[en] Arsenic is a metalloid that occurs naturally in aquatic and terrestrial environments. The high toxicity of arsenic derivatives converts this element in a serious problem of public health worldwide. There is a global arsenic geocycle in which microbes play a relevant role. Ancient exposure to arsenic derivatives, both inorganic and organic, has represented a selective pressure for microbes to evolve or acquire diverse arsenic resistance genetic systems. In addition, arsenic compounds appear to have been used as a toxin in chemical warfare for a long time selecting for an extended range of arsenic resistance determinants. Arsenic resistance strategies rely mainly on membrane transport pathways that extrude the toxic compounds from the cell cytoplasm. The ars operons, first discovered in bacterial R-factors almost 50 years ago, are the most common microbial arsenic resistance systems. Numerous ars operons, with a variety of genes and different combinations of them, populate the prokaryotic genomes, including their accessory plasmids, transposons, and genomic islands. Besides these canonical, widespread ars gene clusters, which confer resistance to the inorganic forms of arsenic, additional genes have been discovered recently, which broadens the spectrum of arsenic tolerance by detoxifying organic arsenic derivatives often used as toxins. This review summarizes the presence, distribution, organization, and redundance of arsenic resistance genes in prokaryotes.
Precision for document type :
Review article
Disciplines :
Environmental sciences & ecology
Author, co-author :
Ben Fekih, Ibtissem ✱; Université de Liège - ULiège > Département GxABT > Gestion durable des bio-agresseurs ; Institute of Environmental Microbiology, College of Resources and Environment, Fujian Agriculture and Forestry University, Fuzhou, China
Zhang, Chengkang ✱; Institute of Environmental Microbiology, College of Resources and Environment, Fujian Agriculture and Forestry University, Fuzhou, China
Li, Yuan Ping; Institute of Environmental Microbiology, College of Resources and Environment, Fujian Agriculture and Forestry University, Fuzhou, China
Zhao, Yi; Department of Plant and Environmental Sciences, University of Copenhagen, Copenhagen, Denmark
Alwathnani, Hend A; Department of Botany and Microbiology, King Saud University, Riyadh, Saudi Arabia
Saquib, Quaiser; Department of Zoology, College of Sciences, King Saud University, Riyadh, Saudi Arabia
Rensing, Christopher; Institute of Environmental Microbiology, College of Resources and Environment, Fujian Agriculture and Forestry University, Fuzhou, China ; Key Laboratory of Urban Environment and Health, Institute of Urban Environment, Chinese Academy of Sciences, Xiamen, China
Cervantes, Carlos; Instituto de Investigaciones Químico-Biológicas, Universidad Michoacana, Morelia, Mexico
✱ These authors have contributed equally to this work.
Language :
English
Title :
Distribution of Arsenic Resistance Genes in Prokaryotes.
NSCF - National Natural Science Foundation of China CONACYT - Consejo Nacional de Ciencia y Tecnología
Funding text :
Authors would like to thank Twasol Research Excellence Program (TRE Program), King Saud University, Riyadh, Saudi Arabia for support.Work in the lab of CR was supported by the National Natural Science Foundation of China (Grant No. 31770123), “100” Talents Program from Fujian province, High level foreigner expertise program from Fujian province, International cooperation program from Fujian Agriculture and Forestry University. CC acknowledges support from Consejo Nacional de Ciencia y Tecnología (CONACYT), México (Grant No. 220040) and Coordinación de Investigación Científica, Universidad Michoacana (Grant No. 2.6).
