, merci à vous deux, et à toute votre équipe ! Un très grand merci à mes directrices en or, Camille et Nathalie. Vous m’avez fait confiance par téléphone, sans même que l’on se rencontre, dès le début de cette histoire ! Et vous avez continué pendant ces trois années au point même de partir vers d’autres horizons la dernière année. Et pourtant, même à distance, vous avez toujours été là pour m’aider, me guider, parler de tout et de rien, que ce soit scientifique ou non et c’est agréable d’être aussi bien encadré. Parce que ce n’est encore que le début, et qu’il reste un bon tas de pages à lire. A mes rapporteurs, merci d’avoir accepté d’évaluer mes travaux et bon courage ! J’ai une pensée particulière pour l’ensemble de notre société, qui par ses travers m’a fourni un bel objet d’étude. La pollution, c’est moche. Ceci dit, ça crée de l’emploi. Merci ou pas, à chacun de voir. Merci EcoLab, et en particulier l‘équipe Biogeochim, devenue Biz pour m‘avoir trouvé un bureau et des espaces de recherche autant en laboratoire que dans les serres. Un grand merci aux techniciennes, Marie-Jo et Virginie. On a assez peu travaillé ensemble finalement, mais vous avez toujours su vous montrer disponibles et réactives pour m’aider et m’aiguiller quand j’en avais besoin. Annick, merci pour ta gentillesse et ta disponibilité. Ecolab c’est évidemment tant d’autres rencontres, d’un bout à l’autre de ces longs couloirs un peu sombres que je ne pourrai pas passer tout le monde en revue. D’abord parce que c’est très long, ensuite parce que ceux qui me connaissent savent que je suis très mauvais avec les prénoms ! Merci à tous pour ces petits moments, qui ont rendu le quotidien si agréable.
iv Il y a quand même le bureau 204, ma deuxième maison où il s’est passé tant de choses. Du curling, le tour de France, du pistolet à billes et à fléchettes, du chamboule-tout d’échantillons et même un punching-ball. Du boulot aussi, ne vous méprenez pas ! Un grand merci à tous ses habitants, compagnons de galère et amis qui sont venus et partis : Thibaut, qui m’a initié aux joies de la bioaccessibilité. Xiaoling et sa punk attitude, toujours prête à tout essayer ! Adrien, sacré rencontre. On est même devenu colocs, brassé de la bière, (tenté de) faire pousser des champignons, faire fermenter toutes sortes de choses depuis la choucroute jusqu’au sureau en passant par la betterave et j’en passe ! Léonard, pour ce face à face pendant plus de deux ans. Tu incarnes la jovialité que je n’ai pas ; si si, la science l’a prouvé ! Et comme je suis sûr que ça te fait plaisir, cette dédicace est dans ta police préférée. Youen, ce parfait mélange de bonne humeur et de complaintes qui te caractérise tant, tu m’as bien fait rire ! Et puis Théo, arrivant tardif mais tu as bien rattrapé ton retard. Les jours racines ou feuilles n’ont plus de secret pour moi, ou presque ! Il y en a quelques-uns qui ne sont pas vraiment du bureau mais vous le méritez bien quand même : Sophia, c’est comme si tu étais dans le bureau, à moitié finalement. Merci pour ton sourire, ta très bonne cuisine et pour garder Loulou de temps en temps. Pierre-Alexis, grand fan de chanson Française ! Stéphane, on se soutient mutuellement, commencer ensemble, terminer ensemble ! Merci à tout le LRSV pour m’avoir accueilli chaleureusement pour toutes ces manips que je ne pouvais pas faire à EcoLab. J’ai trouvé chez vous une troisième maison pleine d’entraide, et de discussions passionnantes. Vous m’avez tous énormément appris et motivé, en particulier Christophe et Francis. Merci aussi à Alexis, Elise et Arthur pour votre aide précieuse (indispensable !) en métagénomique. Aller plus hauuuuuuuuuuuut… Tina Arena, 1997
(Vous l’avez chanté dans votre tête ? maintenant oui…)
Quand on arrive à saturation, des tubes, des flacons, des échantillons et des citations, il faut un exutoire ; pour moi c’était l’escalade. Grimper, toujours plus, en salle ou en nature, surtout en nature pour tout oublier. Grace à elle, j’ai appris à connaitre des gens formidables. Pour n’en citer que deux : Jojo, l’infatigable autant sur les falaises qu’en soirée ! Vincent, Je ne sais pas si je dois te remercier pour les patates ou la grimpe, on va dire les deux. Y hay también todas estas semanas que pasé en Toledo a descubrir el mundo apasionante de las enzimas del suelo y del biochar. Todo esto con croissant a la plancha, heavy metal música en un ambiente memorable. ¡Muchísimas gracias JuanK, fue un gran placer! Viví allá en la familia la más internacional e increíble del mundo: Marga y sus hermanos, Miguel, Raquel, Rodrigo, Marjio, Kevin, Shane, Viviana, Johnson, Olivia y tantas otras personas que tenían esta misma visión de un mundo que se comparte, Gracias para todo. Volveré pronto, ¡para vacaciones esta vez!
v A tous mes amis, d’ici ou ailleurs, merci de m’avoir suivi et soutenu pendant ces trois années. En particulier Luiz, coloc d’un temps pour ces soirées passées à refaire le monde. Maxime et Mélanie, qui êtes venus jusqu’à Madrid profiter des tapas ! La douche baquet dans la chambre triple de 12m², ça c’est de l’amitié. Merci Manu, toi seul sais pourquoi, gros ! A tous ceux que j’oublie, merci et désolé, ou l’inverse. Merci à toute ma famille, Papa, Maman, Clément et Hadrien. C’est aussi cette enfance dans la nature et tous ces moments partagés qui m’ont guidé jusqu’ici. Vous m’avez toujours soutenu dans mes décisions, même si vous vous êtes probablement beaucoup demandé pourquoi une thèse ? Pourquoi pas un vrai travail ? Pourquoi encore être étudiant après une école d’ingénieur ? Pourquoi, pourquoi, pourquoi ? N’est-ce pas l’un des fondements de la recherche de se demander pourquoi ? But of all these friends and lovers, There is no one compares with you. The Beatles, In my life
Enfin, un immense merci à toi ma Bichette, pour m’avoir épaulé tous les jours, autant dans mes réussites que dans mes passages à vide, où malgré mon air sûr de moi j’avais bien besoin de toi. Loulou, Mimi, merci d’avoir pris soin de mon moral en creusant dans le jardin et de mon sommeil en dormant sur ma tête. Remercier les bêtes, pourquoi pas… Les enfants ne sont pas encore là, alors on se rabat sur ce que l’on peut.
vi ABBREVIATIONS AMF: Arbuscular Mycorrhizal Fungi %B: Bioaccessible fraction BF: Bioaccumulation Factor BARGE: BioAccessibility Research Group of Europe CARBOX: Carboxylesterase CAT: Catalase DEHY: Dehydrogenase GLUCO: β-Glucosidase ICP-MS: Induced Coupled Plasma-Mass Spectrometry ICP-OES: Induced Coupled Plasma-Optical Emission Spectrometry KSb: potassium antimony tartrate trihydrate %OM: Total Organic Matter content OTU: Operational Taxonomic Unit PCR: Polymerase Chain Reaction PHO_ACI: Phosphatase Acide PHO_ALK: Phoshatase Alkaline PROTEA: Protease SCG: Spent Coffee Ground SCGc: charred Spent Coffee Ground (biochar) SEM: Scanning Electron Microscopy s-µ-p: Soil-microorganism-plant (interface) TEM: Transmission Electron Microscopy TF: Translocation Factor TM: (ETM in French version) General term for metalloid and heavy metal trace elements UBM: Unified Barge Method UPA: (AUP in French version) Urban and Peri-urban Agriculture UREA: Urease
vii VALUATION OF WORKS Published articles Pierart A., Shahid M., Séjalon-Delmas N., Dumat C., 2015. Antimony bioavailability: knowledge and research perspectives for agriculture. J. of Hazar. Mat., 289, 21. Xiong T., Austruy A., Pierart A., Shahid M., Schreck E., Mombo S., Dumat C., 2016a. Kinetic study of phytotoxicity induced by foliar lead uptake for vegetables exposed to fine particles and implications for sustainable urban agriculture. J. of Env. Sc., 46, 16-27. Xiong T., Dumat C., Pierart A., Shahid M., Kang Y., Li N., Bertoni G., Laplanche C., 2016b. Measurement of metal bioaccessibility in vegetables to improve human exposure assessments: field study of soil–plant–atmosphere transfers in urban areas, South China. Env. Geochem. Health, 1-19. Goix S., Mombo S., Schreck E., Pierart A., Lévêque T., Deola F., Dumat C., 2015. Field isotopic study of lead fate and compartmentalization in earthworm–soil–metal particle systems for highly polluted soil near Pb recycling factory. Chemosphere, 138, 10-17. Mombo S., Foucault Y., Deola F., Gaillard I., Goix S., Shahid M., Schreck E., Pierart A., Dumat C., 2016. Management of human health risk in the context of kitchen gardens polluted by lead and cadmium near a lead recycling company. Journal of Soils and Sediments, 16, 1214-1224 Mombo S., Schreck E., Dumat C., Laplanche C., Pierart A., Longchamp M., Besson P., CastrecRouelle M., 2016. Bioaccessibility of selenium after human ingestion in relation to its chemical species and compartmentalization in maize. Envir. Geo. and health, 38, 3, 869-883. Dumat C., Wu J.T., Pierart A., Sochacki L., 2015. Interdisciplinary and participatory research for sustainable management of arsenic pollution in French collective gardens: collective process of risk manufacture, in: 9ième Journées de Recherche En Sciences Sociales. Nancy, pp. 1-20. Sanchez-Hernandez J.C., Sandoval M., Pierart A., 2017. Short-term response of soil enzyme activities in a chlorpyrifos-treated Andisol: use of enzyme-based indexes. Ecological Indicators, 73, 525-535.
