Microbial mediated arsenic biotransformation in wetlands
Si-Yu Zhang, Paul N. Williams, Jinming Luo, Yong-Guan Zhu
Microbial mediated arsenic biotransformation in wetlands
Distribution and behavior of arsenic in wetland are summarized.
Macro-scale and micro-scale processes in wetland are reviewed.
Microbes act as the switch in determining wetland as a source or sink of arsenic.
Environmental factors affecting arsenic microbial biotransformation are summarized.
Arsenic (As) is a pervasive environmental toxin and carcinogenic metalloid. It ranks at the top of the US priority List of Hazardous Substances and causes worldwide human health problems. Wetlands, including natural and artificial ecosystems (i.e. paddy soils) are highly susceptible to As enrichment; acting not only as repositories for water but a host of other elemental/chemical moieties. While macro-scale processes (physical and geological) supply As to wetlands, it is the micro-scale biogeochemistry that regulates the fluxes of As and other trace elements from the semi-terrestrial to neighboring plant/aquatic/atmospheric compartments. Among these fine-scale events, microbial mediated As biotransformations contribute most to the element’s changing forms, acting as the ‘switch’ in defining a wetland as either a source or sink of As. Much of our understanding of these important microbial catalyzed reactions follows relatively recent scientific discoveries. Here we document some of these key advances, with focuses on the implications that wetlands and their microbial mediated transformation pathways have on the global As cycle, the chemistries of microbial mediated As oxidation, reduction and methylation, and future research priorities areas.
Arsenic / Wetland / Microbes / Switch
[1] |
Oremland R S, Stolz J F. The ecology of arsenic. Science, 2003, 300(5621): 939–944
CrossRef
Pubmed
Google scholar
|
[2] |
Zhu Y G, Yoshinaga M, Zhao F J, Rosen B P. Earth abides arsenic biotransformations. Annual Review of Earth and Planetary Sciences, 2014, 42(0): 443–467
CrossRef
Pubmed
Google scholar
|
[3] |
Bhattacharya P, Welch A H, Stollenwerk K G, McLaughlin M J, Bundschuh J, Panaullah G. Arsenic in the environment: Biology and Chemistry. Science of the Total Environment, 2007, 379(2-3): 109–120
CrossRef
Pubmed
Google scholar
|
[4] |
Bentley R, Chasteen T G. Microbial methylation of metalloids: arsenic, antimony, and bismuth. Microbiology and Molecular Biology Reviews, 2002, 66(2): 250–271
CrossRef
Pubmed
Google scholar
|
[5] |
Silbergeld E K, Nachman K. The environmental and public health risks associated with arsenical use in animal feeds. Annals of the New York Academy of Sciences, 2008, 1140(1): 346–357
CrossRef
Pubmed
Google scholar
|
[6] |
Murray L A, Raab A, Marr I L, Feldmann J. Biotransformation of arsenate to arsenosugars by Chlorella vulgaris. Applied Organometallic Chemistry, 2003, 17(9): 669–674
CrossRef
Google scholar
|
[7] |
Moore J W, Ramamoorthy S. Heavy metals in natural waters: applied monitoring and impact assessment. New York: Springer Science & Business Media, 2012
|
[8] |
Zedler J B, Kercher S. Wetland resources: status, trends, ecosystem services, and restorability. Annual Review of Environment and Resources, 2005, 30(1): 39–74
CrossRef
Google scholar
|
[9] |
Keddy P A. Wetland Ecology: Principles and Conservation. Cambridge: Cambridge University Press, 2010
|
[10] |
Chmura G L, Anisfeld S C, Cahoon D R, Lynch J C. Global carbon sequestration in tidal, saline wetland soils. Global Biogeochemical Cycles, 2003, 17(4): 1–12