Achour, A. R., Bauda, P., and Billard, P. (2007). Diversity of arsenite transporter genes from arsenicresistant soil bacteria. Res. Microbiol. 158, 128-137. doi: 10.1016/j.resmic.2006.11.006
Achour-Rokbani, A., Cordi, A., Poupin, P., Bauda, P., and Billard, P. (2010). Characterization of the ars gene cluster from extremely arsenic-resistant Microbacterium sp strain A33. Appl. Environ. Microbiol. 76, 948-955. doi: 10.1128/Aem.01738-09
Bentley, R., and Chasteen, T. G. (2002). Microbial methylation of metalloids: arsenic, antimony, and bismuth. Microbiol. Mol. Biol. Rev. 66, 250-271. doi: 10.1128/Mmbr.66.2.250-271.2002
Besold, J., Biswas, A., Suess, E., Scheinost, A. C., Rossberg, A., Mikutta, C., et al. (2018). Monothioarsenate transformation kinetics determining arsenic sequestration by sulfhydryl groups of peat. Environ. Sci. Technol. 52, 7317-7326. doi: 10.1021/acs.est.8b01542
Bhat, S., Luo, X., Xu, Z. Q., Liu, L. X., and Zhang, R. (2011). Bacillus sp CDB3 isolated from cattle dipsites possesses two ars gene clusters. J. Environ. Sci. 23, 95-101. doi: 10.1016/S1001-0742 (10) 60378-6
Bienert, G. P., Schussler, M. D., and Jahn, T. P. (2008). Metalloids: essential, beneficial or toxic? Major intrinsic proteins sort it out. Trends Biochem. Sci. 33, 20-26. doi: 10.1016/j.tibs.2007.10.004
Branco, R., Chung, A. P., and Morais, P. V. (2008). Sequencing and expression of two arsenic resistance operons with different functions in the highly arsenic-resistant strain Ochrobactrum tritici SCII24 (T). BMC Microbiol. 8:95. doi: 10.1186/1471-2180-8-95
Busenlehner, L. S., Pennella, M. A., and Giedroc, D. P. (2003). The SmtB/ArsR family of metalloregulatory transcriptional repressors: structural insights into prokaryotic metal resistance. FEMS Microbiol. Rev. 27, 131-143. doi: 10.1016/S0168-6445 (03) 00054-8
Butcher, B. G., Deane, S. M., and Rawlings, D. E. (2000). The chromosomal arsenic resistance genes of Thiobacillus ferrooxidans have an unusual arrangement and confer increased arsenic and antimony resistance to Escherichia coli. Appl. Environ. Microbiol. 66, 1826-1833. doi: 10.1128/AEM.66.5.1826-1833.2000
Butcher, B. G., and Rawlings, D. E. (2002). The divergent chromosomal ars operon of Acidithiobacillus ferrooxidans is regulated by an atypical ArsR protein. Microbiology 148(Pt 12), 3983-3992. doi: 10.1099/00221287-148-12-3983
Cai, J., Salmon, K., and DuBow, M. S. (1998). A chromosomal ars operon homologue of Pseudomonas aeruginosa confers increased resistance to arsenic and antimony in Escherichia coli. Microbiology 144(Pt 10), 2705-2713. doi: 10.1099/00221287-144-10-2705
Cai, L., Liu, G., Rensing, C., and Wang, G. (2009). Genes involved in arsenic transformation and resistance associated with different levels of arsenic-contaminated soils. BMC Microbiol. 9:4. doi: 10.1186/1471-2180-9-4
Carlin, A., Shi, W., Dey, S., and Rosen, B. P. (1995). The ars operon of Escherichia coli confers arsenical and antimonial resistance. J. Bacteriol. 177, 981-986. doi: 10.1128/jb.177.4.981-986.1995
Castillo, R., and Saier, M. H. (2010). Functional promiscuity of homologues of the bacterial ArsA ATPases. Int. J. Microbiol. 2010:187373. doi: 10.1155/2010/187373
Chauhan, N. S., Ranjan, R., Purohit, H. J., Kalia, V. C., and Sharma, R. (2009). Identification of genes conferring arsenic resistance to Escherichia coli from an effluent treatment plant sludge metagenomic library. FEMS Microbiol. Ecol. 67, 130-139. doi: 10.1111/j.1574-6941.2008.00613.x
Chen, C. M., Misra, T. K., Silver, S., and Rosen, B. P. (1986). Nucleotide sequence of the structural genes for an anion pump. The plasmid-encoded arsenical resistance operon. J. Biol. Chem. 261, 15030-15038.