Submitted articles Pierart A., Dumat C., Braud A., Séjalon-Delmas N., under review. How do soil biofertilizers and organic amendments influence Cd phytoavailability and human bioaccessibility? J. of Hazar. Mat.
viii
Oral communications Pierart A., Dumat C., Séjalon-Delmas N., Plant-Fungi Association: Track to Dig for Sustainable Agriculture; Beware of Metal Pollutions in Urban Areas. 18th International Conference on Heavy Metals in the Environment, 12-15 September 2016, Ghent, Belgium. Pierart A., Gestion raisonnée des pollutions pour une agriculture durable. Favoriser les agricultures urbaines durables Retours d’expériences et initiatives innovantes à développer, 5th november 2015, Auzeville, France. Pierart A., Braud A., Lebeau T., Séjalon-Delmas N., Dumat C., Influence of mycorrhization and soil organic matters on lead and antimony transfers to vegetables cultivated in urban gardens: environmental and sanitary consequences. 24è Réunion des Sciences de la Terre, 27-31 October 2014, Pau, France. Dumat C., Wu J.T., Pierart A., Sochacki L., Interdisciplinary and participatory research for sustainable management of arsenic pollution in French collective gardens: collective process of risk manufacture, 9ième Journées de Recherche En Sciences Sociales. 10-11 december 2015, Nancy, France. Mombo S., Foucault Y., Shahid M., Gaillard I., Goix S., Schreck E., Pierart A., Dumat C., Metal bioaccessibility to refine human health risk assessment: case of Pb and Cd pollution in kitchen gardens. 24è Réunion des Sciences de la Terre, 27-31 October 2014, Pau, France.
Posters Pierart A., Dumat C., Séjalon Delmas N. Influence de la mycorhization sur la phytodisponibilité et la bioaccessibilité du plomb, du cuivre et de l’antimoine présents dans les sols. Focus sur les jardins potagers contaminés en zones urbaines. Les 12è Rencontres de la fertilisation raisonnée et de l'analyse, 18-19 november 2015, Lyon, France. Pierart A., Dumat C., Séjalon-Delmas N. How do mycorrhizal symbiosis and organic matter influence Cd transfer from soil to edibles? Special focus on health threats of urban and periurban soils. 8th International Conference on Mycorrhiza, 3-7 August 2015, Flagstaff, Arizona, USA. Pierart A., Mombo S., Dumat C., Séjalon-Delmas N. Antimony in urban gardens: mycorrhizal symbiosis and organic matter influence on vegetables accumulation and human bioaccessibility. Congrès InterSol 24-26 Mars 2015, Paris. Pierart A., Braud A., Lebeau T., Séjalon-Delmas N., Dumat C. Influence of mycorrhization and soil organic matters on lead and antimony transfers to vegetables cultivated in urban gardens: environmental and sanitary consequences. International Congress on Mycorrhizae, 15-17 October 2014, Marrakesh, Morocco. Shahid M., Pierart A., Sabir M., Ghafoor A., Dumat C. Assessing the effect of organic amendments on soil properties, nickel availability in soil and uptake by Trifolium alexandrinum L. 24è Réunion des Sciences de la Terre, 27-31 October 2014, Pau, France.
ix TABLE OF CONTENTS NOTE TO READERS............................................................................................................................................................... i CITATIONS ...........................................................................................................................................................................ii THANKS ..............................................................................................................................................................................iii ABBREVIATIONS………………………………………………………………………………………………………………………………………………………….…iv VALUATION OF WORKS .....................................................................................................................................................vii TABLE OF CONTENTS ..........................................................................................................................................................ix LISTE OF FIGURES ...............................................................................................................................................................xi LISTE OF TABLES ............................................................................................................................................................... xiii
CHAPTER 1. SCIENTIFIC CONTEXT: HOW AND WHY STUDY INORGANIC POLLUTION IN URBAN SOILS? ............ 1 1.1. INTRODUCTION GÉNÉRALE .................................................................................................................................. 2 1.2. METAL(LOID) SOIL CONTAMINATION AND POLLUTION .............................................................................................. 9 1.3. SB BIOAVAILABILITY: KNOWLEDGE AND RESEARCH PERSPECTIVES FOR SUSTAINABLE AGRICULTURE………………………………..17 1.4. URBAN AGRICULTURE, TO A SAFE AUTO-CONSUMPTION MODEL ............................................................................... 38 1.4. USING OF BIOFERTILIZERS AND ORGANIC AMENDMENTS TO DEAL WITH METALLOID CONTAMINATION .............................. 41 1.5. HEALTH RISK ASSESSMENT & HUMAN BIOACCESSIBILITY .......................................................................................... 53 1.6. WHAT DO WE STUDY AND HOW DO WE PROCEED? ................................................................................................ 56 CHAPTER 2. MATERIAL AND METHODS .......................................................................................................... 59 2.1. SOIL DESCRIPTION ........................................................................................................................................... 60 2.2. FULL PLANT CULTIVATED IN POT UNDER GREENHOUSE CONDITION............................................................................. 62 2.3. SB TRANSFER IN SIMPLIFIED HYDROPONIC SYSTEMS ................................................................................................ 64 2.4. INFLUENCE OF BIOCHAR AND SB CONCENTRATION ON SOIL MICROBIAL ACTIVITY .......................................................... 66 2.5. MEASUREMENT OF METAL(LOID) CONCENTRATION................................................................................................ 69 2.6. FUNGAL DESCRIPTION ...................................................................................................................................... 71 2.7. ENZYME ASSAY AND MATHEMATICAL INDEXES....................................................................................................... 78 2.8. MICROSCOPY ................................................................................................................................................. 82 2.9. STATISTICAL ANALYSIS ...................................................................................................................................... 83 CHAPTER 3. HOW DO SOIL AMF AND OM INFLUENCE CD PHYTOAVAILABILITY AND BIOACCESSIBILITY? ....... 85 3.1. GENERAL INTRODUCTION ................................................................................................................................. 85 3.2. SUBMITTED ARTICLE……………………………………………………………………………………………………………………………………87 3.3. ADDITIONAL RESULTS .................................................................................................................................... 108 3.4. GENERAL CONCLUSION .................................................................................................................................. 110 CHAPTER 4. INFLUENCE OF AMF AND OM ON PB AND SB ACCUMULATION AND BIOACCESSIBILITY ............ 111 4.1. GENERAL INTRODUCTION ............................................................................................................................... 111 4.2. PB AND SB ACCUMULATION INFLUENCED BY AMF COMMUNITY AND OM IN A CROP ROTATION .................................... 113 4.3. ADDITIONAL RESULTS AND DISCUSSION ............................................................................................................. 133 4.4. GENERAL CONCLUSION .................................................................................................................................. 143 CHAPTER 5. USING AN HYDROPONIC APPROACH TO STUDY THE ROLE OF AMF IN VEGETABLE SB UPTAKE . 145 5.1. GENERAL INTRODUCTION ............................................................................................................................... 145 5.2. EXPERIMENTAL DESIGN SUMMARY.................................................................................................................... 147 5.3. RESULTS AND DISCUSSION .............................................................................................................................. 147 5.4. CONCLUSIONS AND PERSPECTIVES .................................................................................................................... 153
x CHAPTER 6. PHYTOACCUMULATION OF SB AND SOIL ENZYME ACTIVITIES: EFFECTS OF OM AND BIOCHAR..155 6.1. INTRODUCTION............................................................................................................................................. 155 6.2. EXPERIMENTAL DESIGN .................................................................................................................................. 157 6.3. RESULTS AND DISCUSSION .............................................................................................................................. 158 6.4. CONCLUSION ............................................................................................................................................... 171 6.5. SUPPLEMENTARY MATERIALS........................................................................................................................... 172 CHAPTER 7. DISCUSSION .............................................................................................................................. 173 7.1. SPECIES AND VARIETIES HAVE TO BE CHOSEN WISELY ............................................................................................ 173 7.2. IS IT RISKY OR SAFE TO USE ORGANIC MATTER AMENDMENTS IN UPA? .................................................................... 175 7.3. WHAT ABOUT BIOFERTILIZERS LIKE MYCORRHIZAL FUNGI?..................................................................................... 177 7.4. COULD BIOCHAR APPLICATION IN URBAN GARDENS REDUCE TM IMPACT ON CROPS QUALITY?...................................... 179 7.5. SOME RECOMMENDATIONS ............................................................................................................................ 180 CHAPTER 8. GENERAL CONCLUSION & PERSPECTIVES .................................................................................. 186 BIBLIOGRAPHY……………………………………………………………………………………………………………………………….………….201
xi LIST OF FIGURES