CrossRef
Google scholar
|
[11] |
Wang S, Wang Y, Feng X, Zhai L, Zhu G. Quantitative analyses of ammonia-oxidizing Archaea and bacteria in the sediments of four nitrogen-rich wetlands in China. Applied Microbiology and Biotechnology, 2011, 90(2): 779–787
CrossRef
Pubmed
Google scholar
|
[12] |
Qin J, Lehr C R, Yuan C, Le X C, McDermott T R, Rosen B P. Biotransformation of arsenic by a Yellowstone thermoacidophilic eukaryotic alga. Proceedings of the National Academy of Sciences of the United States of America, 2009, 106(13): 5213–5217
CrossRef
Pubmed
Google scholar
|
[13] |
Bhakta J N, Munekage Y. Spatial distribution and contamination status of arsenic, cadmium and lead in some coastal shrimp (Macrobrachium rosenbergii) farming ponds of Viet Nam. Pacific Journal of Science and Technology, 2009, 11: 606–615
|
[14] |
Wang S, Mulligan C N. Occurrence of arsenic contamination in Canada: sources, behavior and distribution. Science of the Total Environment, 2006, 366(2-3): 701–721
CrossRef
Pubmed
Google scholar
|
[15] |
Chapman P M, Wang F, Janssen C, Persoone G, Allen H E. Ecotoxicology of metals in aquatic sediments: binding and release, bioavailability, risk assessment, and remediation. Canadian Journal of Fisheries and Aquatic Sciences, 1998, 55(10): 2221–2243
CrossRef
Google scholar
|
[16] |
National Standard of PR China. National Standard of PR China Marine Sediment Quality (GB 18668–2002). Beijing: Standards Press of China, 2002 (in Chinese)
|
[17] |
Canadian Sediment Quality Guidelines for the Protection of Aquatic Life. Canadian Environmental Quality Guidelines (1999). Canadian Council of Ministers of the Environment Winnipeg, 2001
|
[18] |
Bai J, Xiao R, Zhang K, Gao H. Arsenic and heavy metal pollution in wetland soils from tidal freshwater and salt marshes before and after the flow-sediment regulation regime in the Yellow River Delta, China. Journal of Hydrology (Amsterdam), 2012, 450: 244–253
CrossRef
Google scholar
|
[19] |
Gorenc S, Kostaschuk R, Chen Z. Spatial variations in heavy metals on tidal flats in the Yangtze Estuary, China. Environmental Geology, 2004, 45(8): 1101–1108
CrossRef
Google scholar
|
[20] |
Wilkin R T, Ford R G. Arsenic solid-phase partitioning in reducing sediments of a contaminated wetland. Chemical Geology, 2006, 228(1): 156–174
CrossRef
Google scholar
|
[21] |
Kraus U, Wiegand J. Long-term effects of the Aznalcóllar mine spill-heavy metal content and mobility in soils and sediments of the Guadiamar River Valley (SW Spain). Science of the Total Environment, 2006, 367(2-3): 855–871
CrossRef
Pubmed
Google scholar
|
[22] |
Stroud J L, Khan M A, Norton G J, Islam M R, Dasgupta T, Zhu Y G, Price A H, Meharg A A, McGrath S P, Zhao F J. Assessing the labile arsenic pool in contaminated paddy soils by isotopic dilution techniques and simple extractions. Environmental Science & Technology, 2011, 45(10): 4262–4269
CrossRef
Pubmed
Google scholar
|
[23] |
Zhang S Y, Zhao F J, Sun G X, Su J Q, Yang X R, Li H, Zhu Y G. Diversity and abundance of arsenic biotransformation genes in paddy soils from southern China. Environmental Science & Technology, 2015, 49(7): 4138–4146
CrossRef
Pubmed
Google scholar
|
[24] |
Alam M, Ali M, Al-Harbi N A, Choudhury T R. Contamination status of arsenic, lead, and cadmium of different wetland waters. Toxicological and Environmental Chemistry, 2011, 93(10): 1934–1945
CrossRef
Google scholar
|
[25] |
Huq S I, Rahman A, Sultana N, Naidu R. Extent and Severity of Arsenic Contamination in Soils of Bangladesh. Fate of Arsenic in the Environment. Dhaka: Bangladesh University of Engineering and Technology, 2003, 69–84