Chen, J., Bhattacharjee, H., and Rosen, B. P. (2015a). ArsH is an organoarsenical oxidase that confers resistance to trivalent forms of the herbicide monosodium methylarsenate and the poultry growth promoter roxarsone. Mol. Microbiol. 96, 1042-1052. doi: 10.1111/mmi.12988
Chen, J., Madegowda, M., Bhattacharjee, H., and Rosen, B. P. (2015b). ArsP: a methylarsenite efflux permease. Mol. Microbiol. 98, 625-635. doi: 10.1111/mmi.13145
Chen, J., Sun, S., Li, C. Z., Zhu, Y. G., and Rosen, B. P. (2014). Biosensor for organoarsenical herbicides and growth promoters. Environ. Sci. Technol. 48, 1141-1147. doi: 10.1021/es4038319
Chen, J., Yoshinaga, M., Garbinski, L. D., and Rosen, B. P. (2016). Synergistic interaction of glyceraldehydes-3-phosphate dehydrogenase and ArsJ, a novel organoarsenical efflux permease, confers arsenate resistance. Mol. Microbiol. 100, 945-953. doi: 10.1111/mmi.13371
Cuebas, M., Villafane, A., McBride, M., Yee, N., and Bini, E. (2011). Arsenate reduction and expression of multiple chromosomal ars operons in Geobacillus kaustophilus A1. Microbiology 157(Pt 7), 2004-2011. doi: 10.1099/mic.0.048678-0
Drewniak, L., Dziewit, L., Ciezkowska, M., Gawor, J., Gromadka, R., and Sklodowska, A. (2013). Structural and functional genomics of plasmid pSinA of Sinorhizobium sp. M14 encoding genes for the arsenite oxidation and arsenic resistance. J. Biotechnol. 164, 479-488. doi: 10.1016/j.jbiotec.2013.01.017
Falgenhauer, L., Ghosh, H., Guerra, B., Yao, Y., Fritzenwanker, M., Fischer, J., et al. (2017). Comparative genome analysis of IncHI2 VIM-1 carbapenemase-encoding plasmids of Escherichia coli and Salmonella enterica isolated from a livestock farm in Germany. Vet. Microbiol. 200, 114-117. doi: 10.1016/j.vetmic.2015.09.001
Freel, K. C., Krueger, M. C., Farasin, J., Brochier-Armanet, C., Barbe, V., Andres, J., et al. (2015). Adaptation in toxic environments: arsenic genomic islands in the bacterial genus thiomonas. PLoS One 10:e0139011. doi: 10.1371/journal.pone.0139011
Ghosh, M., Shen, J., and Rosen, B. P. (1999). Pathways of As (III) detoxification in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. U. S. A. 96, 5001-5006. doi: 10.1073/pnas.96.9.5001
Gihring, T. M., Bond, P. L., Peters, S. C., and Banfield, J. F. (2003). Arsenic resistance in the archaeon "Ferroplasma acidarmanus": new insights into the structure and evolution of the ars genes. Extremophiles 7, 123-130. doi: 10.1007/s00792-002-0303-6
Hao, X., Li, X., Pal, C., Hobman, J., Larsson, D. G. J., Saquib, Q., et al. (2017). Bacterial resistance to arsenic protects against protist killing. Biometals 30, 307-311. doi: 10.1007/s10534-017-0003-4
Hao, X., Lüthje, F. L., Qin, Y., McDevitt, S. F., Lutay, N., Hobman, J. L., et al. (2015). Survival in amoeba-a major selection pressure on the presence of bacterial copper and zinc resistance determinants? Identification of a "copper pathogenicity island". Appl. Microbiol. Biotechnol. 99, 5817-5824. doi: 10.1007/s00253-015-6749-0
Hedges, R. W., and Baumberg, S. (1973). Resistance to arsenic compounds conferred by a plasmid transmissible between strains of Escherichia coli. J. Bacteriol. 115, 459-460.
