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Exposure to different arsenic species drives the establishment of iron- and sulfur-oxidizing bacteria on rice root iron plaques

  • Sarah Zecchin
  • Milena Colombo
  • Lucia CavalcaEmail author
Original Paper
  • 64 Downloads

Abstract

Iron- and sulfur-oxidizing bacteria inhabiting rice rhizoplane play a significant role on arsenic biogeochemistry in flooded rice paddies, influencing arsenic translocation to rice grains. In the present study, the selective pressure of arsenic species on these microbial populations was evaluated. Rice roots from continuously flooded plants were incubated in iron sulfide (FeS) gradient tubes and exposed to either arsenate or arsenite. The biomass developed in the visible iron-oxidation band of the enrichments was analyzed by Scanning Electron Microscopy and Energy-Dispersive Spectroscopy (SEM–EDS) and the bacterial communities were characterized by 16S rRNA gene sequencing. Different Proteobacteria communities were selected depending on exposure to arsenate and arsenite. Arsenate addition favored the versatile iron-oxidizers Dechloromonas and Azospira, associated to putative iron (hydr)oxide crystals. Arsenite exposure decreased the diversity in the enrichments, with the development of the sulfur-oxidizer Thiobacillus thioparus, likely growing on sulfide released by FeS. Whereas sulfur-oxidizers were observed in all treatments, iron-oxidizers disappeared when exposed to arsenite. These results reveal a strong impact of different inorganic arsenics on rhizospheric iron-oxidizers as well as a crucial role of sulfur-oxidizing bacteria in establishing rice rhizosphere communities under arsenic pressure.

Keywords

Iron-oxidizing bacteria Sulfur-oxidizing bacteria Arsenic Rice rhizosphere Rice iron plaques Gradient tubes 

