Biotransformation of selenium and arsenic in multi-species biofilm
Soo In Yang A , John R. Lawrence B , George D. W. Swerhone B and Ingrid J. Pickering A CA Department of Geological Sciences, University of Saskatchewan, 114 Science Place, Saskatoon, SK, S7N 5E2, Canada.
B Environment Canada, 11 Innovation Boulevard, Saskatoon, SK, S7N 3H5, Canada.
C Corresponding author. Email: ingrid.pickering@usask.ca
Environmental Chemistry 8(6) 543-551 https://doi.org/10.1071/EN11062
Submitted: 5 May 2011 Accepted: 16 September 2011 Published: 17 November 2011
Environmental context. Elevated levels of selenium and arsenic in the environment as a result of anthropogenic activities are creating significant concerns for the health of aquatic ecosystems. How biofilms, or aquatic microbial communities, interact with and chemically modify selenium and arsenic species has been examined. The results demonstrate that selenium and arsenic induce structural changes in biofilms, and concurrently undergo extensive biotransformation, in most cases to less bioavailable species.
Abstract. Arsenic and selenium are both elements of concern especially when released into the environment by anthropogenic activity. Biofilms, or communities of microorganisms, can play important roles in biotransforming elements to less toxic chemical forms. This study used novel tools to characterise the fate of oxyanions (selenate, selenite, arsenate or arsenite) in multi-species biofilms inoculated from a source receiving coal mining effluent. Confocal laser scanning microscopy (CLSM) demonstrated a distinct biofilm morphology at elevated oxyanion concentrations. Selenium and arsenic K near-edge X-ray absorption spectroscopy (XAS) showed biofilm biotransformation of oxyanions; extended X-ray absorption fine structure (EXAFS) confirmed elemental selenium as a product. Micro X-ray fluorescence imaging combined with CLSM revealed highly localised reduced selenium species in the biofilm. Isolation and partial 16S rRNA gene sequencing suggested four principle bacterial genera were responsible. Biofilms can both detoxify and sequester selenium and arsenic, playing critical roles in their fate and effects in aquatic environments.
References
[1] J. R. Arthur, G. J. Beckett, Symposium 2. Newer aspects of micronutrients in at risk groups. Proc. Nutr. Soc. 1994, 53, 615.| Symposium 2. Newer aspects of micronutrients in at risk groups.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXjslSmtLo%3D&md5=41e1882a5b9d3e0f5cfaeb8b53dea7d9CAS |
[2] R. Abdulah, K. Miyazaki, M. Nakazawa, H. Koyama, Chemical forms of selenium for cancer prevention. J. Trace Elem. Med. Biol. 2005, 19, 141.
| Chemical forms of selenium for cancer prevention.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xhslagtrc%3D&md5=986bbd2a2b35e0c26b9b6a1404d220d6CAS |
[3] K. Brown, J. Arthur, Selenium, selenoproteins and human health: a review. Public Health Nutr. 2001, 4, 593.
| Selenium, selenoproteins and human health: a review.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3MngvVaitQ%3D%3D&md5=f9514dbe75e53050f804b5ad2aad9d26CAS |
[4] P. L. Orr, K. R. Guiguer, C. K. Russel, Food chain transfer of selenium in lentic and lotic habitats of a western Canadian watershed. Ecotoxicol. Environ. Saf. 2006, 63, 175.
| Food chain transfer of selenium in lentic and lotic habitats of a western Canadian watershed.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XisFKisb4%3D&md5=3ed66182d267832c931877fc0f5181bcCAS |
[5] S. J. Hamilton, Review of selenium toxicity in the aquatic food chain. Sci. Total Environ. 2004, 326, 1.
| Review of selenium toxicity in the aquatic food chain.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXktVChsrs%3D&md5=e221dfe9d4edf15a493c5fb06bd0204cCAS |
[6] H. M. Ohlendorf, R. L. Hothem, D. Welsh, Nest success, cause-specific nest failure, and hatchability of aquatic birds at selenium-contaminated Kesterson Reservoir and a reference site. Condor 1989, 91, 787.
| Nest success, cause-specific nest failure, and hatchability of aquatic birds at selenium-contaminated Kesterson Reservoir and a reference site.Crossref | GoogleScholarGoogle Scholar |
[7] H. Yan-Chu, Arsenic distribution in soils, in Arsenic in the Environment. Part 1 Cycling and Characterization (Ed. J. O. Nriagu) 1994, pp. 17–50 (Wiley: New York).