FIGURE 1.1: BIOGEOCHEMICAL CYCLE OF TM.................................................................................................................. 10 FIGURE 1.2: PROPORTION OF MAJOR CONTAMINATION SOURCES FOR TM ENTRANCE IN ARABLE LANDS...................................... 10 FIGURE 1.3: CADMIUM CONTENT IN FRENCH SOILS .......................................................................................................... 11 FIGURE 1.4: LEAD CONTENT IN SOIL............................................................................................................................... 12 FIGURE 1.5: ANTIMONY, AN ALLOY IN AMMUNITIONS ....................................................................................................... 14 FIGURE 1.6: HOW TO TREAT A POLLUTED OR CONTAMINATED SOIL? .................................................................................... 15 FIGURE 1.7: MYCORRHIZAL ROLE IN ANTIMONY (SB) TRANSFER FROM SOIL TO PLANTS………………………………………………………… 27 FIGURE 1.8: ANTIMONY BIOACCUMULATION IN EARTHWORMS ........................................................................................... 28 FIGURE 1.9: FERTILIZING CROPS, COSTS AND BENEFITS. ..................................................................................................... 41 FIGURE 1.10: DIFFERENT GROUP OF MYCORRHIZAL FUNGI ................................................................................................. 42 FIGURE 1.11: ARBUSCULAR MYCORRHIZAL FUNGI SYMBIOSIS IN A NUTSHELL ......................................................................... 43 FIGURE 1.12: SIMPLIFIED BIOCHAR PRODUCTION, FROM ORGANIC MATTER TO BIOCHAR INTERESTS AND RISKS ............................. 52 FIGURE 1.13: SCHEMATIC REPRESENTATION OF THE BIOACCESSIBILITY OF AN ELEMENT WHEN INGESTED AND DIGESTED ................. 54 FIGURE 1.14: REPRESENTATION OF THE TRIALS’ GRADIENT OF COMPLEXITY ........................................................................... 57 FIGURE 2.1: SCIENTIFIC QUESTIONS DEVELOPED IN THE PRESENT THESIS................................................................................ 59 FIGURE 2.2: STUDIED SOIL LOCALIZATION. BZC, BAZOCHES; NTE, NANTES; TLD, TOLEDO. ..................................................... 61 FIGURE 2.3: EXPERIMENTAL DESIGN OF A CROP ROTATION ON CONTAMINATED SOILS .............................................................. 63 FIGURE 2.4: EXPERIMENTAL DESIGN FOR HYDROPONIC CARROT CULTIVATION TREATED WITH SB................................................ 65 FIGURE 2.5: HOME-MADE BIOCHAR (SCGC) FROM SPENT COFFEE GROUND (SCG)................................................................. 66 FIGURE 2.6: EXPERIMENTAL DESIGN OF PEAS (PISUM SATIVUM L.) ...................................................................................... 68 FIGURE 2.7: PICTURE OF STAINED LEEK ROOTS ................................................................................................................. 71 FIGURE 2.8: THE MOTHURGUI INTERFACE AND THE PIPELINE OF ANALYSIS DEVELOPED AND USED FOR SEQUENCE CLEANING .......... 73 FIGURE 2.9: THE USEARCH USER FRIENDLY INTERFACE ...................................................................................................... 75 FIGURE 2.10: SEAVIEW INTERFACE AND NON-ALIGNED SEQUENCES (EXTRACT). EACH COLOR REPRESENT A NUCLEOTIDE. ............... 77 FIGURE 2.11: ALIGNED SEQUENCES, WITH MUSCLE ALGORITHM.......................................................................................... 77 FIGURE 2.12: EXAMPLE OF PHYLOGENIC TREE (CLAD FORMAT). .......................................................................................... 77 FIGURE 2.13: THE BASIC PRINCIPLE OF SCANNING ELECTRON MICROSCOPY .......................................................................... 82 FIGURE 3.1: SCIENTIFIC OBJECTIVES AND METHODS FOR CD FATE AT THE SOIL-MICROORGANISM-PLANT INTERFACE. ..................... 86 FIGURE 3.2: CADMIUM CONCENTRATION IN PLANT ORGANS............................................................................................... 96 FIGURE 3.3: CADMIUM BIOACCESSIBLE FRACTION IN EDIBLE PARTS. ..................................................................................... 96 FIGURE 3.4: SCHEMATIC REPRESENTATION OF CD FLUXES FROM AERIAL DEPOSITION THROUGH SOIL TO (AND WITHIN) PLANTS …….101 FIGURE 3.51: SCANNING ELECTRON MICROSCOPY COUPLED WITH X-RAY ANALYSIS OF MYCORRHIZED LEEK ROOTS ...................... 108 FIGURE 4.1: SCIENTIFIC OBJECTIVES FOR STUDYING THE FATE OF PB AND SB AT THE ‘SOIL-MICROORGANISM-PLANT’ INTERFACE. ... 112 FIGURE 4.2: METALLOID (PB OR SB) ACCUMULATION IN PLANTS ORGANS (AVERAGE ± STANDARD DEVIATION)........................... 124 FIGURE 4.3: SCANNING ELECTRON MICROSCOPY COUPLED WITH X-RAY ANALYSIS OF MYCORRHIZED LEEK ROOTS ........................ 126
xii FIGURE 4.4: RELATIVE ABUNDANCE OF FUNGI IN DIFFERENT TREATMENTS........................................................................... 127 FIGURE 4.5: ONE COPY OF RIBOSOMAL GENOME SEQUENCE WITH ITS INTERNAL TRANSCRIBED SPACERS (ITS1&2).................... 133 FIGURE 4.6: TAXONOMY OF GLOMEROMYCOTA OBTAINED FOR THE ARTIFICIAL COMMUNITY WITH EACH PRIMER PAIR ................. 136 FIGURE 4.7: NEIGHBOR-JOINING PHYLOGENIC TREE OF THE ARTIFICIAL COMMUNITY’S OTU................................................... 137 FIGURE 5.1: OBJECTIVES OF THE HYDROPONIC EXPERIMENT REGARDING AMF INFLUENCE ON SB TRANSFER TO PLANTS ............... 146 FIGURE 5.2: EXPERIMENTAL DESIGN FOR HYDROPONIC CARROT CULTIVATION TREATED WITH SB.............................................. 147 FIGURE 5.3: PLANT DRY BIOMASS AND MYCORRHIZATION RATE (%)................................................................................... 148 FIGURE 5.4: SB CONTENT IN MG PER KG DRY WEIGHT OF PLANT ORGANS IN CARROT AND LETTUCE. .......................................... 149 FIGURE 5.5: MAIN RESULTS OF THE INFLUENCE OF AMF ON SB TRANSFER DEPENDING ON PLANT AND SB SPECIATION ................. 153 FIGURE 5.6: THE USE OF DOUBLE COMPARTMENT IN VITRO HAIRY ROOT SYSTEM .................................................................. 154 FIGURE 6.1: CONCEPTUAL SCHEME ILLUSTRATING THE MAIN OBJECTIVES OF THE SB–BIOCHAR–SOIL ENZYMES EXPERIMENT.......... 156 FIGURE 6.2: EXPERIMENTAL DESIGN. PEAS (PISUM SATIVUM L.) ....................................................................................... 157 FIGURE 6.3: IBRV2 INDEX OF CONTROL SOILS (SCG- AND SCGC-FREE) .............................................................................. 159 FIGURE 6.4: DETAIL OF THE A FACTOR FROM THE IBRV2................................................................................................. 160 FIGURE 6.5: VARIATION OF THE IBRV2 INDEX (Δ T2-T0) ................................................................................................ 164 FIGURE 6.6: DETAIL OF THE A-SCORES FROM THE IBRV2................................................................................................. 166 FIGURE 6.7: SCGC EXTRACTION FROM SOIL. ................................................................................................................. 168 FIGURE 6.8: SCANNING ELECTRON MICROSCOPY (A), OPTIC MICROSCOPY (B) (C) OF FUNGAL STRUCTURES AND BACTERIA ........... 168 FIGURE 6.9: SCGC AFTER EXTRACTION AND WASHING .................................................................................................... 169 FIGURE 6.10: DEHYDROGENASE ACTIVITY BEFORE AND AFTER STERILIZATION ....................................................................... 170 FIGURE 6.11: INDEXES OF CONTROL SOILS (SCG- AND SCGC-FREE) DEPENDING ON SB CONCENTRATIONS ................................ 172 FIGURE 7.1: PICTURE OF LEEK ROOT CELLS IN TRANSMISSION ELECTRONIC MICROSCOPY COUPLED WITH X RAY ANALYSIS.. ............ 174 FIGURE 7.2: CHOOSING THE BEST PLANT TYPE FACING A HAZARDOUS CONTAMINATION ......................................................... 175 FIGURE 7.3: FACTORS () AFFECTING THE POSSIBLE EFFECTS OF BIOAMENDMENTS ON TM FATE IN SOIL.................................. 177 FIGURE 7.4: ANNUAL (2012) MEAN OF PM10............................................................................................................. 181 FIGURE 7.5: WIND DIRECTION AND BUILDING ARRANGEMENT EFFECTS ON PARTICLE DISPERSION. ............................................ 182 FIGURE 7.6: MANAGEMENT OF A CONTAMINATION IN URBAN AGRICULTURE PROJECT ........................................................... 183
xiii LIST OF TABLES TABLE 1.1: LEGAL THRESHOLD OF PB IN DRINKING WATER, SOIL, AND ALIMENTS .................................................................... 13 TABLE 1.2: MINIMAL AND MAXIMAL SB VALUES IN SELECTED SOIL AND LIVING ORGANISMS…………………………………………………… 20 TABLE 1.3: ANTIMONY BIOACCUMULATIONFACTOR (BAF) IN EDIBLE PLANTS………………………………………..……………………………21 TABLE 1.4: REVIEW OF SB CONTENT IN EDIBLE PLANTS IN RELATION WITH THE FORM OF SB AND TYPE OF EXPERIMENT ................... 23 TABLE 1.5: REVIEW OF SB CONTENT IN RICE IN RELATION WITH THE FORM OF SB AND TYPE OF EXPERIMENT……………………………….25 TABLE 1.6: MYCORRHIZAL RESPONSE UNDER TM STRESS…………………………………………………………………………………..…………..26 TABLE A.1: SOLUBLE ANTIMONY FRACTION………………………………………………………………………………………………………………….35
TABLE A.2: ANTIMONY BIOACCUMULATION FACTOR (BAF) IN EDIBLE PLANTS………………………………………………………………..…..36 TABLE A.3: PRESENCE OR ABSENCE OF (CH3)3SB WHEN SCOPULARIOPSIS BREVICAULIS IS EXPOSED TO DIFFERENT SB SPECIES ………..37 TABLE A.4: DAILY INTAKE OF ANTIMONY IN CHINA WITH REGARD TO TOLERABLE DAILY INTAKE (TDI) ………………………………………37 TABLE 1.7: SYNTHESIS OF AMF IMPACT ON TM MOBILITY IN SOIL AND PHYTOACCUMULATION ……..………………………………………44 TABLE 2.1: BAZOCHES (BZC) AND NANTES (NTE) SOIL CHARACTERISTICS………………………………………………………………………….61 TABLE 2.2: TOLEDO SOIL CHARACTERISTICS AT THE END OF THE EXPERIMENT ......................................................................... 67 TABLE 2.3: METALLOID RECOVERY RATE ......................................................................................................................... 70 TABLE 2.4: PRIMER PAIRS USED FOR ILLUMINA MISEQ IDENTIFICATION OF AMF COMMUNITIES. .............................................. 72 TABLE 2.5: POTENTIAL ENZYME ACTIVITIES MEASURED IN PEAS EXPERIMENT ......................................................................... 78 TABLE 3.1: SOIL CHARACTERISTICS AT BAZOCHES (BZC) AND NANTES (NTE) ........................................................................ 90 TABLE 3.2: MEASURED PARAMETERS IN SOIL AND PLANT ................................................................................................... 95 TABLE 3.3: MOBILE (CACL2 EXTRACT) AND MOBILIZABLE (EDTA EXTRACT) FRACTIONS (%) OF CADMIUM IN SOIL ......................... 95 TABLE 3.4: AVERAGE CADMIUM DAILY INTAKE (DI) AND MAXIMAL DAILY CONSUMPTION (DCMAX)............................................ 97 TABLE 1 (SM): CHEMICAL COMPOSITION OF LOMBRICOMPOST……………………………………………………………………………………..107 TABLE 2 (SM): DETAIL OF SIGNIFICANT GROUPS AT Α = 5% FOR CD CONCENTRATION IN PLANT ORGANS…………………………………107 TABLE 3.5: SOIL BIOACCESSIBLE FRACTION OF CD ........................................................................................................... 109 TABLE 3.6 TWO TAILS PEARSON CORRELATION MATRIX ................................................................................................... 110 TABLE 4.1: BAZOCHES (BZC) AND NANTES (NTE) SOIL CHARACTERISTICS........................................................................... 116 TABLE 4.2: METALLOID RECOVERY RATE. AVERAGE ± STANDARD ERROR, % ........................................................................ 118 TABLE 4.3: LEAD (PB) AND ANTIMONY (SB) CONTENT IN BAZOCHES (BZC) AND NANTES (NTE) SOILS ..................................... 122 TABLE 4.4: SOIL PHYSICOCHEMICAL DATA (PH, %OM) AND PLANT (LEEK OR LETTUCE) PARAMETERS ....................................... 122 TABLE 4.5: RELATIVE ABUNDANCE OF FUNGI FROM GLOMEROMYCOTA PHYLUM IN THE BIO-AUGMENTATION SOLUTION.............. 125 TABLE 4.6: ARTIFICIAL COMMUNITY DESIGNED FOR ILLUMINA MISEQ ANALYSIS ................................................................... 135 TABLE 4.7: HUMAN BIOACCESSIBLE FRACTION OF PB AND SB IN LEAVES.............................................................................. 139 TABLE 4.8: SOIL BIOACCESSIBLE FRACTION OF PB AND SB ................................................................................................ 140 TABLE 4.9: TWO TAILS PEARSON CORRELATION MATRIX.................................................................................................. 141 TABLE 5.1: TRANSLOCATION FACTOR (TF) AND BIOACCUMULATION FACTOR (BF) IN DIFFERENT EDIBLE PLANTS.......................... 151 TABLE 5.2: BIOACCESSIBLE FRACTION OF SB IN EDIBLE ORGANS………………………………………………………………………………………152 TABLE 6.1: PEA PLANT AERIAL BIOMASS (G) .................................................................................................................. 163 TABLE 6.2: VARIATIONS OF THE IBRV2 INDEX IN CONTROL, SCG, AND SCGC TREATMENTS .................................................... 163
1
Chapter 1. SCIENTIFIC CONTEXT: HOW AND WHY STUDY INORGANIC POLLUTION IN URBAN SOILS?