Notes

Funding

This work was supported by Ministry of University and Research program PRIN [Grant Number 2010JBNLJ7-004]; Sarah Zecchin was awarded of a PhD fellowship by the University of Milan.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Abraham W, Strömpl C, Meyer H, Lindholst S, Moore ERB, Christ R, Vancanneyt M, Tindall BJ, Bennasar A, Smit J, Tesar M (1999) Phylogeny and polyphasic taxonomy of Caulobacter species. Proposal of Maricaulis gen. nov. with Maricaulis maris (Poindexter) comb. nov. as the type species, and emended description of the genera Brevundimonas and Caulobacter. Int J Syst Bacteriol 49:1053–1073PubMedGoogle Scholar
  2. Achenbach LA, Michaelidou U, Bruce RA, Fryman J, Coates JD (2001) Dechloromonas agitata gen. nov., sp. nov. and Dechlorosoma suillum gen. nov., sp. nov., two novel environmentally dominant (per)chlorate-reducing bacteria and their phylogenetic position. Int J Syst Evol Microbiol 51:527–533PubMedGoogle Scholar
  3. Achour AR, Bauda P, Billard P (2007) Diversity of arsenite transporter genes from arsenic-resistant soil bacteria. Res Microbiol 158:128–137PubMedGoogle Scholar
  4. Bachate SP, Cavalca L, Andreoni V (2009) Arsenic-resistant bacteria isolated from agricultural soils of Bangladesh and characterization of arsenate-reducing strains. J Appl Microbiol 107:145–156PubMedGoogle Scholar
  5. Bay Y, Muller DB, Srinivas G, Garrido-Oter R, Potthoff E, Rott M, Dombrowski N, Munch PC, Spaepen S, Remus-Emsermann M, Huttel B, McHardy AC, Vorholt JA, Schulze-Lefert P (2015) Functional overlap of the Arabidopsis leaf and root microbiota. Nature 528(7582):364–369Google Scholar
  6. Boden R, Cleland D, Green PN, Katayama Y, Uchino Y, Murrell JC, Kelly DP (2012) Phylogenetic assessment of culture collection strains of Thiobacillus thioparus, and definitive 16S rRNA gene sequences for T. thioparus, T. denitrificans, and Halothiobacillus neapolitanus. Arch Microbiol 194(3):187–195PubMedGoogle Scholar
  7. Cavalca L, Corsini A, Zaccheo P, Andreoni V, Muyzer G (2013) Microbial transformations of arsenic: perspectives for biological removal of arsenic from water. Future Microbiol 86:753–768Google Scholar
  8. Coenye T, Vancanneyt M, Falsen E, Swings J, Vandamme P (2003) Achromobacter insolitus sp. nov. and Achromobacter spanius sp. nov., from human clinical samples. Int J Syst Evol Microbiol 53:1819–1824PubMedGoogle Scholar
  9. Colmer TD (2003) Long-distance transport of gases in plants: a perspective on internal aeration and radial oxygen loss from roots. Plant Cell Environ 26:17–36Google Scholar
  10. Commission regulation (EC) No 2015/1006 of 25 June 2015 amending Regulation (EC) No 1881/2006 as regard maximum levels of inorganic arsenic in foodstuffs. OJ L 161:14–16Google Scholar
  11. Crook MB, Mitra S, Ané JM, Sadowsky MJ, Gyaneshwar P (2013) Complete genome sequence of the Sesbania symbiont and rice growth-promoting endophyte Rhizobium sp. strain IRBG74. Genome Announc 1(6):e00934-13PubMedPubMedCentralGoogle Scholar
  12. Dahl C, Friedrich C, Kletzin A (2008) Sulfur oxidation in prokaryotes. In: eLS, (ed)Google Scholar
  13. Das S, Chou ML, Jean JS, Liu CC, Yang HJ (2016) Water management impacts on arsenic behavior and rhizosphere bacterial communities and activities in a rice agro-ecosystem. Sci Total Environ 542:642–652PubMedGoogle Scholar
  14. de Zamaroczy M, Delorme F, Elmerich C (1989) Regulation of transcription and promoter mapping of the structural genes for nitrogenase (nifHDK) of Azospirillum brasilense Sp7. Mol Gen Genet 220(1):88–94PubMedGoogle Scholar
  15. Dixit S, Hering JG (2003) Comparison of arsenic(V) and arsenic(III) sorption onto iron oxide minerals: implications for arsenic mobility. Environ Sci Technol 37(2003):4182–4189PubMedGoogle Scholar
  16. Dubinina GA, Sorokina AY (2014) Neutrophilic lithotrophic iron-oxidizing prokaryotes and their role in the biogeochemical processes of the iron cycle. Microbiology 83:1–14Google Scholar
  17. Edgar RC (2004) MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinform 5:113Google Scholar