Hug, K., Maher, W. A., Stott, M. B., Krikowa, F., Foster, S., and Moreau, J. W. (2014). Microbial contributions to coupled arsenic and sulfur cycling in the acid-sulfide hot spring Champagne Pool, New Zealand. Front. Microbiol 5:569. doi: 10.3389/fmicb.2014.00569
Ji, G., and Silver, S. (1992). Regulation and expression of the arsenic resistance operon from Staphylococcus aureus plasmid pI258. J. Bacteriol. 174, 3684-3694. doi: 10.1128/jb.174.11.3684-3694.1992
Kanwal, R., and Hua, N. (2013). Double-edged effects of arsenic compounds: anticancer and carcinogenic effects. Curr. Drug Metab. 14, 1029-1041. doi: 10.2174/13892002113146660116
Kerschen, E. J., Cohen, D. A., Kaplan, A. M., and Straley, S. C. (2004). The plague virulence protein YopM targets the innate immune response by causing a global depletion of NK cells. Infect. Immun. 72, 4589-4602. doi: 10.1128/IAI.72.8.4589-4602.2004
Kruger, M. C., Bertin, P. N., Heipieper, H. J., and Arsene-Ploetze, F. (2013). Bacterial metabolism of environmental arsenic-mechanisms and biotechnological applications. Appl. Microbiol. Biotechnol. 97, 3827-3841. doi: 10.1007/s00253-013-4838-5
Li, J., Mandal, G., and Rosen, B. P. (2016a). Expression of arsenic resistance genes in the obligate anaerobe Bacteroides vulgatus ATCC 8482, a gut microbiome bacterium. Anaerobe 39, 117-123. doi: 10.1016/j.anaerobe.2016.03.012
Li, J., Pawitwar, S. S., and Rosen, B. P. (2016b). The organoarsenical biocycle and the primordial antibiotic methylarsenite. Metallomics 8, 1047-1055. doi: 10.1039/c6mt00168h
Li, R., Haile, J. D., and Kennelly, P. J. (2003). An arsenate reductase from Synechocystis sp. strain PCC 6803 exhibits a novel combination of catalytic characteristics. J. Bacteriol. 185, 6780-6789. doi: 10.1128/JB.185.23.6780-6789.2003
Li, X., and Krumholz, L. R. (2007). Regulation of arsenate resistance in Desulfovibrio desulfuricans G20 by an arsRBCC operon and an arsC gene. J. Bacteriol. 189, 3705-3711. doi: 10.1128/JB.01913-06
Li, X., Zhang, L., and Wang, G. (2014). Genomic evidence reveals the extreme diversity and wide distribution of the arsenic-related genes in Burkholderiales. PLoS One 9:e92236. doi: 10.1371/journal.pone.0092236
Lin, Y. F., Walmsley, A. R., and Rosen, B. P. (2006). An arsenic metallochaperone for an arsenic detoxification pump. Proc. Natl. Acad. Sci. U. S. A. 103, 15617-15622. doi: 10.1073/pnas.0603974103
Lopez-Maury, L., Florencio, F. J., and Reyes, J. C. (2003). Arsenic sensing and resistance system in the cyanobacterium Synechocystis sp. strain PCC 6803. J. Bacteriol. 185, 5363-5371. doi: 10.1128/JB.185.18.5363-5371.2003
Maimaitiyiming, Y., Wang, C., Xu, S., Islam, K., and Chen, Y. J. (2018). Role of arsenic (+ 3 oxidation state) methyltransferase in arsenic mediated APL treatment: an in vitro investigation. Metallomics 10, 828-837. doi: 10.1039/c8mt00057c
McMurry, L., Petrucci, R. E. Jr., and Levy, S. B. (1980). Active efflux of tetracycline encoded by four genetically different tetracycline resistance determinants in Escherichia coli. Proc. Natl. Acad. Sci. U. S. A. 77, 3974-3977. doi: 10.1073/pnas.77.7.3974
Meng, Y. L., Liu, Z., and Rosen, B. P. (2004). As (III) and Sb (III) uptake by GlpF and efflux by ArsB in Escherichia coli. J. Biol. Chem. 279, 18334-18341. doi: 10.1074/jbc. M400037200
Mobley, H. L., and Rosen, B. P. (1982). Energetics of plasmid-mediated arsenate resistance in Escherichia coli. Proc. Natl. Acad. Sci. U. S. A. 79, 6119-6122. doi: 10.1073/pnas.79.20.6119
Mukhopadhyay, R., Bhattacharjee, H., and Rosen, B. P. (2014). Aquaglyceroporins: generalized metalloid channels. Biochim. Biophys. Acta 1840, 1583-1591. doi: 10.1016/j.bbagen. 2013.11.021
Mukhopadhyay, R., Rosen, B. P., Phung, L. T., and Silver, S. (2002). Microbial arsenic: from geocycles to genes and enzymes. FEMS Microbiol. Rev. 26, 311-325. doi: 10.1016/S0168-6445 (02) 00112-2
Muller, D., Medigue, C., Koechler, S., Barbe, V., Barakat, M., Talla, E., et al. (2007). A tale of two oxidation states: bacterial colonization of arsenic-rich environments. PLoS Genet. 3:e53. doi: 10.1371/journal.pgen. 0030053
Naranmandura, H., Ibata, K., and Suzuki, K. T. (2007). Toxicity of dimethylmonothioarsinic acid toward human epidermoid carcinoma A431 cells. Chem. Res. Toxicol. 20, 1120-1125. doi: 10.1021/tx700103y
Neyt, C., Iriarte, M., Thi, V. H., and Cornelis, G. R. (1997). Virulence and arsenic resistance in Yersiniae. J. Bacteriol. 179, 612-619. doi: 10.1128/jb.179.3.612-619.1997
Nies, D. H. (2003). Efflux-mediated heavy metal resistance in prokaryotes. FEMS Microbiol. Rev. 27, 313-339. doi: 10.1016/S0168-6445 (03) 00048-2
Novick, R. P., and Roth, C. (1968). Plasmid-linked resistance to inorganic salts in Staphylococcus aureus. J. Bacteriol. 95, 1335-1342.