[8] I. Cano-Aguilera, B. E. Rubio-Campos, G. De la Rosa, A. F. Aguilera-Alvarado, Arsenic mobility from mining tailings of Monte San Nicolas to Presa de Mata in Guanajuato, Mexico. World Acad. Sci. Eng. Technol. 2008, 47, 390.
[9] R. B. Finkelman, H. E. Belkin, B. Zheng, Health impacts of domestic coal use in China. Proc. Natl. Acad. Sci. USA 1999, 96, 3427.
| Health impacts of domestic coal use in China.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXjslCitrw%3D&md5=67f2165fbd7189b6634060133026169dCAS |
[10] Y. E. Yudovich, M. P. Ketris, Arsenic in coal: a review. Int. J. Coal Geol. 2005, 61, 141.
| Arsenic in coal: a review.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXms1Kmsg%3D%3D&md5=f95a705ced97075739719d7b7585d767CAS |
[11] Y. E. Yudovich, M. P. Ketris, Selenium in coal: a review. Int. J. Coal Geol. 2006, 67, 112.
| Selenium in coal: a review.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XjvVWrur8%3D&md5=96e19848cc764d5b26e42332c63094a9CAS |
[12] A. W. Cantafio, K. D. Hagen, G. E. Lewis, T. L. Bledsoe, K. M. Nunan, J. M. Macy, Pilot-scale selenium bioremediation of San Joaquin drainage water with Thauera selenatis. Appl. Environ. Microbiol. 1996, 62, 3298.
| 1:CAS:528:DyaK28XlsFeqsrY%3D&md5=8b2c4613e612d4ba620917cf248b9725CAS |
[13] K. A. Natarajan, Microbial aspects of acid mine drainage and its bioremediation. Trans. Nonferrous Met. Soc. China 2008, 18, 1352.
| Microbial aspects of acid mine drainage and its bioremediation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXitlahsr8%3D&md5=a6a4a90887e73f2660e9be0ff2cf1aabCAS |
[14] J. M. Macy, S. Rech, G. Auling, M. Dorsch, E. Stackebrandt, L. I. Sly, Thauera selenatis gen. nov., sp. nov., a member of the beta subclass of Proteobacteria with a novel type of anaerobic respiration. Int. J. Syst. Bacteriol. 1993, 43, 135.
| Thauera selenatis gen. nov., sp. nov., a member of the beta subclass of Proteobacteria with a novel type of anaerobic respiration.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK3s7lt1CmtA%3D%3D&md5=c18b3d1f040c64d1a074a502ff3621eeCAS |
[15] R. Burra, G. A. Pradenas, R. A. Montes, C. C. Vásquez, T. G. Chasteen, Production of dimethyl triselenide and dimethyl diselenenyl sulfide in the headspace of metalloid-resistant Bacillus species grown in the presence of selenium oxyanions. Anal. Biochem. 2010, 396, 217.
| Production of dimethyl triselenide and dimethyl diselenenyl sulfide in the headspace of metalloid-resistant Bacillus species grown in the presence of selenium oxyanions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsFShtb3I&md5=1f2d03042601b7007e2be427c05a054bCAS |
[16] S. Hapuarachchi, J. Swearingen, T. G. Chasteen, Determination of elemental and precipitated selenium production by a facultative anaerobe grown under sequential anaerobic/aerobic conditions. Process Biochem. 2004, 39, 1607.
| Determination of elemental and precipitated selenium production by a facultative anaerobe grown under sequential anaerobic/aerobic conditions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXlsVejtL8%3D&md5=b7926eebebead89544a43421e7487858CAS |
[17] V. Van Fleet-Stalder, T. G. Chasteen, I. J. Pickering, G. N. George, R. C. Prince, Fate of selenate and selenite metabolized by Rhodobacter sphaeroides. Appl. Environ. Microbiol. 2000, 66, 4849.