|
[26] |
Huq S I, Shoaib J U M. Soils and humans. The Soils of Bangladesh. 2013, 125–129
|
[27] |
Lu Y, Adomako E E, Solaiman A R, Islam M R, Deacon C, Williams P N, Rahman G K, Meharg A A. Baseline soil variation is a major factor in arsenic accumulation in Bengal Delta paddy rice. Environmental Science & Technology, 2009, 43(6): 1724–1729
CrossRef
Pubmed
Google scholar
|
[28] |
Meharg A A, Rahman M M. Arsenic contamination of Bangladesh paddy field soils: implications for rice contribution to arsenic consumption. Environmental Science & Technology, 2003, 37(2): 229–234
CrossRef
Pubmed
Google scholar
|
[29] |
Williams P N, Zhang H, Davison W, Meharg A A, Hossain M, Norton G J, Brammer H, Islam M R. Organic matter-solid phase interactions are critical for predicting arsenic release and plant uptake in Bangladesh paddy soils. Environmental Science & Technology, 2011, 45(14): 6080–6087
CrossRef
Pubmed
Google scholar
|
[30] |
Polizzotto M L, Kocar B D, Benner S G, Sampson M, Fendorf S. Near-surface wetland sediments as a source of arsenic release to ground water in Asia. Nature, 2008, 454(7203): 505–508
CrossRef
Pubmed
Google scholar
|
[31] |
Meharg A A.Venomous Earth: How Arsenic Caused the World's Worst Mass Poisoning. London: Palgrave Macmillan Ltd., 2005
|
[32] |
Meharg A A, Zhao F J. Biogeochemistry of Arsenic in Paddy Environments. In Arsenic & Rice. 2012, 71–101
|
[33] |
Williams P N, Villada A, Deacon C, Raab A, Figuerola J, Green A J, Feldmann J, Meharg A A. Greatly enhanced arsenic shoot assimilation in rice leads to elevated grain levels compared to wheat and barley. Environmental Science & Technology, 2007, 41(19): 6854–6859
CrossRef
Pubmed
Google scholar
|
[34] |
Huang H, Jia Y, Sun G X, Zhu Y G. Arsenic speciation and volatilization from flooded paddy soils amended with different organic matters. Environmental Science & Technology, 2012, 46(4): 2163–2168
CrossRef
Pubmed
Google scholar
|
[35] |
Jia Y, Huang H, Zhong M, Wang F H, Zhang L M, Zhu Y G. Microbial arsenic methylation in soil and rice rhizosphere. Environmental Science & Technology, 2013, 47(7): 3141–3148
Pubmed
|
[36] |
Williams P N, Lei M, Sun G, Huang Q, Lu Y, Deacon C, Meharg A A, Zhu Y G. Occurrence and partitioning of cadmium, arsenic and lead in mine impacted paddy rice: Hunan, China. Environmental Science & Technology, 2009, 43(3): 637–642
CrossRef
Pubmed
Google scholar
|
[37] |
Zhao F J, Harris E, Yan J, Ma J, Wu L, Liu W, McGrath S P, Zhou J, Zhu Y G. Arsenic methylation in soils and its relationship with microbial arsM abundance and diversity, and as speciation in rice. Environmental Science & Technology, 2013, 47(13): 7147–7154
Pubmed
|
[38] |
Zhang S Y, Zhao F J, Sun G X, Su J Q, Yang X R, Li H, Zhu Y G. Diversity and abundance of arsenic biotransformation genes in paddy soils from southern China. Environmental Science & Technology, 2015, 49(7): 4138–4146
CrossRef
Pubmed
Google scholar
|
[39] |
Mestrot A, Feldmann J, Krupp E M, Hossain M S, Roman-Ross G, Meharg A A. Field fluxes and speciation of arsines emanating from soils. Environmental Science & Technology, 2011, 45(5): 1798–1804
CrossRef
Pubmed
Google scholar
|
[40] |
Grimalt J O, Ferrer M, Macpherson E. The mine tailing accident in Aznalcollar. Science of the Total Environment, 1999, 242(1–3): 3–11
CrossRef
Pubmed
Google scholar
|
[41] |