To follow the charter of thesis from the University Paul Sabatier of Toulouse, the following chapter is preceded by a summarized French version, with references to the figures and tables present in the English version. For the whole introduction, you can skip to page 9. You will find here summarized information as a frame of the following investigation work. Why do we study heavy metal at the soil-microorganism-plant interface? Which are the risks for urban and peri-urban gardeners? How can one manage a contaminated soil when the will is to use it for food production? These are some of the questions raised here. At the end of each part, you will find a If you want more! section, with specific literature to go further in one or another field of interest as it is not exhaustive. As antimony has been much less studied, a focus has been added for this element about its bioavailability to edible plants (Section 1.3).
Heavy metal group, Pierart, 2016
What do you want? Heavy metal, heavy metal! Judas Priest, Heavy Metal, Ram It Down
Chapter 1 – Scientific context
2
1.1. Introduction générale Métaux et métalloïdes, origines, flux et dangers Tous les éléments traces métalliques et métalloïdes (ETM) sont naturellement présents dans la croûte continentale en proportions généralement faibles mais variables (Gao et al., 1998). La seule présence d'un ETM ne suffit pas à définir une zone comme contaminée. L'origine et la quantité du métal doivent être prises en compte, tout comme sa dangerosité. Les cycles biogéochimiques des ETM sont influencés, de façon rapide (Kim et al., 2014), par les rejets dans l'environnement d’origines naturelles (activité volcanique, érosion hydrique et éolienne du sol) et anthropique depuis la révolution industrielle (Catinon et al., 2011), (Figure 1.1). Les substances chimiques (de synthèse ou d’origine naturelle) accompagnent nos sociétés humaines depuis des siècles avec leurs avantages (fabrication d’outils, de médicaments, etc.) et leurs inconvénients (intoxication au plomb, effets secondaires graves de certains médicaments, etc.). Ces dernières années, la réglementation concernant la production, l’utilisation et les émissions dans l’environnement des substances chimiques s’est renforcée (règlement européen REACH1 et règlement Français des ICPE2 par exemple). Le « Global Harmonized System » s’est également mis en place à l’échelle de la planète afin d’assurer la même information « environnement-santé » partout dans le monde pour une substance chimique donnée. On peut donc considérer que des progrès ont été faits en termes de prise de conscience sur les risques potentiels liés à l’utilisation des substances chimiques. Malgré tout, les méthodes de mesure de plus en plus sensibles permettent de détecter certaines pollutions historiques ainsi que des nouveaux contaminants, qualifiés alors d'émergents. Deux métaux lourds: cadmium (Cd) et plomb (Pb) et un métalloïde: l’antimoine (Sb) ont été particulièrement investigués. Le cadmium et le plomb ont été sélectionnés pour leur présence récurrente en tant que contaminants environnementaux / alimentaires, en raison de leur utilisation historique (et actuelle) dans de nombreux processus industriels. Le cadmium a augmenté de façon considérable dans notre alimentation ces 10 dernières années (+400%) tandis que les teneurs en Pb tendent à diminuer légèrement mais restent encore préoccupantes comme le montre l’évolution de leurs teneurs dans les aliments mise en évidence par l’ANSES (Agence nationale de sécurité sanitaire de l’alimentation, de l’environnement et du travail) dans deux évaluations totales de l’alimentation sur le territoire
1
REACH - Registration, Evaluation, Authorization and restriction of CHemicals
2
ICPE - Installations Classées pour la Protection de l'Environnement
Chapter 1 – Scientific context
3 Français. Les sources de Cd et Pb et leurs proportions ont été bien documentées, celles de Sb beaucoup moins (Figure 1.2). De façon générale, leur utilisation dans différents procédés industriels (batterie, retardateurs de flamme, pesticides et engrais) constitue la source majoritaire de ces éléments dans l’environnement. Dans les sols français, les teneurs en Cd et Pb ont été mesurées dans les horizons de surface par le Gis Sol (Groupement d’intérêt scientifique sol) au cours de la dernière décennie au travers du programme RMQS (Réseau de Mesure de la Qualité des Sols) (Figure 1.3). Cette étude n’a cependant pas porté sur l’antimoine. Des teneurs légales dans les aliments, les sols (dans le cadre de l’épandage de boues de stations d’épuration) et les eaux existent pour Cd et Pb (résumés dans le Tableau 1.1 pour Pb). Pour Sb, en dépit de son classement comme élément à haute toxicité, il n’existe pas de norme fixant la concentration limite admise dans l’alimentation. L’antimoine a été étudié ici en raison de risques émergents liés à son utilisation. En effet, ce dernier est de plus en plus détecté en zones urbaines et péri-urbaines ainsi que dans l’alimentation comme indiqué par l’évolution de ses teneurs entre les deux évaluations totales de l’alimentation réalisées par l’ANSES. Or, on manque encore d'information sur son comportement le long de la chaîne alimentaire. Le rôle des micro-organismes dans le transfert de ces polluants inorganiques entre le sol et les plantes est l'un des thèmes centraux de cette étude. La littérature traitant ce sujet existe pour Cd et Pb, mais les liens éventuels entre ces micro-organismes et la bioaccessibilité humaine de ces éléments n’avaient pas été étudiés. Les études et synthèses bibliographiques traitant du comportant de ces éléments à l’interface sol-plante sont nombreuses, mais les interactions avec les champignons mycorhiziens à arbuscules et les bioamendements tel que le lombricompost sont moins étudiées, particulièrement dans le cas de l’antimoine (Pierart et al., 2015, CHAPITRE 4). Gestion raisonnée des pollutions métalliques Alors que les surfaces des sols contaminés par des ETM persistants augmentent depuis la révolution industrielle, la réhabilitation des sols à usage résidentiel et agricole est désormais un défi environnemental et sanitaire majeur (Wong et al., 2006). Les stratégies d'assainissement sont nombreuses (Khan et al., 2004), comme résumé dans la Figure 1.6. Ces techniques sont principalement divisées en deux groupes selon que la contamination ciblée soit traitée sur place (in situ) ou à l'extérieur de la zone, dans un lieu spécialisé (ex situ). Les traitements ex situ, du fait de leur rapidité, sont particulièrement intéressants pour les lieux d'intérêt économique élevé (urbanisation, etc…). Cependant, ils passent par une phase
Chapter 1 – Scientific context
4 d'excavation des sols qui affecte de façon importante les écosystèmes locaux. Enfin, leur coût est généralement trop élevé pour être appliqué à de grandes surfaces. Les solutions in situ, comme la phytoremédiation ou la phytostabilisation, sont en principe moins chères et certainement meilleures d'un point de vue environnemental. Cependant, elles restent moins efficaces pour les taux élevés de contamination. L'utilisation de produits chimiques donne des résultats rapides, mais impacte aussi les écosystèmes, tandis que les solutions biologiques perturbent beaucoup moins l'environnement, mais requièrent un temps de dépollution beaucoup plus long. Enfin, pour de nombreux sites, une approche complémentaire est généralement développée sur la base d'un examen préalable des zones en fonction du degré de pollution. Dans les zones d'agriculture urbaine et péri-urbaine, la volonté principale des utilisateurs est de continuer à cultiver leurs terres, élément clé à considérer lors du choix du plan de gestion à mettre en place (Dumat et al., 2015). Par conséquent, la recherche et le développement de solutions (1) non-destructives (2) économiquement viables et (3) si possible, permettant l’accès au site en cours de traitement, fait partie des objectifs de la présente étude. Agriculture urbaine et biofertilisants/bioamendements L'agriculture urbaine et péri-urbaine (AUP) est l'acte de produire des aliments à l'intérieur ou à proximité immédiate des villes. Toutefois, l'AUP couvre un objectif plus large et son développement révèle également un rôle crucial dans le développement écologique, social et individuel (McClintock, 2010). Pour résumer brièvement, l'agriculture urbaine a commencé au 19ème siècle avec la révolution industrielle et l'exode rural qu’elle engendra (Boulianne, 2001). En effet, à cette époque les villes ont prévu des espaces arables pour les travailleurs, leur permettant de cultiver leur propre nourriture avec l'objectif de maintenir et de développer la puissance de travail et la productivité. Puis, au cours des deux guerres mondiales, et entre ces périodes, leur rôle était plus nettement alimentaire. Le boom économique qui a eu lieu au début des années 70 a transformé les habitudes de consommation en raison du développement de l'agriculture industrialisée telle qu’on la connait aujourd’hui. Dès lors, l’agriculture urbaine est devenue davantage récréative et paysagère, et a été partiellement délaissée par les citoyens. Cette période a perduré jusqu'à la dernière décennie, qui a marqué une rupture dans la perception de l'agriculture urbaine: actuellement, elle semble susciter l'intérêt en raison de la crise économique et plus profondément du rejet des modèles de développement économiques et urbains. L’agriculture urbaine est aujourd’hui un thème complexe et diversifié, un mot-clé regroupant de nombreux types de jardiniers et autant de lieux aux objectifs différents (production, lien social, loisirs, ...). Aujourd’hui, les projets d'agriculture urbaine et la littérature associée germent au moins aussi vite que les cultures elles-mêmes.