| Fate of selenate and selenite metabolized by Rhodobacter sphaeroides.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXnvFyrtbc%3D&md5=f11fb3f621591cc0ed7e46fb0bd0165cCAS |
[18] R. Singh, D. Paul, R. K. Jain, Biofilms: implications in bioremediation. Trends Microbiol. 2006, 14, 389.
| Biofilms: implications in bioremediation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XotlWns7Y%3D&md5=f5bfac37f0c048e6a64d8555b3f0931eCAS |
[19] E. van Hullebusch, M. Zandvoort, P. Lens, Metal immobilisation by biofilms: mechanisms and analytical tools. Rev. Environ. Sci. Biotechnol. 2003, 2, 9.
| Metal immobilisation by biofilms: mechanisms and analytical tools.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXlsVCku7Y%3D&md5=d33a3bff625362748df81be4da751f83CAS |
[20] W. G. Weisburg, S. M. Barns, D. A. Pelletier, D. J. Lane, 16S ribosomal DNA amplification for phylogenetic study. J. Bacteriol. 1991, 173, 697.
| 1:CAS:528:DyaK3MXhsl2lurY%3D&md5=bcc8ec5bbd5da0b3d7f684dffaa20a34CAS |
[21] J. R. Lawrence, G. D. W. Swerhone, T. R. Neu, A simple rotating annular reactor for replicated biofilm studies. J. Microbiol. Methods 2000, 42, 215.
| A simple rotating annular reactor for replicated biofilm studies.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXos1Sgsbw%3D&md5=a334b3c5eca5f3e15aa3047304be1694CAS |
[22] W. T. Frankenberger Jr, U. Karlson, Microbial volatilization of selenium from soils and sediments, in Selenium in the Environment (Eds W. T. Frankenberger Jr, S. Benson) 1995, pp. 369–387 (Marcel Dekker Inc.: New York).
[23] J. R. Lawrence, G. D. W. Swerhone, G. G. Leppard, T. Araki, X. Zhang, M. M. West, A. P. Hitchcock, Scanning transmission X-ray, laser scanning, and transmission electron microscopy mapping of the exopolymeric matrix of microbial biofilms. Appl. Environ. Microbiol. 2003, 69, 5543.
| Scanning transmission X-ray, laser scanning, and transmission electron microscopy mapping of the exopolymeric matrix of microbial biofilms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXntlSis74%3D&md5=8693896a65c718e9e145957d8a42e3caCAS |
[24] M. D. Abramoff, P. J. Magelhaes, S. J. Ram, Image processing with Image J. Biophoton Int. 2004, 11, 36.
[25] R. Andrahennadi, I. J. Pickering, Arsenic accumulation, biotransformation and localisation in bertha armyworm moths. Environ. Chem. 2008, 5, 413.
| Arsenic accumulation, biotransformation and localisation in bertha armyworm moths.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsFWgu7bL&md5=f21760bbb6aeca98495eed25acb15bb6CAS |
[26] S. I. Zabinsky, J. J. Rehr, A. Ankudinov, R. C. Albers, M. J. Eller, Multiple-scattering calculations of X-ray-absorption spectra. Phys. Rev. B 1995, 52, 2995.
| Multiple-scattering calculations of X-ray-absorption spectra.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXnt1Ggt7w%3D&md5=7dac54f978ce8272d7f771b6654f96ceCAS |
[27] G. A. Burton, T. H. Giddings, P. DeBrine, R. Fall, High incidence of selenite-resistant bacteria from a site polluted with selenium. Appl. Environ. Microbiol. 1987, 53, 185.
| 1:CAS:528:DyaL2sXotFCqsg%3D%3D&md5=374a8d3a79a3514eeb8468bddafd3553CAS |
[28] W. Hunter, D. Manter, Reduction of selenite to elemental red selenium by Pseudomonas sp. strain CA5. Curr. Microbiol. 2009, 58, 493.