Ordóñez, E., Letek, M., Valbuena, N., Gil, J. A., and Mateos, L. M. (2005). Analysis of genes involved in arsenic resistance in Corynebacterium glutamicum ATCC 13032. Appl. Environ. Microbiol. 71, 6206-6215. doi: 10.1128/AEM.71.10.6206-6215.2005
Oremland, R. S., Saltikov, C. W., Wolfe-Simon, F., and Stolz, J. F. (2009). Arsenic in the evolution of earth and extraterrestrial ecosystems. Geomicrobiol. J. 26, 522-536. doi: 10.1080/01490450903102525
Oremland, R. S., and Stolz, J. F. (2003). The ecology of arsenic. Science 300, 939-944. doi: 10.1126/science.1081903
Páez-Espino, A. D., Durante-Rodriguez, G., and De Lorenzo, V. (2015). Functional coexistence of twin arsenic resistance systems in Pseudomonas putida KT2440. Environ. Microbiol. 17, 229-238. doi: 10.1111/1462-2920.12464
Páez-Espino, D., Tamames, J., De Lorenzo, V., and Canovas, D. (2009). Microbial responses to environmental arsenic. Biometals 22, 117-130. doi: 10.1007/s10534-008-9195-y
Petrick, J. S., Ayala-Fierro, F., Cullen, W. R., Carter, D. E., and Vasken Aposhian, H. (2000). Monomethylarsonous acid (MMA (III)) is more toxic than arsenite in Chang human hepatocytes. Toxicol. Appl. Pharmacol. 163, 203-207. doi: 10.1006/taap. 1999.8872
Planer-Friedrich, B., Franke, D., Merkel, B., and Wallschlager, D. (2008). Acute toxicity of thioarsenates to Vibrio fischeri. Environ. Toxicol. Chem. 27, 2027-2035. doi: 10.1897/07-633.1
Planer-Friedrich, B., Hartig, C., Lohmayer, R., Suess, E., McCann, S. H., and Oremland, R. (2015). Anaerobic chemolithotrophic growth of the haloalkaliphilic bacterium Sstrain MLMS-1 by disproportionation of monothioarsenate. Environ. Sci. Technol. 49, 6554-6563. doi: 10.1021/acs.est.5b01165
Prithivirajsingh, S., Mishra, S. K., and Mahadevan, A. (2001). Detection and analysis of chromosomal arsenic resistance in Pseudomonas fluorescens strain MSP3. Biochem. Biophys. Res. Commun. 280, 1393-1401. doi: 10.1006/bbrc.2001.4287
Qin, J., Rosen, B. P., Zhang, Y., Wang, G., Franke, S., and Rensing, C. (2006). Arsenic detoxification and evolution of trimethylarsine gas by a microbial arsenite S-adenosylmethionine methyltransferase. Proc. Natl. Acad. Sci. U. S. A. 103, 2075-2080. doi: 10.1073/pnas.0506836103
Ramos, J. L., Duque, E., Gallegos, M. T., Godoy, P., Ramos-Gonzalez, M. I., Rojas, A., et al. (2002). Mechanisms of solvent tolerance in gram-negative bacteria. Annu. Rev. Microbiol. 56, 743-768. doi: 10.1146/annurev. micro.56.012302.161038
Rosen, B. P. (1999). Families of arsenic transporters. Trends Microbiol. 7, 207-212. doi: 10.1016/S0966-842X (99) 01494-8
Rosen, B. P. (2002). Biochemistry of arsenic detoxification. FEBS Lett. 529, 86-92. doi: 10.1016/S0014-5793 (02) 03186-1
Rosen, B. P., and Liu, Z. (2009). Transport pathways for arsenic and selenium: a minireview. Environ. Int. 35, 512-515. doi: 10.1016/j.envint.2008.07.023