  18. Emerson D (2012) Biogeochemistry and microbiology of microaerobic Fe(II) oxidation. Biochem Soc Trans 40:1211–1216PubMedGoogle Scholar
  19. Emerson D, Moyer C (1997) Isolation and characterization of novel iron-oxidizing bacteria that grow at circumneutral pH. Appl Environ Microbiol 63(12):4784–4792PubMedPubMedCentralGoogle Scholar
  20. Emerson D, Fleming EJ, McBeth JM (2010) Iron-oxidizing bacteria: an environmental and genomic perspective. Ann Rev Microbiol 64:561–583Google Scholar
  21. Emerson D, Field E, Chertkov O, Davenport K, Goodwin L, Munk C, Nolan M, Woyke T (2013) Comparative genomics of freshwater Fe-oxidizing bacteria: implications for physiology, ecology, and systematics. Front Microbiol 4:1–17Google Scholar
  22. European Food Safety Authority (2010) Scientific opinion of lead in food. EFSA J 8(4):1570Google Scholar
  23. European Food Safety Authority (2012) Cadmium dietary exposure in the European population. EFSA J 10(1):2551Google Scholar
  24. European Food Safety Authority (2014) Dietary exposure to inorganic arsenic in the European population. EFSA J 12:3597Google Scholar
  25. Fisher JC, Wallschläger D, Planer-Friedrich B, Hollibaugh JT (2008) A new role for sulfur in arsenic cycling. Environ Sci Technol 42:81–85PubMedGoogle Scholar
  26. Friedrich CG, Bardischewsky F, Rother D, Quentimeier A, Fischer J (2005) Prokaryotic sulfur oxidation. Curr Opin Microbiol 8:253–259PubMedGoogle Scholar
  27. Giloteaux L, Holmes DE, Williams KH, Wrighton KC, Wilkins MJ, Montgomery AP, Smith JA, Orellana R, Thompson CA, Roper TJ, Long PE, Loveley DR (2013) Characterization and transcription of arsenic respiration and resistance genes during in situ uranium bioremediation. ISME J 7:370–383PubMedGoogle Scholar
  28. Gosh W, Dam B (2009) Biochemistry and molecular biology of lithotrophic sulfur oxidation by taxonomically and ecologically diverse bacteria and archaea. FEMS Microbiol Rev 33:999–1043Google Scholar
  29. Gray JS, Birmingham JM, Fenton JI (2010) Got swimming dots in your cell culture? Identification of Achromobacter as a novel cell culture contaminant. Biologicals 38(2):273–277PubMedGoogle Scholar
  30. Hanert HH (1992) The prokaryotes: the genus Gallionella. Springer, New York, pp 4082–4088Google Scholar
  31. Hassan Z, Sultana M, Westerhoff HV, Khan SI, Röling WFM (2015) Iron cycling potentials of arsenic-contaminated groundwater in Bangladesh as revealed by enrichment cultivation. Geomicrobiol J 33(9):779–792Google Scholar
  32. Hedrich S, Schlömann M, Johnson DB (2011) The iron-oxidizing Proteobacteria. Microbiology 157:1551–1564PubMedGoogle Scholar
  33. Henrici AT, Johnson DE (1935) Studies of freshwater bacteria: II. Stalked bacteria, a new order of Schizomycetes 1. J Bacteriol 30(1):61PubMedPubMedCentralGoogle Scholar
  34. Hohmann C, Winkler E, Morin G, Kappler A (2010) Anaerobic Fe(II)-oxidizing bacteria show As resistance and immobilize As during Fe(III) mineral precipitation. Environ Sci Technol 44:94–101PubMedGoogle Scholar
  35. Hu Z, Yang Z, Xu C, Haneklaus S, Cao Z, Schnug E (2002) Effect of crop growth on the distribution and mineralization of soil sulfur fractions in the rhizosphere. J Plant Nutr Soil Sci 165:249–254Google Scholar
  36. Hu Z, Zhu Y, Li M, Zhang L, Cao Z, Smith FA (2007) Sulfur (S)-induced enhancement of iron plaque formation in the rhizosphere reduces arsenic accumulation in rice (Oryza sativa L.) seedlings. Environ Pollut 147:387–393PubMedGoogle Scholar
  37. Jia Y, Bao P, Zhu Y (2015) Arsenic bioavailability to rice plant in paddy soil: influence of microbial sulfate reduction. J Soil Sediments 15:1960–1967Google Scholar
  38. Jin L, Kim KK, Baek SH, Lee ST (2011) Kaistia geumhonensis sp. nov. and Kaistia dalseonensis sp. nov., two members of the class Alphaproteobacteria. Int J Syst Evol Microbiol 61(11):2577–2581PubMedGoogle Scholar
  39. Joint FAO/WHO Expert Committee on Food Additives (2010) Joint FAO/WHO expert committee on food additives seventy-third meeting. World Health Organization, GenevaGoogle Scholar