Mateo R, Taggart M A, Green A J, Cristófol C, Ramis A, Lefranc H, Figuerola J, Meharg A A. Altered porphyrin excretion and histopathology of greylag geese (Anser anser) exposed to soil contaminated with lead and arsenic in the Guadalquivir Marshes, southwestern Spain. Environmental Toxicology and Chemistry, 2006, 25(1): 203–212
CrossRef
Pubmed
Google scholar
|
[42] |
Yamaguchi N, Nakamura T, Dong D, Takahashi Y, Amachi S, Makino T. Arsenic release from flooded paddy soils is influenced by speciation, Eh, pH, and iron dissolution. Chemosphere, 2011, 83(7): 925–932
CrossRef
Pubmed
Google scholar
|
[43] |
Xu X Y, McGrath S P, Meharg A A, Zhao F J. Growing rice aerobically markedly decreases arsenic accumulation. Environmental Science & Technology, 2008, 42(15): 5574–5579
CrossRef
Pubmed
Google scholar
|
[44] |
Cummings D E, Caccavo F, Fendorf S, Rosenzweig R F. Arsenic mobilization by the dissimilatory Fe(III)-reducing bacterium Shewanella alga BrY. Environmental Science & Technology, 1999, 33(5): 723–729
CrossRef
Google scholar
|
[45] |
Takahashi Y, Minamikawa R, Hattori K H, Kurishima K, Kihou N, Yuita K. Arsenic behavior in paddy fields during the cycle of flooded and non-flooded periods. Environmental Science & Technology, 2004, 38(4): 1038–1044
CrossRef
Pubmed
Google scholar
|
[46] |
Harvey C F, Swartz C H, Badruzzaman A B, Keon-Blute N, Yu W, Ali M A, Jay J, Beckie R, Niedan V, Brabander D, Oates P M, Ashfaque K N, Islam S, Hemond H F, Ahmed M F. Arsenic mobility and groundwater extraction in Bangladesh. Science, 2002, 298(5598): 1602–1606
CrossRef
Pubmed
Google scholar
|
[47] |
Bostick B C, Chen C, Fendorf S. Arsenite retention mechanisms within estuarine sediments of Pescadero, CA. Environmental Science & Technology, 2004, 38(12): 3299–3304
CrossRef
Pubmed
Google scholar
|
[48] |
Lizama A K, Fletcher T D, Sun G. Removal processes for arsenic in constructed wetlands. Chemosphere, 2011, 84(8): 1032–1043
CrossRef
Pubmed
Google scholar
|
[49] |
Morse J W. Interactions of trace metals with authigenic sulfide minerals: implications for their bioavailability. Marine Chemistry, 1994, 46(1): 1–6
CrossRef
Google scholar
|
[50] |
Saulnier I, Mucci A. Trace metal remobilization following the resuspension of estuarine sediments: Saguenay Fjord, Canada. Applied Geochemistry, 2000, 15(2): 191–210
CrossRef
Google scholar
|
[51] |
Kirk G. The Biogeochemistry of Submerged Soils. London: John Wiley & Sons, 2004
|
[52] |
Ye J, Rensing C, Rosen B P, Zhu Y G. Arsenic biomethylation by photosynthetic organisms. Trends in Plant Science, 2012, 17(3): 155–162
CrossRef
Pubmed
Google scholar
|
[53] |
Maguffin S C, Kirk M F, Daigle A R, Hinkle S R, Jin Q. Substantial contribution of biomethylation to aquifer arsenic cycling. Nature Geoscience, 2015, 8(4): 290–293
CrossRef
Google scholar
|
[54] |
Drahota P, Falteisek L, Redlich A, Rohovec J, Matoušek T, Cepička I. Microbial effects on the release and attenuation of arsenic in the shallow subsurface of a natural geochemical anomaly. Environmental Pollution, 2013, 180: 84–91
CrossRef
Pubmed
Google scholar
|
[55] |
Mumford A C, Barringer J L, Benzel W M, Reilly P A, Young L Y. Microbial transformations of arsenic: mobilization from glauconitic sediments to water. Water Research, 2012, 46(9): 2859–2868
CrossRef
Pubmed
Google scholar
|
[56] |
Ohtsuka T, Yamaguchi N, Makino T, Sakurai K, Kimura K, Kudo K, Homma E, Dong D T, Amachi S. Arsenic dissolution from Japanese paddy soil by a dissimilatory arsenate-reducing bacterium Geobacter sp. OR-1. Environmental Science & Technology, 2013, 47(12): 6263–6271
Pubmed
|
[57] |