Chapter 1 – Scientific context
5 En France par exemple, l'agence nationale de la recherche a financé un programme de recherche « villes durables » de trois ans appelé JASSUR (ANR-12-VBDU-0011), comme acronyme de Jardins ASSociatifs URbains. L'objectif principal était d'y étudier les services fournis par les jardins urbains dans le développement durable des villes et également d’analyser les pollutions éventuelles ainsi que leur gestion. Le présent travail s’est déroulé dans le cadre de ce projet national et a été financé par l’ANR JASSUR. Les zones urbaines et péri-urbaines sont connues pour être des lieux souvent contaminés en raison de nombreuses activités anthropiques historiques ou plus récentes (Werkenthin et al., 2014). Par ailleurs, les citoyens sont généralement mal informés sur les potentiels risques de cultiver leur propre nourriture liés à la qualité des milieux (sols, eaux, air) et/ou la qualité des supports de cultures, amendements et fertilisants utilisés (Dumat et al., 2015). En effet, à l’échelle globale la qualité de l'air, de l'eau, du sol et de divers amendements organiques diminue en raison d’une augmentation significative des teneurs en contaminants organiques et inorganiques (Borrego et al., 2006). Les sols urbains sont soumis à une telle pression économique que les espaces dédiés aux projets d’agriculture urbaine sont souvent implantés sur d’anciennes friches industrielles, des sols très anthropisés, ou des lieux à proximité des industries et des axes de communication où aucun projet immobilier ne pourrait naitre. Par conséquent, la question de la qualité du sol, de l'eau et de l'air est essentielle à traiter de façon collective et transparente afin que les projets d’AUP jouent pleinement leurs rôles de vecteurs de santé et bien-être des populations et de réduction des inégalités écologiques. Par ailleurs, les agriculteurs et jardiniers urbains par leurs pratiques peuvent également améliorer ou dégrader la qualité de leurs productions et de leurs parcelles. En effet, la qualité et les quantités des divers fertilisants, amendements et traitements utilisés soulèvent des questions comme par exemple des problèmes de sur-fertilisation ou d’emploi de pesticides aux conséquences toxiques (pour lesquels l’agriculture bio n’est pas épargnée, du fait de l’écotoxicité du cuivre présent dans certaines substances autorisées par exemple). --Afin de recycler les déchets organiques et de développer des pratiques culturales biologiques, l'utilisation de fertilisants et amendements organiques ‘faits maison’ ou non tels que les microorganismes ou le compost est très courante en agriculture urbaine. Cependant, peu de littérature a été publiée concernant leur influence sur la mobilité des ETM à l'interface sol-plante, ce qui est l'objectif principal de la présente thèse, en particulier dans le cas de l’antimoine (polluant émergeant) mais aussi du plomb et du cadmium (très couramment observés en zones urbaines dans le monde). ---
Chapter 1 – Scientific context
6 Les champignons mycorhiziens à arbuscules (AMF) sont des microorganismes symbiotiques de plus de 94% des plantes à fleurs (Brundrett, 2009, Figure 1.8). Ils sont naturellement présents dans les sols et sont d’orse et déjà vendus comme biofertilisants du fait de leur capacité à solubiliser le phosphore, élément majeur de la croissance des plantes. Cependant, plusieurs études tendent à montrer leur rôle dans le transfert des métaux lourds des sols vers les plantes. Le compost peut être produit à partir de très nombreux résidus organiques et selon des procédés variables, ce qui modifie ses caractéristiques biophysicochimiques. Or, selon Moreno Flores (2007), l’utilisation de lombricompost en agriculture urbaine se développe, alors que ces matières organiques sont connues pour séquestrer/relarguer les métaux lourds en fonction de l’acidité du sol, du fait des liaisons ioniques en jeu (Gerritse and van Driel, 1984; Sauvé et al., 2000). Or, Les AMF sont connus pour affecter le pH du sol rhizosphérique (Hu et al., 2013), ce qui pourrait affecter la mobilité des ETM liés à la matière organique. Ces interactions sont donc au cœur de la présente étude. Enfin, le biochar (Figure 1.10) est actuellement très étudié pour ses nombreuses qualités physicochimiques en tant qu’amendement organique (Lehmann and Joseph, 2015). Dans le cas des sols contaminés en ETM, son utilisation a également révélé un bon potentiel de fixation de ces polluants (Paz-Ferreiro et al., 2014), dont l’efficacité varie principalement selon le processus de préparation (température, matériaux initiaux) (Uchimiya et al., 2011). C’est pourquoi nous nous sommes intéressés au rôle d’un biochar préparé à base de marc de café dans le transfert de l’antimoine vers les plantes comestibles. Gestion du risque sanitaire La teneur totale en contaminants dans les sols cultivés et les plantes n’est pas nécessairement un bon indicateur de leur toxicité. En effet, au cours de la digestion seule une fraction (dite bioaccessible) de ces contaminants est extraite et mise en solution dans le tractus digestif (Pascaud et al., 2014; Xiong et al., 2014a, 2014b). Cette fraction bioaccessible est ensuite de nouveau filtrée par la barrière intestinale, qui limite le passage de ces éléments vers le système sanguin (Figure 1.11). Pour étudier ces phénomènes en laboratoire (sans avoir à pratiquer des analyses sur des êtres vivants), des solutions d’extraction de synthèse ont été développées, (Denys et al., 2009) afin de simuler les processus de digestion, ainsi que les temps et températures physiologiques adaptés. Cette méthode a été standardisée et validée in vivo par le groupe de recherche européen sur la bioaccessibilité (BARGE) sous le nom d’Unified BARGE Method (UBM) (Foucault et al., 2013).
Chapter 1 – Scientific context
7 Qu’étudie-t-on et comment ? Les objectifs généraux de cette thèse étaient les suivants :
Évaluer la phytodisponibilité et la bioaccessibilité des ETM dont l’origine de la contamination diffère (géogénique vs anthropique), sur les plantes comestibles.
Étudier l'impact des champignons mycorhiziens à arbuscules et de la matière organique sur le transfert des ETM du sol vers les plantes (transfert, translocation et compartimentation).
Évaluer l'influence de la communauté microbienne sur le devenir des ETM à l'interface sol-microorganisme-plante.
Étudier l'influence de ces paramètres physico-chimiques et biologiques sur la bioaccessibilité humaine des ETM dans les sols et les organes comestibles des plantes, afin d’en évaluer le risque sanitaire.
La complexité des mécanismes impliqués dans le devenir des métalloïdes à l'interface solmicroorganisme-plante (s-μ-p) met en évidence la nécessité de mieux comprendre les rôles de chacun à travers une approche multidisciplinaire et multi-échelles basée sur la complémentarité
des
approches
de
biogéochimie,
agronomie,
génomique
et
(éco)toxicologie. Ce travail fait lien avec l'approche de (1) Leveque, (2014) sur l'écotoxicologie et la biosurveillance des sols contaminés par des ETM et (2) Xiong, (2015) sur le devenir de la pollution atmosphérique en ETM à l'interface air-plante. Pour étudier le transfert des ETM à l’interface s-µ-p ainsi que l'impact des micro-organismes et de la matière organique, nous avons développé plusieurs expériences organisées autour d’un gradient de complexité (Figure 1.12). En effet, les systèmes les plus simples produisent des résultats plus fondamentaux, sans beaucoup d'interactions entre paramètres, mais leur réalité sur le terrain nécessite d’être vérifiée. En outre, les essais sur sol réels (et non substrats) tentent d'aborder plus précisément la réalité du terrain, avec toutes les interactions qui peuvent s’y produire. Cependant, ces résultats sont généralement plus complexes à interpréter, même si le degré de confiance accordé est considéré comme supérieur.
Chapter 1 – Scientific context
8 Le présent manuscrit est organisé de la façon suivante : Le CHAPITRE 1 est une introduction contextuelle, recueil d’informations essentielles sur le thème scientifique traité dans cette thèse. Un manque de littérature sur la biodisponibilité de Sb dans les plantes comestibles et le rôle des AMF dans son transfert a été mis en évidence ; par conséquent, un focus traite ce sujet au travers d’un article publié, intitulé ‘’Antimony bioavailability: knowledge and research perspectives for sustainable agriculture’’ en seconde partie de ce premier chapitre. Ensuite, l’ensemble des méthodes et outils utilisés sont détaillés au CHAPITRE 2. Le manuscrit étant organisé comme une séquence cohérente de publications, certaines méthodes apparaîtront également dans les chapitres suivants, mais sous une forme condensée. Les principaux résultats sur le devenir du cadmium à l'interface s-μ-p sous différents traitements (bioaugmentation avec AMF, lombricompost) sur deux sols péri-urbains aux caractéristiques et histoires contrastées sont décrits au CHAPITRE 3. Celui-ci est présenté sous forme d’un article soumis, intitulé ‘’How do soil biofertilizers
and
organic
amendments
influence
Cd
phytoavailability and
human
bioaccessibility?’’. . La même expérience a également été utilisée pour étudier le devenir de Sb et Pb à l'interface s-μ-p, avec une approche plus détaillée de microscopie et d’analyse des communautés fongiques (CHAPITRE 4, un article en phase finale de rédaction avant soumission intitulé ‘’Pb and Sb accumulation influenced by arbuscular mycorrhizal fungi community and organic matter in a crop rotation Lactuca sativa L. –> Allium porrum L.’’). La complexité des systèmes a rendu l’interprétation délicate. Par conséquent, une approche expérimentale simplifiée traitant du rôle des AMF dans le transfert de Sb vers des plantes comestibles en hydroponie a été développée. Les résultats sont développés dans le CHAPITRE 5. Jusqu'à présent, l'impact de Sb sur l'activité enzymatique du sol (exsudats racinaires, microbiens et activité microbienne interne) en relation avec l'addition de biochar n'a pas été décrit à ce jour. C’est pourquoi nous avons abordé ces mécanismes dans le CHAPITRE 6, au travers de l'étude de l'effet du biochar de marc de café sur le transfert solplante de Sb. Tous ces résultats et questionnements sont ensuite discutés et mis en perspectives dans le CHAPITRE 7 avant une conclusion finale (CHAPITRE 8).
Chapter 1 – Scientific context
9
1.2. Metal(loid) soil contamination and pollution 1.2.1. Terminology and definition, what are we talking about? All of the trace metals and metalloids (TM) occur naturally in the continental crust in small but variable proportions (Gao et al., 1998). The only presence of an element isn’t sufficient to classify these areas as ‘contaminated’. The origin and quantity of the metal need to be taken into account to define whether or not it is a contaminant. According to the FAO, there is a difference to be made between contamination and pollution. Indeed, “Pollution (is) the introduction by man, directly or indirectly, of substances or energy into the (…) environment (…) resulting in such deleterious effects as harm to living resources, hazards to human health. Contamination, on the other hand, is the presence of elevated concentrations of substances in the environment above the natural background level for the area and for the organism”3. For instance, a positive geochemical anomaly means naturally high amount of metal in a soil, such as for urban gardens in Nantes (France) which are enriched with lead from the mother rock. However, this semantic distinction is rarely done because terms are inverted and the substance origin isn’t always easy to trace.