  40. Kämpfer P, Young CC, Arun AB, Shen FT, Jäckel U, Rossello-Mora R, Lai W, Rekha PD (2006) Pseudolabrys taiwanensis gen. nov., sp. nov., an alphaproteobacterium isolated from soil. Int J Syst Evol Microbiol 56(10):2469–2472PubMedGoogle Scholar
  41. Katsoyiannis IA, Zouboulis AI (2006) Use of iron- and manganese-oxidizing bacteria for the combined removal of iron, manganese and arsenic from contaminated groundwater. Water Qual Res J Can 41(2):117–129Google Scholar
  42. Kelly DP, Wood AP (2000) Confirmation of Thiobacillus denitrificans as a species of the genus Thiobacillus, in the b-subclass of the Proteobacteria, with strain NCIMB 9548 as the type strain. Int J Syst Evol Microbiol 50:547–550PubMedGoogle Scholar
  43. Kleinjan WE, de Keizer A, Janssen AJH (2003) Biologically produced sulfur. Top Curr Chem 230:167–188Google Scholar
  44. Kögel-Knabner I, Amelung W, Cao Z, Fiedler S, Frenzel P, Jahn R, Kalbitz K, Kölbl A, Schloter M (2010) Biogeochemistry of paddy soils. Geoderma 157:1–14Google Scholar
  45. Kojima H, Fukui M (2010) Sulfuricella denitrificans gen. nov., sp. nov., a sulfur-oxidizing autotroph isolated from a freshwater lake. Int J Syst Evol Microbiol 60(12):2862–2866PubMedGoogle Scholar
  46. Kucera S, Wolfe RS (1957) A selective enrichment method for Gallionella ferruginea. J Bacteriol 74(3):344PubMedPubMedCentralGoogle Scholar
  47. La Scola B, Birtles RJ, Mallet MN, Raoult D (1998) Massilia timonae gen. nov., sp. nov., isolated from blood of an immunocompromised patient with cerebellar lesions. J Clin Microbiol 36(10):2847–2852PubMedPubMedCentralGoogle Scholar
  48. Li HB, Singh RK, Singh P, Song QQ, Xing YX, Yang LT, Li YR (2017) Genetic diversity of nitrogen-fixing and plant growth promoting Pseudomonas species isolated from sugarcane rhizosphere. Front Microbiol 8:1268PubMedPubMedCentralGoogle Scholar
  49. Liu WJ, Zhu YG, Smith FA (2005) Effects of iron and manganese plaques on arsenic uptake by rice seedlings (Oryza sativa L.) grown in solution culture supplied with arsenate and arsenite. Plant Soil 277:127–138Google Scholar
  50. Ma R, Shen J, Wu J, Tang Z, Shen Q, Zhao FJ (2014) Impact of agronomic practices on arsenic accumulation and speciation in rice grain. Environ Pollut 194:217–223PubMedGoogle Scholar
  51. Mouchet P (1992) From conventional to biological removal of iron and manganese in France. J Am Water Works Assoc 84(4):158–166Google Scholar
  52. Muyzer G, Teske A, Wirsen CO, Jannasch HW (1995) Phylogenetic relationships of Thiomicrospira species and their identification in deep-sea hydrothermal vent samples by denaturing gradient gel electrophoresis of 16S rDNA fragments. Arch Microbiol 164(3):165–172PubMedGoogle Scholar
  53. Neumann G, Veeranagouda Y, Karegoudar TB, Sahin Ö, Mäusezahl I, Kabelitz N, Kappelmeyer U, Heipieper HJ (2005) Cells of Pseudomonas putida and Enterobacter sp. adapt to toxic organic compounds by increasing their size. Extremophiles 9(2):163–168PubMedGoogle Scholar
  54. Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O'Hara RB, Simpson GL, Solymos P, Stevens MHH, Szoecs E, Wagner H (2017) vegan: Community Ecology Package. https://CRAN.R-project.org/package=vegan
  55. Oremland RS, Stolz JF (2005) Arsenic, microbes and contaminated aquifers. Trends Microbiol 13(2):45–49PubMedGoogle Scholar
  56. Pester M, Knorr K, Friedrich MW, Wagner M, Loy A (2012) Sulfate-reducing microorganisms in wetlands—fameless actors in carbon cycling and climate change. Front Microbiol 3:1–19Google Scholar
  57. Pielou EC (1966) Shannon’s formula as a measure of specific diversity: its use and misuse. Am Nat 100:463–465Google Scholar
  58. Poindexter JS (1964) Biological properties and classification of the Caulobacter group. Bacteriol Rev 28(3):231PubMedPubMedCentralGoogle Scholar
  59. Poindexter JS (2006) The prokaryotes: dimorphic prosthecate bacteria: the genera Caulobacter, Asticcacaulis, Hyphomicrobium, Pedomicrobium, Hyphomonas and Thiodendron. Springer, New York, pp 72–90Google Scholar