Slyemi D, Bonnefoy V. How prokaryotes deal with Arsenic. Environmental Microbiology Reports, 2012, 4(6): 571–586
Pubmed
|
[58] |
Silver S, Phung L T. Genes and enzymes involved in bacterial oxidation and reduction of inorganic arsenic. Applied and Environmental Microbiology, 2005, 71(2): 599–608
CrossRef
Pubmed
Google scholar
|
[59] |
Rosen B P, Liu Z. Transport pathways for arsenic and selenium: a minireview. Environment International, 2009, 35(3): 512–515
CrossRef
Pubmed
Google scholar
|
[60] |
Mukhopadhyay R, Rosen B P, Phung L T, Silver S. Microbial arsenic: from geocycles to genes and enzymes. FEMS Microbiology Reviews, 2002, 26(3): 311–325
CrossRef
Pubmed
Google scholar
|
[61] |
Stolz J F, Basu P, Santini J M, Oremland R S. Arsenic and selenium in microbial metabolism. Annual Review of Microbiology, 2006, 60(1): 107–130
CrossRef
Pubmed
Google scholar
|
[62] |
Jia Y, Huang H, Chen Z, Zhu Y G. Arsenic uptake by rice is influenced by microbe-mediated arsenic redox changes in the rhizosphere. Environmental Science & Technology, 2014, 48(2): 1001–1007
CrossRef
Pubmed
Google scholar
|
[63] |
Cai L, Yu K, Yang Y, Chen B W, Li X D, Zhang T. Metagenomic exploration reveals high levels of microbial arsenic metabolism genes in activated sludge and coastal sediments. Applied Microbiology and Biotechnology, 2013, 97(21): 9579–9588
CrossRef
Pubmed
Google scholar
|
[64] |
Chang J S, Yoon I H, Lee J H, Kim K R, An J, Kim K W. Arsenic detoxification potential of aox genes in arsenite-oxidizing bacteria isolated from natural and constructed wetlands in the Republic of Korea. Environmental Geochemistry and Health, 2010, 32(2): 95–105
CrossRef
Pubmed
Google scholar
|
[65] |
Macur R E, Jackson C R, Botero L M, McDermott T R, Inskeep W P. Bacterial populations associated with the oxidation and reduction of arsenic in an unsaturated soil. Environmental Science & Technology, 2004, 38(1): 104–111
CrossRef
Pubmed
Google scholar
|
[66] |
Afkar E, Lisak J, Saltikov C, Basu P, Oremland R S, Stolz J F. The respiratory arsenate reductase from Bacillus selenitireducens strain MLS10. FEMS Microbiology Letters, 2003, 226(1): 107–112
CrossRef
Pubmed
Google scholar
|
[67] |
Saltikov C W, Newman D K. Genetic identification of a respiratory arsenate reductase. Proceedings of the National Academy of Sciences of the United States of America, 2003, 100(19): 10983–10988
CrossRef
Pubmed
Google scholar
|
[68] |
Krafft T, Macy J M. Purification and characterization of the respiratory arsenate reductase of Chrysiogenes arsenatis. European Journal of Biochemistry, 1998, 255(3): 647–653
CrossRef
Pubmed
Google scholar
|
[69] |
van Lis R, Nitschke W, Duval S, Schoepp-Cothenet B. Arsenics as bioenergetic substrates. Biochimica et Biophysica Acta (BBA). Bioenergetics, 2013, 1827(2): 176–188
CrossRef
Google scholar
|
[70] |
Malasarn D, Saltikov C W, Campbell K M, Santini J M, Hering J G, Newman D K. arrA is a reliable marker for As(V) respiration. Science, 2004, 306(5695): 455–455
CrossRef
Pubmed
Google scholar
|
[71] |
Hoeft S E, Kulp T R, Stolz J F, Hollibaugh J T, Oremland R S. Dissimilatory arsenate reduction with sulfide as electron donor: experiments with Mono lake water and isolation of strain MLMS-1, a chemoautotrophic arsenate respirer. Applied and Environmental Microbiology, 2004, 70(5): 2741–2747
CrossRef
Pubmed
Google scholar
|
[72] |
Bhattacharjee H, Rosen B P. Arsenic Metabolism in Prokaryotic and Eukaryotic Microbes. Molecular Microbiology of Heavy Metals. In: Nies D H, Silver S, eds. Heidelberg: Springer, 2002, 371–406
|
[73] |