| Reduction of selenite to elemental red selenium by Pseudomonas sp. strain CA5.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXktFCjtbg%3D&md5=1cb02d8a95a0b3018cee7c1a72ecbef1CAS |
[29] W. Hunter, L. Kuykendall, Reduction of selenite to elemental red selenium by Rhizobium sp. strain B1. Curr. Microbiol. 2007, 55, 344.
| Reduction of selenite to elemental red selenium by Rhizobium sp. strain B1.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtVOisbnK&md5=e75a158ee9297d3e9130d07a8eae3531CAS |
[30] G. N. George, I. J. Pickering, C. J. Doonan, M. Korbas, S. P. Singh, R. Hoffmeyer, Inorganic molecular toxicology and chelation therapy of heavy metals and metalloids. Adv. Mol. Toxicol. 2008, 2, 123.
| Inorganic molecular toxicology and chelation therapy of heavy metals and metalloids.Crossref | GoogleScholarGoogle Scholar |
[31] J. F. Stolz, P. Basu, J. M. Santini, R. S. Oremland, Arsenic and selenium in microbial metabolism. Annu. Rev. Microbiol. 2006, 60, 107.
| Arsenic and selenium in microbial metabolism.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xht1Whtb%2FE&md5=4bb864be8fbe46e7ef1c69b4656d2735CAS |
[32] M. Basaglia, A. Toffanin, E. Baldan, M. Bottegal, J. P. Shapleigh, S. Casella, Selenite-reducing capacity of the copper-containing nitrite reductase of Rhizobium sullae. FEMS Microbiol. Lett. 2007, 269, 124.
| Selenite-reducing capacity of the copper-containing nitrite reductase of Rhizobium sullae.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXjvVyntb0%3D&md5=fe1aece1fab43c4032448e78f42b43dbCAS |
[33] F. Challenger, Biological methylation. Chem. Rev. 1945, 36, 315.
| Biological methylation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaH2MXisFGrtQ%3D%3D&md5=86537b05dfe94a77d9ebc74199bd310eCAS |
[34] D. J. Thompson, A chemical hypothesis for arsenic methylation in mammals. Chem. Biol. Interact. 1993, 88, 89.
| A chemical hypothesis for arsenic methylation in mammals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXit1yi&md5=bf3d897d4989e0c70bb8ef038ed5f3ceCAS |
[35] R. Bentley, T. G. Chasteen, Microbial methylation of metalloids: arsenic, antimony, and bismuth. Microbiol. Mol. Biol. Rev. 2002, 66, 250.
| Microbial methylation of metalloids: arsenic, antimony, and bismuth.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XltFSltrs%3D&md5=ab04aacfabc1be19a2f6735212e61b6fCAS |
[36] M. G. Ord, L. A. Stocken, A contribution to chemical defence in World War II. Trends Biochem. Sci. 2000, 25, 253.
| A contribution to chemical defence in World War II.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXjtVeqsr8%3D&md5=735ffcaa214ac2da1806df2ad5cda9a2CAS |
[37] H. Wiseman, B. Halliwell, Damage to DNA by reactive oxygen and nitrogen species: role in inflammatory disease and progression to cancer. Biochem. J. 1996, 313, 17.
| 1:CAS:528:DyaK28XivVOgtA%3D%3D&md5=0e722e0d0ba58c7393c9f704cd3fbc1eCAS |
[38] S. Yamamoto, Y. Konishi, T. Murai, M. Shibata, T. Matsuda, K. Kuroda, G. Endo, S. Fukushima, Enhancing effects of an organic arsenic compound, dimethylarsinic acid (cacodylic acid), in a multi-organ carcinogenesis bioassay. Appl. Organomet. Chem. 1994, 8, 197.
| Enhancing effects of an organic arsenic compound, dimethylarsinic acid (cacodylic acid), in a multi-organ carcinogenesis bioassay.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXltVWltL0%3D&md5=fb481c698894ea17fe9c39441a7d9a7cCAS |
[39] E. Dopp, L. M. Hartmann, A. M. Florea, U. von Recklinghausen, R. Pieper, B. Shokouhi, A. W. Rettenmeier, A. V. Hirner, G. Obe, Uptake of inorganic and organic derivatives of arsenic associated with induced cytotoxic and genotoxic effects in Chinese hamster ovary (CHO) cells. Toxicol. Appl. Pharmacol. 2004, 201, 156.