  60. Pokhrel D, Viraraghavan T (2009) Biological filtration for removal of arsenic from drinking water. J Environ Manag 90:1956–1961Google Scholar
  61. Quéméneur M, Heinrich-Salmeron A, Muller D, Lièvremont D, Jauzein M, Bertin PN, Garrido F, Joulian C (2008) Diversity surveys and evolutionary relationships of aoxB genes in aerobic arsenite-oxidizing bacteria. Appl Environ Microbiol 74(14):4567–4573PubMedPubMedCentralGoogle Scholar
  62. Rawlings DE (2005) Characteristics and adaptability of iron- and sulfur-oxidizing microorganisms used for the recovery of metals from minerals and their concentrates. Microb Cell Fact 4:1–15Google Scholar
  63. R Development Core Team (2008) R: a language and environment for statistical computing. Version 2.6.2 (2008-02-08). R foundation for statistical computing, Vienna, Austria. http://www.R-project.org/
  64. Reinhold-Hurek B, Hurek T (2000) Reassessment of the taxonomic structure of the diazotrophic genus Azoarcus sensu lato and description of three new genera and new species, Azovibrio restrictus gen. nov., sp. nov., Azospira oryzae gen. nov., sp. nov. and Azonexus fungiphilus gen. nov., sp. nov. Int J Syst Evol Microbiol 50(2):649–659PubMedGoogle Scholar
  65. Rinklebe J, Shaheen SM, Yu K (2016) Release of As, Ba, Cd, Cu, Pb, and Sr under pre-definite redox conditions in different rice paddy soils originating from the U.S.A. and Asia. Geoderma 270:21–32Google Scholar
  66. Rizwan M, Ali S, Adrees M, Rizvi H, Zia-ur-Rehman M, Hannan F, Qayyum MF, Hafeez F, Ok YS (2016) Cadmium stress in rice: toxic effects, tolerance mechanisms and management: a critical review. Environ Sci Pollut Res 23:17859–17879Google Scholar
  67. Roberts LC, Hug SJ, Ruettimann T, Billah MM, Khan AW, Rahman MT (2004) Arsenic removal with iron (II) and iron (III) in waters with high silicate and phosphate concentrations. Environ Sci Technol 38(1):307–315PubMedGoogle Scholar
  68. Seyfferth AL, Webb SM, Andrews JC, Fendorf S (2010) Arsenic localization, speciation, and co-occurrence with iron on rice (Oryza sativa L.) roots having variable Fe coatings. Environ Sci Technol 44(21):8108–8113PubMedGoogle Scholar
  69. Siddiqi MZ, Im WT (2016) Lysobacter pocheonensis sp. nov., isolated from soil of a ginseng field. Arch Microbiol 198:551–557PubMedGoogle Scholar
  70. Somenahally AC, Hollister EB, Loeppert RH, Yan W, Gentry TJ (2011) Microbial communities in rice rhizosphere altered by intermittent and continuous flooding in fields with long-term arsenic application. Soil Biol Biochem 43:1220–1228Google Scholar
  71. Spanu A, Daga L, Orlandoni AM, Sanna G (2012) The role of irrigation techniques in arsenic bioaccumulation in rice (Oryza sativa L.). Environ Sci Technol 46:8333–8340PubMedGoogle Scholar
  72. Stanier RY, Palleroni NJ, Doudoroff M (1966) The aerobic pseudomonads a taxonomic study. Microbiology 43(2):159–271Google Scholar
  73. Stubner S, Wind T, Conrad R (1998) Sulfur oxidation in rice field soil: activity, enumeration, isolation and characterization of thiosulfate-oxidizing bacteria. Syst Appl Microbiol 21:569–578PubMedGoogle Scholar
  74. Sullivan RF, Holtman MA, Zylstra GJ, White JF, Kobayashi DY (2003) Taxonomic positioning of two biological control agents for plant diseases as Lysobacter enzymogenes based on phylogenetic analysis of 16S rDNA, fatty acid composition and phenotypic characteristics. J Appl Microbiol 94(6):1079–1086PubMedGoogle Scholar
  75. Takahashi Y, Minamikawa R, Hattori KH, Kurishima K, Kihou N, Yuita K (2004) Arsenic behavior in paddy fields during the cycle of flooded and non-flooded periods. Environ Sci Technol 38:1038–1044PubMedGoogle Scholar
  76. Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10:512–526PubMedGoogle Scholar
  77. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729PubMedPubMedCentralGoogle Scholar
  78. van Berkum P, Beyene D, Bao G, Campbell TA, Eardly BD (1998) Rhizobium mongolense sp. nov. is one of three rhizobial genotypes identified which nodulate and form nitrogen-fixing symbioses with Medicago ruthenica [(L.) Ledebour]. Int J Syst Bacteriol 48:13–22PubMedGoogle Scholar