1.2.2. Why Cadmium, Lead and Antimony need to be studied in urban soils? Among the whole periodic table, we focused on two heavy metal: cadmium (Cd) and lead (Pb) and one metalloid: antimony (Sb). These elements were studied because their concentration in food was shown to increase between two recent studies performed by the ANSES in France (Agence nationale de sécurité sanitaire de l’alimentation, de l’environnement et du travail). Indeed, it showed that Cd increased up to 400%, Pb decreased a little but its concentrations remained of concern and Sb content began to increase due to its emerging use. Indeed, the latter is being more and more detected in urban and peri-urban areas while a critical lack of information on its behavior along food chain exists. The role of microorganisms in the transfer of these inorganic pollutants between soil and plants is one of the central themes of our study. Literature dealing with this topic exist for Cd and Pb, but nothing about the eventual links between these microorganisms and TM human bioaccessibility. Moreover, very few data has been published for Sb, which is why a part of this thesis was focused on a review of Sb biogeochemistry and bioavailability (CHAPTER 1 – Section 1.3) (Pierart et al., 2015).
3
http://www.fao.org/docrep/x5624e/x5624e04.htm#1.1 contamination or pollution
Chapter 1 – Scientific context
10
The biogeochemical cycles of TM generate releases in the environment which can be both natural (volcanic activity, hydric and aeolian soil erosion) and anthropic (industrial activities), the latter being generally the most important (Catinon et al., 2011) and the fastest dispersion pathway (Kim et al., 2014) (Figure 1.1).
Figure 1.1: Biogeochemical cycle of TM, adapted from Tremel & Feix, 2005
Sources of Cd and Pb have been estimated in France. But, as such detailed information does not exist for Sb (Figure 1.2), it is estimated that its use in fire retardant, battery manufacture, brake linings and mining processes are the major Sb sources. However, Sb can also reach agricultural soils through lead arsenate pesticides application, since it is present as a contaminant in these metal ores (Wagner et al., 2003).
Figure 1.2: Proportion of major contamination sources for TM entrance in arable lands. Adapted from Repères. Sols et environnement, Chiffres Clés, 2015.
Chapter 1 – Scientific context
11 Facing these contaminations, worldwide regulation is highly heterogeneous, with loose regulation in some countries while in Europe for example, the release in the environment of major TM contaminant is being controlled (Xiong, 2015). Since 2006, the European REACH regulation (Registration, Evaluation, Authorization and restriction of CHemicals) classified some of them (Cd, Pb, Ni, As, Hg) as Substances of Very High Concern requiring a life cycle monitoring by industrials and communication towards citizens (EC 1907/20064).
1.2.3. Cadmium: a highly mobile carcinogenic element An extensive review of Cd behavior and toxicity at the soil-plant interface has been published by Shahid et al (Shahid et al., 2016); here are some summarized data showing the needs to study it: cadmium is naturally present in small quantity in the continental crust, being the 65th most abundant element within the periodic table. Its industrial exploitation always comes as a by-product, mostly in Zinc refining process. Figure 1.3: Cadmium content in French soils. In mg.kg-1 at 0-30cm depth, between 2000 and 2009. Adapted from foot note 5
Its concentration in natural soil ranges between 0.1 and 1.1 mg.kg-1 soil (Shahid et al., 2016).
In European agricultural soils, it has been estimated to range between 0.06 and 0.6 ppm (Salminen et al., 2005). However, in the case of soil developed above sedimentary rocks or subjected to recurrent Cd-phosphate fertilizers (Schroeder and Balassa, 1963) and sewage sludge amendment, Cd content can easily reach more than 15 mg.kg-1. In French soils, Cd content has been monitored on surface horizons by the Gis Sol organism5 during the last decade through the RMQS 6 program with a concentration range of 0.02 to 5.5 mg.kg-1 (Figure 1.3). Cd causes strong deleterious effects on living organisms such as kidney disorder and increased probability of bone fractures (Järup, 2003). Since 1993, the CIRC (French International Centre for Cancer Investigation) classified Cd as a group 1 harmful element (carcinogenic for human being). Cd hazard is of major concern because of its relatively high mobility in soil and water systems (Beesley et al., 2010). Indeed, its phytoavailability is high
4
http://eur-lex.europa.eu/legal-content/EN/TXT/?uri=CELEX%3A02006R1907-20140410
5
http://www.statistiques.developpement-durable.gouv.fr/lessentiel/ar/272/1122/contamination-sols-elements-traces.html Réseau de Mesure de la Qualité des Sols – connected to European ENVASSO (Environmental Assessment of Soil for Monitoring) 6
Chapter 1 – Scientific context
12 with a relatively weak bondage to clays, but strong affinity to OM (Prokop et al., 2003). For non-smoking people, the major source of Cd exposure has been estimated to be food diet (90%) (EFSA, 2009). For example, horticultural crops such as lettuce can present a high Cd accumulation in edible parts when cultivated both in contaminated soil and in spiking experiment (Peris et al., 2007; Zorrig and El Khouni, 2013). Cd is also found in cereals but in lower concentrations (Denaix et al., 2010). Cd concentration has been limited in drinking water to 5 µg.L-1 (INERIS, 2007), in agricultural soil (where sewage sludge are willing to be spread) to 2 mg.kg-1 and in leafy and stem/root vegetables to 0.2 and 0.1 mg.kg-1 fresh weight by the European directive EC1881/2006 because of its toxicity. But, this threshold might be lowered in the upcoming years according to recent discussions from the European commission (Nguyen et al., 2013).
1.2.4. Lead: a major contaminant widely present in urban soils Lead (Pb) is a post-transition metal belonging to the carbon group for which four stable isotopes are found in the environment. Although Pb can occur naturally in the environment through alteration of a rich mother rock, its presence in the environment
is
predominantly
due
to
anthropogenic activities such as mining, smelting, battery manufacture and past (but intense) use of leaded petrol until 2000 (Lim et al., 2013). Pb content in soil is highly variable, but it is Figure 1.4: Lead content in soil. In mg.kg-1 at 030cm depth, between 2000 and 2009. Adapted from: see foot note 4
present in almost all compartments of the biosphere: in a natural and undisturbed soil, Pb content ranges between 2 and 60 mg.kg-1
(Pettinelli, n.d.). However, local geochemical anomaly and industrial processes can increase its presence to more than 1 000 mgPb.kg-1. In France, the RMQS estimated that Pb content in soil ranged between 3 and 624 mgPb.kg-1 (Figure 1.4), but intense local contamination (~ 40 000mg.kg-1) exists as shown for instance by Leveque in 2014 (Leveque, 2014). Indeed, the RMQS specification requires the sampling areas either to be a natural soil or arable lands (i.e. it excludes anthropic soils such as industrial areas which are usually the more contaminated).
Chapter 1 – Scientific context
13 Lead is one of the most measured contaminant in the environment because of numerous industrial activities. As for Cd, ingestion might be the principal exposure way for Pb accumulation in living organisms, followed by dust/particles inhalation. Lead intoxication is usually called saturnism with nerve, brain and kidney diseases (Navas-Acien et al., 2009). Actually, it is classified 2B by the CIRC (potentially carcinogenic for human beings). Lead presents a lower mobility than Cd at the soil-water interface and generally binds more strongly to mineral surfaces (such as phosphates) than to soil organic matters (Quenea et al., 2009). Its speciation and mobility depend on iron and aluminum oxi-hydroxide contents (Dumat et al., 2001) and as for most of trace elements, pH is one of the major factors of influence in soil (Cecchi, 2008; Leveque, 2014). Hence, plant and microorganism exudates can affect Pb mobility and phytoavailability (Khan, 2005; Lin et al., 2004). Lead accumulation by plant can be high, with no general pattern: some plants such as Allium cepa L. accumulate in root (Wierzbicka, 1987) while other translocate Pb to their leaves, such as maize (Huang and Cunningham, 1996). These characteristics, linked with Pb elevated toxicity, led to set up legal thresholds for Pb in food products and drinking water (Table 1.1). For soils, in France, only sewage sludge inputs present legal threshold for cultivated soils, but due to the bioavailability concept, no legal threshold values were fixed for the other contexts. Table 1.1: Legal threshold of Pb in drinking water, soil, and aliments. Adapted from Cecchi (2008)
Maximal threshold
Law (Source) Drinking water (µg.L-1) Decree 2003-461 & 2003-462 (2003) EU Directive 98/83/CE (1998) Directive drinking water quality (1996) US EPA
AFNOR NFU 44-041 CE/466/2001
France European Union World health Organization Soil (mg.kg-1)
Play areas Other France, agricultural soil (when sewage sludges are willing to be spread)
Aliments (mg.kg-1 fresh weight)
Fruit juice Oil & Fat, Vegetables (except leafy vegetables, Brassicaceae, aromatics, mushroom), Fruits (except small fruits & small berries) Wines, small fruits & small berries, cereals, leguminous crops and vegetables leafy vegetables, Brassicaceae, aromatics, mushroom
Chapter 1 – Scientific context
10 400 1200 100 0.05 0.1 0.2 0.3
14
1.2.5. Antimony: emerging metalloid; emerging risks? From the Latin Stibnium, Antimony (Sb) is a metalloid from the nitrogen group. It has been given such a name because it can only be found combined with other elements (Anti-monos = opposite to solitude). It is mostly present in two stable isotopic forms
Sb (57.36%) and
121
Sb
123
(42.64%). Antimony’s concentration in earth crust has been estimated to range between 0.20.3 mg.kg-1. Its background concentrations in Figure 1.5: Antimony, an alloy in ammunitions, http://www.lab-initio.com/
uncontaminated soil vary between 90%) of three macro-fungi (Agaricus campestris, Amanita muscaria, and Trametes gibbosa) from Sb-contaminated water has also been reported, but further investigation on metal-binding mechanisms is still needed [137]. Concerning the relationship between mycorrhizal fungi and Sb in soils, one study has been reported on ectomycorrhizal fungi [101]. These organisms, as well as endomycorrhizal fungi, are already known as metal(loid) hyperaccumulators [138]. In their study, the authors sampled fungi on tailing piles and slag dumps (old As/Sb mining sites), and found no major differences for Sb concentration between ectomycorrhizal and saprobic fungi. Interestingly, among all their samples Sb content in the soil was higher than in fruit bodies, which could indicate that mycorrhizal fungi play a barrier role against this metalloid. However, the case of some ectomycorrhizal fungi (Chalciporus piperatus and various Suillus) able to accumulate Sb up to 103 mg kg.1 is also mentioned. This suggests that these genera possess a specific biological metabolism to mobilize and concentrate Sb from the soil, while Sb is generally present in species with poor solubility (cf. §2.2, [57]). How then do some mycorrhizal fungi influence Sb speciation in the soil compartment? What about the reactivity of these newly formed Sb species under the influence of mycorrhizal fungi? Other recent studies found (CH3 )3 Sb and another unidentified Sb species in some herbaceous plants [51], suggesting the role of the microbial community in the synthesis and transfer of these compounds. As stated earlier, it is well-documented that herbaceous plants generally develop more endomycorrhizal symbioses (such as AMF), suggesting the role of AMF in the biosynthesis and transfer
Chapter 1 – Scientific context
27 228
A. Pierart et al. / Journal of Hazardous Materials 289 (2015) 219–234
Fig. 1. Mycorrhizal role in Antimony (Sb) transfer from soil to plants. [?] Represents the actual mechanisms to be elucidated. Sb regroups the different Sb oxidative states and species.