| Uptake of inorganic and organic derivatives of arsenic associated with induced cytotoxic and genotoxic effects in Chinese hamster ovary (CHO) cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXpslCqu78%3D&md5=4fe7137dc9146460349faadc7fac1231CAS |
[40] N. Eguchi, K. Kuroda, G. Endo, Metabolites of arsenic induced tetraploids and mitotic arrest in cultured cells. Arch. Environ. Contam. Toxicol. 1997, 32, 141.
| Metabolites of arsenic induced tetraploids and mitotic arrest in cultured cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXisFejsLk%3D&md5=429c12b79ff44fca4a0d35e987aca486CAS |
[41] P. Andrewes, K. T. Kitchin, K. Wallace, Dimethylarsine and trimethylarsine are potent genotoxins in vitro. Chem. Res. Toxicol. 2003, 16, 994.
| Dimethylarsine and trimethylarsine are potent genotoxins in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXltlejsLw%3D&md5=02b53f4113f5d0ac44687e948cf5b0a9CAS |
[42] H. Yamauchi, T. Kaise, K. Takahashi, Y. Yamamura, Toxicity and metabolism of trimethylarsine in mice and hamsters. Toxicol. Sci. 1990, 14, 399.
| Toxicity and metabolism of trimethylarsine in mice and hamsters.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXhtFert7w%3D&md5=11981e0e8c1dfdedc178e54fb0afbf74CAS |
[43] I. J. Pickering, R. C. Prince, M. J. George, R. D. Smith, G. N. George, D. E. Salt, Reduction and coordination of arsenic in Indian mustard. Plant Physiol. 2000, 122, 1171.
| Reduction and coordination of arsenic in Indian mustard.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXktFSquro%3D&md5=b42becc2a4ce0af897a69f43bc07db1aCAS |
[44] J. Gailer, G. N. George, I. J. Pickering, R. C. Prince, S. C. Ringwald, J. E. Pemberton, R. S. Glass, H. S. Younis, D. W. DeYoung, H. V. Aposhian, A metabolic link between arsenite and selenite: the seleno-bis(S-glutathionyl) arsinium ion. J. Am. Chem. Soc. 2000, 122, 4637.
| A metabolic link between arsenite and selenite: the seleno-bis(S-glutathionyl) arsinium ion.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXivVSksb0%3D&md5=5a75b4d6d30347f0ba8432bd74ec82a3CAS |
[45] D. Páez-Espino, J. Tamames, V. de Lorenzo, D. Cánovas, Microbial response to environmental arsenic. Biometals 2009, 22, 117.
| Microbial response to environmental arsenic.Crossref | GoogleScholarGoogle Scholar |
[46] W. R. Cullen, H. Li, G. Hewitt, K. J. Reimer, N. Zalunardo, Identification of extracellular arsenical metabolites in the growth medium of the microorganisms Apiotrichum humicola and Scopulariopsis brevicaulis. Appl. Organomet. Chem. 1994, 8, 303.
| Identification of extracellular arsenical metabolites in the growth medium of the microorganisms Apiotrichum humicola and Scopulariopsis brevicaulis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXlslCru7k%3D&md5=a933df04e6bf46d822713d00b54330bbCAS |
[47] O. Foss, V. Janickis, Crystal structure of γ-monoclinic selenium. J. Chem. Soc., Dalton Trans. 1980, 4, 624.
| Crystal structure of γ-monoclinic selenium.Crossref | GoogleScholarGoogle Scholar |
[48] B. Cheng, E. T. Samulski, Rapid, high yield, solution-mediated transformation of polycrystalline selenium powder into single-crystal nanowires. Chem. Commun. 2003, 2024.
| Rapid, high yield, solution-mediated transformation of polycrystalline selenium powder into single-crystal nanowires.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXls1Cktr8%3D&md5=20b7466df4ef17ece2cb7a956897d58cCAS |