  79. Vasilyeva LV, Omelchenko MV, Berestovskaya YY, Lysenko AM, Abraham WR, Dedysh SN, Zavarzin GA (2006) Asticcacaulis benevestitus sp. nov., a psychrotolerant, dimorphic, prosthecate bacterium from tundra wetland soil. Int J Syst Evol Microbiol 56(9):2083–2088PubMedGoogle Scholar
  80. Walczak AB, Yee N, Young LY (2018) Draft genome of Bosea sp. WAO an arsenite and sulfide oxidizer isolated from a pyrite rock outcrop in New Jersey. Stand Genomic Sci 13:6PubMedPubMedCentralGoogle Scholar
  81. Weiss JV, Emerson D, Backer SM, Megonigal JP (2003) Enumeration of Fe (II)-oxidizing and Fe (III)-reducing bacteria in the root zone of wetland plants: implications for a rhizosphere iron cycle. Biogeochemistry 64(1):77–96Google Scholar
  82. Weiss JV, Rentz JA, Plaia T, Neubauer SC, Merrill-Floyd M, Lilburn T, Bradburne C, Megonigal JP, Emerson D (2007) Characterization of neutrophilic Fe(II)-oxidizing bacteria isolated from the rhizosphere of wetland plants and description of Ferritrophicum radicicola gen. nov. sp. nov., and Sideroxydans paludicola sp. nov. Geomicrobiol J 24:559–570Google Scholar
  83. Wolin EA, Wolin M, Wolfe RS (1963) Formation of methane by bacterial extracts. J Biol Chem 238(8):2882–2886PubMedGoogle Scholar
  84. Wörner S, Zecchin S, Dan J, Hristova Todorova N, Loy A, Conrad R, Pester M (2016) Gypsum amendment to rice paddy soil stimulated bacteria involved in sulfur cycle but largely preserved the phylogenetic composition of the total bacterial community. Environ Microbiol Rep 8(3):413–423PubMedGoogle Scholar
  85. Xie CH, Yokota A (2005) Azospirillum oryzae sp. nov., a nitrogen-fixing bacterium isolated from the roots of the rice plant Oryza sativa. Int J Syst Evol Microbiol 55(4):1435–1438PubMedGoogle Scholar
  86. Yabuuchi E, Kawamura Y, Kosako Y, Ezaki T (1998) Emendation of genus Achromobacter and Achromobacter xylosoxidans (Yabuuchi and Yano) and proposal of Achromobacter ruhlandii (Packer and Vishniac) comb. nov., Achromobacter piechaudii (Kiredjian et al.) comb. nov., and Achromobacter xylosoxidans subsp. denitrificans (Rüger and Tan) comb. nov. Microbiol Immunol 42(6):429–438PubMedGoogle Scholar
  87. Yamaguchi N, Ohkura T, Takahashi Y, Maejima Y, Arao T (2014) Arsenic distribution and speciation near rice roots influenced by iron plaques and redox conditions of the soil matrix. Environ Sci Technol 48:1549–1556PubMedGoogle Scholar
  88. Ye X, Li H, Zhang L, Chai R, Tu R, Gao H (2018) Amendment damages the function of continuous flooding in decreasing Cd and Pb uptake by rice in acid paddy soil. Ecotoxicol Environ Saf 147:708–714PubMedGoogle Scholar
  89. Zargar K, Conrad A, Bernick DL, Lowe TM, Stolc V, Hoeft S, Oremland RS, Stolz J, Saltikov CW (2012) ArxA, a new clade of arsenite oxidase within the DMSO reductase family of molybdenum oxidoreductase. Environ Microbiol 14(7):1635–1645PubMedGoogle Scholar
  90. Zecchin S, Corsini A, Martin M, Romani M, Beone GM, Zanchi R, Zanzo E, Tenni D, Fontanella MC, Cavalca L (2017a) Rhizospheric iron and arsenic bacteria affected by water regime: implications for metalloid uptake by rice. Soil Biol Biochem 106:129–137Google Scholar
  91. Zecchin S, Corsini A, Martin M, Cavalca L (2017b) Influence of water management on the active root-associated microbiota involved in arsenic, iron, and sulfur cycles in rice paddies. Appl Microbiol Biotechnol 101:6725–6738PubMedGoogle Scholar
  92. Zhao FJ, Ma JF, Meharg AA, McGrath SP (2009) Arsenic uptake and metabolism in plants. New Phytol 181:777–794PubMedGoogle Scholar
  93. Zhu YG, Williams PN, Meharg AA (2008) Exposure to inorganic arsenic from rice: a global health issue? Environ Pollut 154:169–171PubMedGoogle Scholar

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Authors and Affiliations

  1. 1.Dipartimento di Scienze per gli Alimenti, la Nutrizione e l’Ambiente (DeFENS)Università degli Studi di MilanoMilanItaly

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