Islam F S, Gault A G, Boothman C, Polya D A, Charnock J M, Chatterjee D, Lloyd J R. Role of metal-reducing bacteria in arsenic release from Bengal delta sediments. Nature, 2004, 430(6995): 68–71
CrossRef
Pubmed
Google scholar
|
[74] |
Fendorf S, Michael H A, van Geen A. Spatial and temporal variations of groundwater arsenic in South and Southeast Asia. Science, 2010, 328(5982): 1123–1127
CrossRef
Pubmed
Google scholar
|
[75] |
Song B, Chyun E, Jaffé P R, Ward B B. Molecular methods to detect and monitor dissimilatory arsenate-respiring bacteria (DARB) in sediments. FEMS Microbiology Ecology, 2009, 68(1): 108–117
CrossRef
Pubmed
Google scholar
|
[76] |
Héry M, Van Dongen B E, Gill F, Mondal D, Vaughan D J, Pancost R D, Polya D A, Lloyd J R. Arsenic release and attenuation in low organic carbon aquifer sediments from West Bengal. Geobiology, 2010, 8(2): 155–168
CrossRef
Pubmed
Google scholar
|
[77] |
Oremland R S, Stolz J F. Arsenic, microbes and contaminated aquifers. Trends in Microbiology, 2005, 13(2): 45–49
CrossRef
Pubmed
Google scholar
|
[78] |
Tufano K J, Reyes C, Saltikov C W, Fendorf S. Reductive processes controlling arsenic retention: revealing the relative importance of iron and arsenic reduction. Environmental Science & Technology, 2008, 42(22): 8283–8289
CrossRef
Pubmed
Google scholar
|
[79] |
Sri Lakshmi Sunita M, Prashant S, Bramha Chari P V, Nageswara Rao S, Balaravi P, Kavi Kishor P B. Molecular identification of arsenic-resistant estuarine bacteria and characterization of their ars genotype. Ecotoxicology (London, England), 2012, 21(1): 202–212
CrossRef
Pubmed
Google scholar
|
[80] |
Vilo C, Galetovic A, Araya J E, Gómez-Silva B, Dong Q. Draft genome sequence of a Bacillus bacterium from the Atacama Desert wetlands metagenome. Genome Announcements, 2015, 3(4): 1–2
CrossRef
Pubmed
Google scholar
|
[81] |
Qin J, Rosen B P, Zhang Y, Wang G, Franke S, Rensing C. Arsenic detoxification and evolution of trimethylarsine gas by a microbial arsenite S-adenosylmethionine methyltransferase. Proceedings of the National Academy of Sciences of the United States of America, 2006, 103(7): 2075–2080
CrossRef
Pubmed
Google scholar
|
[82] |
Wang P P, Sun G X, Zhu Y G. Identification and characterization of arsenite methyltransferase from an archaeon, Methanosarcina acetivorans C2A. Environmental Science & Technology, 2014, 48(21): 12706–12713
CrossRef
Pubmed
Google scholar
|
[83] |
Yin X X, Chen J, Qin J, Sun G X, Rosen B P, Zhu Y G. Biotransformation and volatilization of arsenic by three photosynthetic cyanobacteria. Plant Physiology, 2011, 156(3): 1631–1638
CrossRef
Pubmed
Google scholar
|
[84] |
Zhang S Y, Sun G X, Yin X X, Rensing C, Zhu Y G. Biomethylation and volatilization of arsenic by the marine microalgae Ostreococcus tauri. Chemosphere, 2013, 93(1): 47–53
CrossRef
Pubmed
Google scholar
|
[85] |
Williams P N, Santner J, Larsen M, Lehto N J, Oburger E, Wenzel W, Glud R N, Davison W, Zhang H. Localized flux maxima of arsenic, lead, and iron around root apices in flooded lowland rice. Environmental Science & Technology, 2014, 48(15): 8498–8506
CrossRef
Pubmed
Google scholar
|
[86] |
Guan D X, Williams P N, Luo J, Zheng J L, Xu H C, Cai C, Ma L Q. Novel precipitated zirconia-based DGT technique for high-resolution imaging of oxyanions in waters and sediments. Environmental Science & Technology, 2015, 49(6): 3653–3661
CrossRef
Pubmed
Google scholar
|
[87] |
Oburger E, Schmidt H. New methods to unravel rhizosphere processes. Trends in Plant Science, 2016, 21(3): 243–255
CrossRef
Pubmed
Google scholar
|
/
〈 | 〉 |