of (CH3 )3 Sb to herbaceous plants. Fig. 1 presents the current state of knowledge of the possible ways for Sb to gain entry from soil to plants, either when associated with mycorrhizal fungi or without these organisms. ‘Sb’ refers without distinction to the various Sb species which have been found in soil and soil water, because not enough data exist about specific pathways for any Sb species. The different possible fluxes of Sb from soil to both plants and fungi are represented by arrows. As shown in Fig. 1, and summarized in this review, portions of these mechanisms are already known [39,88], but others have not yet been described (mostly the entirely of the fungal pathway). Nothing is known about how mycorrhizal fungi either absorb, adsorb and/or transform Sb at the soil–fungal–plant interface. 4.3. Biofertilizers in agriculture With the development of biological agriculture, arbuscular mycorrhizal fungi are now produced and sold in almost every garden center, both for agriculture and casual gardeners, as biofertilizers [139]. As mycorrhizal symbiosis is known to affect different physiological parameters, such as stomatal conductance and fruit development [140–143], it might participate in increasing the entry of metal(loid)s through stomata (i.e., leaves) and fruits. Consequently, in some cases, these biofertilizers could also be factors in the increase of metal(loid) uptake by plants [144]. Therefore, research needs to be conducted, to determine if most fungi able to methylate As have the same capability with regard to Sb, especially in the case of AMF, which could be used as a barrier between edible plants and soil on Sb-contaminated soils. Such results would also allow conclusions to be drawn as to whether or not the knowledge we already have about the relationship between AMF and As is transferable to Sb compounds, and to what extent. 4.4. Bioaccumulation by the soil fauna In addition to their key role in soil fertility, earthworms, as the major living organisms in soils, influence metal(loid) behavior in
soil through bioturbation [145]. In the case of Sb, Nannoni et al. [145] concluded that soil ingestion is the predominant means of exposure and absorption (Pearson correlation (PC) between [Sb] in earthworms and Sb extractable fraction = 0.88, p < 0.001). Nevertheless, they also indicated that skin penetration is not negligible (PC = 0.62, p < 0.05). In their experiment, total Sb concentration in earthworms varied from 0.04 to1.1 mg kg−1 (on clean and contaminated soils, respectively). High Sb concentrations could also cause morphological abnormalities and low activity in Perionyx excavates [96]. Such inhibitory effects on earthworms might cause a loss of fertility. In the case of Sb, the BAF is very low, indicating that, for earthworms, the total Sb concentration in the soil is not a good predictor of their possible contamination, while the extractable fraction seems to fit this role better. It also indicates that these species do not accumulate Sb intensively from the environment, so that Sb will not spread and accumulate through food webs via these organisms. Moreover, as shown for other metal(loid)s, such as Pb, Cu, Cd, Zn, Cr, Co, and Ni [18,52], earthworms can modify metal bioavailability in soils. For example, earthworm activity on a contaminated soil led to a 46% increase in Cd and Pb in lettuce leaves, owing to improved soil–plant transfer [41]. As earthworms are mainly interested in soil organic matter, the same authors also discussed Sb–soil organic matter interactions. Eisenia fetida has also been shown to biotransform As without excreting it after exposure, until its death [146]. This led to a decline in the As concentration in the soil during this period, but no data was given about As speciation or transfer when these organisms die and decompose in the soil. Such effects have not yet been demonstrated for Sb. Fig. 2 represents the actual state of knowledge about Sb behavior in soil–earthworm systems with excreted castings. It shows that such organisms can absorb Sb and further change its bioavailability, but the Sb species involved have not yet been clearly identified. Typically, the bioaccumulation of Sb by soil microfauna varies with their habitat and species type. Antimony concentrations in terrestrial invertebrates (30.4 mg kg−1 dry wt.) are generally higher than those in aquatic invertebrates (5.2 mg kg−1 dry wt.) and
Chapter 1 – Scientific context
28 A. Pierart et al. / Journal of Hazardous Materials 289 (2015) 219–234
Fig. 2. Antimony bioaccumulation in earthworms.
229
Original earthworm drawing (www.onf.fr). BAFSb = bioaccumulation factor of Sb.
amphibians (2.3 mg kg−1 dry wt.) [147]. Some terrestrial invertebrate such as earthworms have already been shown to accumulate Sb [54]. Such disparity could be explained by differences in Sb compartmentation (in particular, soil organic matter influence) or speciation and in diet of these living organisms (soil consumption, water filtration, etc.). The same authors [147] also reported high Sb concentrations in Acrida chinensis and Pheretima aspergillum: 17.3 and 43.6 mg kg−1 , respectively, within 1 km of an Sb mining area. Pauget et al. [148] noted the high availability of Sb to snails, at three industrially impacted sites in northern France. They studied Sb accumulation kinetics from the soil into these organisms, and showed that CaCl2 extract concentrations were the best predictors of Sb bioaccumulation. As noted earlier, organic matter (OM) participates in Sb availability, and the relatively high level of OM in their study area (up to 10%) could partially explain such results. Up to the present, there is no data available concerning Sb accumulation in other living macro/meso-organisms in the soil compartment. It is, therefore, difficult to precisely identify the possible pathway of Sb through the food chain. 5. Human health risks assessment People working with Sb compounds are subject to Sb inhalation, mostly antimony trioxide. For the rest of the population, food represents the predominant source of Sb exposure. Its absorption through the digestive tract has been estimated between 5 and 20% of the total Sb content ingested [149]. In 1992, urban dwellers were exposed to about 60–460 ng day−1 through inhalation [150]. Nowadays, this value has certainly increased with the increase of Sb uses (since 1992) around the world. 5.1. Food-chain biomagnification Antimony biomagnification has not been investigated much as yet, but some studies have intended to evaluate this parameter [151,152]. However, these studies did not discover any evidence of Sb accumulation across the food chain, but their intention was not necessarily to assess trophic linkage. Therefore, this conclusion is not guaranteed. In any case, biomagnification only considers the
xenobiotic accumulation in an organism through its daily alimentation [153]. For example, as shown earlier (cf. §4.2), some fungi have been identified as Sb hyperaccumulators [101], with concentration exceeding 1400 mg kg−1 in the fruiting body of C. piperatus. Consequently, they can become Sb sources in the food web, through slugs, then ducks or chickens, and then humans (or directly to human beings in the case of mushroom consumption). Nevertheless, these organisms are more sensitive to soil contamination than aerial deposition because of the short fruiting period (10–14 day) in which they could accumulate metalloids from dusts. However, it would be necessary to consider other sources of Sb exposure (inhalation, skin contact, etc.), and to focus not only on the biomagnification factor but also on the bioaccumulation factor, which takes into account every kind of exposure. Investigations need to be performed on the transfer of Sb from cereals, such as wheat and maize (which are known to accumulate Sb up to 700 mg kg−1 ), to poultry and livestock, in order to give clues about the risk of transfer through the plant–meat–human food chain. However, little risk of Sb bioaccumulation seems to exist for herbivores, even when their grassland diet suffered major contamination near an Sb smelter [154]. Indeed, rabbits and voles presented relatively high levels of Sb in different organs (0.30 and 0.68 mg–kg−1 DW in voles and rabbit Liver respectively) when they fed in contaminated sites ( poireau), et de l'organe (racine > feuille) pour l'ensemble des ETM étudiés. En outre, la phytoaccumulation des ETM est à la fois spécifique au type d’élément mais aussi à leur origine (anthropique >> géogénique), sauf pour le plomb dont l'accumulation était similaire dans les deux sols étudiés. Les effets observés de l’ajout d’AMF et OM sur la phytoaccumulation des ETM sont complexes, du fait des interactions présentées ci-dessus. La plupart des résultats ont seulement mis en évidence des tendances ; soulignant la nécessité de renforcer cette étude par un travail de terrain, ou éventuellement avec d’avantage de réplicas afin de renforcer les analyses statistiques. Les résultats les plus pertinents ont montré que l'ajout d’AMF augmente le Cd dans la laitue sur sol sablo-limoneux, mais n'a aucun effet sur sol sableux, ce qui était à l'opposé des résultats obtenus pour le Pb. Par ailleurs, l'ajout d’AMF n'a eu aucun effet sur la phytoaccumulation de Sb. Par contre, l'ajout de lombricompost a eu tendance à diminuer les ETM dans les plantes, mais la plupart des résultats étaient seulement des tendances, à l'exception de la phytoaccumulation du Cd dans le poireau cultivé sur sol sablo-limoneux, qui a diminué de manière significative avec l'ajout de lombricompost. Pour la première fois, nos résultats montrent que l’apport couplé d’AMF et de lombricompost semble diminuer les ETM dans les parties comestibles (en diminuant le facteur de translocation). Malheureusement, les designs expérimentaux mis en place ne l’ont pas mis en évidence de façon significative, excepté pour le cadmium dans les poireaux cultivés sur sol sableux. En outre, ces variations d'accumulation ont généralement été observées majoritairement dans les racines, ce qui suggère que les ETM étaient soient stockés dans ces organes, soit liés aux parois racinaires et fongiques. Cette hypothèse a été renforcée par des observations en microscopie électronique à transmission de résidus de sol liés à ces structures, même après lavage des racines. Par conséquent, pour réduire l’exposition humaine, peler les légumes racines pourrait être une recommandation appropriée dans le cas de contamination aux ETM plutôt que de simplement les laver.
Chapter 8 – Conclusion and perspectives
196 Nous avons montré que la bioaccessibilité des ETM dans le sol a été fortement influencée par l'origine des contaminants (anthropique > géogénique), et pour la première fois que que l’ajout d’AMF n'a aucun effet sur ces fractions. A l’opposé, le lombricompost a augmenté la bioaccessibilité du Cd dans le sol (mais n'a eu aucun effet évident sur Pb et Sb). Ceci suggère que les ETM récemment libérés dans l’environnement sont d’avantage bioaccessibles lors de la digestion que les contaminants métalliques anciens. Ces différences de bioaccessibilité étaient corrélées à la mobilité des ETM dans le sol et leur solubilité (disponibilité dans la solution du sol), ce qui pourrait indiquer que leur spéciation chimique influence directement leur bioaccessibilité. Dans nos conditions, nous avons confirmé que la bioaccessibilité des ETM dans les plantes dépend du type d'élément comme suit: Cd (~ 90%) > Pb (~ 60%) >> Sb (~ 20%). L’ajout de lombricompost n'a eu aucun effet sur ces fractions dans les plantes. Pour la première fois, nous rapportons que l’apport d’AMF augmente la bioaccessibilité de Sb. Un effet plante a également été mis en évidence, avec une bioaccessibilité plus élevée dans la laitue que dans le poireau. De plus, l'origine de la contamination a influencé sur sa bioaccessibilité dans les plantes (plus élevée dans les sols présentant une contamination anthropique). Cependant, un effet plante semble aussi intervenir car ces variations ont été mesurées seulement dans la laitue. En hydroponie, le système a été simplifié afin de limiter les éventuelles interactions avec le sol. Nous avons observé comment la spéciation chimique de Sb a influencé la façon dont le mélange d'espèces fongiques (isolées à partir des sols contaminés précédemment étudiés) pourrait participer à sa phytoaccumulation. Toutefois, la réponse était spécifique de la plante : augmentation de l'accumulation en ETM chez la carotte indépendamment de l'espèce chimique ; diminution chez la laitue avec une influence de la forme chimique de Sb à l'échelle de l'organe (la mycorhization n'a eu aucun effet sur KSb dans les feuilles alors qu'elle a diminué l’accumulation de Sb2O3). Par ailleurs, nous montrons ici pour la première fois que l'ajout d’AMF a augmenté à la fois le facteur de translocation et le facteur de bioaccumulation, excepté dans les laitues traitées avec Sb2O3 dans lesquelles nous avons observé une diminution significative du facteur de translocation. Ces résultats suggèrent une absorption et un stockage sélectifs dépendant de la spéciation chimique des ETM plutôt que seulement leur degré d’oxydation. Des biotransformations dans la plante pourraient également modifier la spéciation des ETM et leur bioaccessibilité.
Chapter 8 – Conclusion and perspectives
197 La diversité des communautés fongiques du sol a joué un rôle clé dans la mobilité des ETM et leur phytoaccumulation décrite précédemment. Cette composition semble dépendre du sol et des plantes (elle peut également varier de façon saisonnière d’après la littérature, ce qui complique encore d’avantage l'ensemble du système). Par ailleurs, des risques ont été mis en évidence quant à l’ajout de lombricompost et la bioaugmentation avec des propagules d’AMF locales. En effet, ces deux pratiques ont diminué la diversité fongique associée aux plantes. Par conséquent, ils doivent être utilisés avec précaution dans le cas de contamination en ETM dans les sols cultivés. L’influence de Sb sur l'activité microbienne du sol (étudiée grâce à des dosages d’activité enzymatiques) a été forte. En effet, le dopage du sol en Sb a augmenté de façon significative l'indice IBRv2 révélant d'importantes variations d'activités enzymatiques. Cet effet semble dépendre de la concentration en Sb, avec une influence plus élevée à des teneurs faibles en Sb. Ces résultats originaux mettent en évidence l'utilisation potentielle de l'indice IBRv2 dans le développement des valeurs standards de qualité des sols. Pour la première fois, cette étude montre comment l'utilisation de biochar de marc de café a efficacement atténué la toxicité de Sb par rapport aux traitements SCG (marc de café cru) et sans matière organique. Cependant, certaines enzymes étaient encore affectées par la contamination en Sb (carboxylestérase, uréase et phosphatase acide). Par ailleurs, ce bioamendement a été bien colonisé par les champignons et bactéries du sol, et il a conservé une activité enzymatique microbienne (vivante) après stérilisation. Ces résultats illustrent son potentiel pour la remédiation des sols dégradés, en tant que matériau offrant un abri efficace aux microorganismes du sol tout en étant une source de nutriments favorables à leur développement.
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198 PERSPECTIVES Le présent travail, au travers de ses conclusions, limites et biais, a généré de nombreuses perspectives: Le dispositif expérimental mis en place Tout d'abord, comme il a été discuté au chapitre 7, nous nous sommes concentrés ici sur deux modèles simplifiés (hydroponie et sol réel) dans des expériences en pots. Il serait hautement souhaitable, sinon obligatoire de mettre en place des protocoles similaires en plein champ pour éviter les biais des expérimentations en pot affectant de nombreux paramètres physiologiques tels que la croissance des plantes, des champignons et de la communauté microbienne, et éventuellement le métabolisme des plantes comme l'absorption des ETM par exemple. Cependant, pour évaluer le rôle individuel de chaque acteur, des modèles encore plus simples, tels que les systèmes hairy-root présentés au chapitre 5, sont aussi des outils intéressants. La plante utilisée A plusieurs reprises, nous avons montré un effet plante sur la mobilité et l’accumulation des ETM. Cela pourrait être dû aux espèces utilisées, mais aussi aux cultivars et à la séquence de culture elle-même (laitue poireau). Pour déterminer l'effet prédominant (s'il y en a un), il pourrait être intéressant de comparer l'ordre inverse avec les mêmes plantes, mais aussi d'autres espèces et cultivars. Cela générerait des données intéressantes à ajouter aux bases de données existantes telles que BAPPET4. Les biofertilisants et bioamendements appliqués Comme cela a été développé dans les chapitres 4 et 7, nous avons montré que la mobilité et la phytoaccumulation observées des ETM sont dépendantes à la fois de la communauté fongique et de l’origine de la matière organique (selon des études antérieures). Par conséquent, des recherches supplémentaires seraient nécessaires pour caractériser les effets des biofertilisants et bioamendements commerciaux les plus couramment utilisés dans les jardins urbains. Cela permettrait d’élaborer des stratégies de gestion raisonnée dans les zones urbaines contaminées et au-delà. De plus, nous nous sommes concentrés ici sur les AMF en tant que principaux acteurs du sol dans les processus biogéochimiques afin de simplifier le système et évalué leur propre rôle. Cependant de nombreuses études montrent que les communautés bactériennes rhizosphériques peuvent influencer la mobilité des ETM et des
4
BAPPET - BAse de données sur les teneurs en Eléments Traces métalliques de Plantes Potagères
Chapter 8 – Conclusion and perspectives
199 éléments nutritifs à l'interface sol-plante. Les nouvelles techniques de séquençage haut débit tels que l’Illumina MiSeq présentent un grand potentiel pour étudier l’ensemble des communautés de micro-organismes dans le sol, avec l'inconvénient toutefois que les bases de données taxonomiques sont encore incomplètes et que l'efficacité de la méthode ellemême semble dépendre des espèces microbiennes étudiées. Utiliser les mathématiques comme un outil d’aide à la décision Même s'il y a encore un long chemin avant d'être en mesure de représenter mathématiquement la complexité de chaque scénario sans travail de terrain et collecte de données préalables, la modélisation de ces processus biologiques présente un intérêt considérable pour limiter les études de terrain coûteuses... Lorsqu’ils seront assez robustes, ces outils pourront être utilisés dans les processus de décision lors du développement de projets d’AUP par exemple. Le biochar, un vaste champ de recherche Les résultats du chapitre 6 ont montré le potentiel du biochar de marc de café comme stimulateur et abri propice aux microorganismes. Ceci ouvre la voie à la recherche de méthodes pour activer ce biochar avec des micro-organismes sélectionnés, capables de solubiliser ou stabiliser les ETM, les pesticides ou d'autres contaminants afin de créer un outil recyclé utilisable dans les processus de phytoremédiation ou phytostabilisation.
--- Le mot de la faim --Finalement, la meilleure des recommandations pourrait être de compléter le conseil santé mangez au moins cinq fruits et légumes par jours … par … d’origines différentes, pour limiter l’ingestion répétée de contaminants.
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201
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PIERART Antoine
TITLE: Role of arbuscular mycorrhizal fungi and bioamendments in the transfer and human bioaccessibility of Cd, Pb, and Sb contaminant in vegetables cultivated in urban areas ABSTRACT: Urban agriculture (UA) and pollution are two worlds more inter-connected every day, creating one of the main challenges of sustainable cities as persistent metal(loid) contamination increases as much as the interest for urban agriculture. Biofertilizers and bioamendments used in UA (arbuscular mycorrhizal fungi, compost, and biochar) can influence the mobility of contaminants in soil. This study aims to better understand the fate of anthropic or geogenic, major (Cd, Pb) and emerging (Sb), inorganic contaminants in soil-plant-biofertilizer systems and their human bioaccessibility. While contaminant mobility in soil is affected by biofertilizers, their origin influences also their bioaccessibility. The fungal community seems crucial in this phenomenon but is impacted by compost addition. Hence, using these biofertilizers in contaminated soils has to be thought wisely because of the multiple interactions affecting contaminant’s phytoavailability. -KEYWORDS: Mycorrhization, Trace Elements, Transfer, Bioaccessibility, Enzymatic Activity, Biochar
AUTEUR : PIERART Antoine -DIRECTRICES DE THESE : DUMAT Camille et SEJALON-DELMAS Nathalie LIEU ET DATE DE SOUTENANCE : Toulouse
TITRE : Rôle des champignons mycorhiziens à arbuscules et des bioamendments dans le transfert et la bioaccessibilité humaine de Cd, Pb et Sb vers les végétaux cultivés en milieu urbain. RESUME : Pollution et agriculture urbaine (AU) sont deux mondes interconnectés soumettant les villes au défi de la durabilité, dans un contexte où la pollution aux metalloïdes augmente au moins autant que l’intérêt pour l’agriculture urbaine. Les biofertilisants / bioamendements utilisés en AU (champignons mycorhiziens à arbuscules, compost, biochar) peuvent influencer la mobilité des polluants du sol. Cette étude vise à mieux comprendre le devenir de contaminants inorganiques géogéniques et anthropiques, majeurs (Cd, Pb) ou émergents (Sb), dans des systèmes sol-plante-biofertilisant et leur bioaccessibilité pour l’homme. Si la mobilité des polluants est modifiée par les biofertilisants, le type de source influence aussi leur bioaccessibilité. La communauté fongique semble cruciale dans ces phénomènes mais est impactée par l’ajout de compost. Ainsi, l’utilisation de ces biofertilisants sur sol pollué est à raisonner du fait des interactions multiples affectant la phytodisponibilité des polluants. -MOTS-CLES : Mycorhization, Eléments traces métalliques, Transfert, Bioaccessibilité, Activité enzymatique, Biochar
DISCIPLINE ADMINISTRATIVE : Ecologie Fonctionnelle
INTITULE ET ADRESSE DU LABORATOIRE : Ecolab – Laboratoire d’Ecologie Fonctionnelle et Environnement Av. de l’Agrobiopôle BP 32607 Auzeville Tolosane France