Rosenstein, R., Peschel, A., Wieland, B., and Gotz, F. (1992). Expression and regulation of the antimonite, arsenite, and arsenate resistance operon of Staphylococcus xylosus plasmid pSX267. J. Bacteriol. 174, 3676-3683. doi: 10.1128/jb.174.11.3676-3683.1992
Ryan, D., and Colleran, E. (2002). Arsenical resistance in the IncHI2 plasmids. Plasmid 47, 234-240. doi: 10.1016/S0147-619X (02) 00012-4
Saltikov, C. W., Cifuentes, A., Venkateswaran, K., and Newman, D. K. (2003). The ars detoxification system is advantageous but not required for As (V) respiration by the genetically tractable Shewanella species strain ANA-3. Appl. Environ. Microbiol. 69, 2800-2809. doi: 10.1128/AEM.69.5.2800-2809.2003
Sanders, O. I., Rensing, C., Kuroda, M., Mitra, B., and Rosen, B. P. (1997). Antimonite is accumulated by the glycerol facilitator GlpF in Escherichia coli. J. Bacteriol. 179, 3365-3367. doi: 10.1128/jb.179.10.3365-3367.1997
Sato, T., and Kobayashi, Y. (1998). The ars operon in the skin element of Bacillus subtilis confers resistance to arsenate and arsenite. J. Bacteriol. 180, 1655-1661.
Shen, Z., Luangtongkum, T., Qiang, Z., Jeon, B., Wang, L., and Zhang, Q. (2014). Identification of a novel membrane transporter mediating resistance to organic arsenic in Campylobacter jejuni. Antimicrob. Agents Chemother. 58, 2021-2029. doi: 10.1128/AAC.02137-13
Silver, S., and Keach, D. (1982). Energy-dependent arsenate efflux: the mechanism of plasmidmediated resistance. Proc. Natl. Acad. Sci. U. S. A. 79, 6114-6118. doi: 10.1073/pnas.79.20.6114
Silver, S., and Phung, L. T. (2005a). Genes and enzymes involved in bacterial oxidation and reduction of inorganic arsenic. Appl. Environ. Microbiol. 71, 599-608. doi: 10.1128/AEM.71.2.599-608.2005
Silver, S., and Phung, L. T. (2005b). A bacterial view of the periodic table: genes and proteins for toxic inorganic ions. J. Ind. Microbiol. Biotechnol. 32, 587-605. doi: 10.1007/s10295-005-0019-6
Stauder, S., Raue, B., and Sacher, F. (2005). Thioarsenates in sulfidic waters. Environ. Sci. Technol. 39, 5933-5939. doi: 10.1021/es048034k
Stolz, J. F., Basu, P., Santini, J. M., and Oremland, R. S. (2006). Arsenic and selenium in microbial metabolism. Annu. Rev. Microbiol. 60, 107-130. doi: 10.1146/annurev. micro.60.080805.142053
Suzuki, K., Wakao, N., Kimura, T., Sakka, K., and Ohmiya, K. (1998). Expression and regulation of the arsenic resistance operon of Acidiphilium multivorum AIU 301 plasmid pKW301 in Escherichia coli. Appl. Environ. Microbiol. 64, 411-418.
Thomas, F., Diaz-Bone, R. A., Wuerfel, O., Huber, B., Weidenbach, K., Schmitz, R. A., et al. (2011). Connection between multimetal (loid) methylation in methanoarchaea and central intermediates of methanogenesis. Appl. Environ. Microbiol. 77, 8669-8675. doi: 10.1128/Aem.06406-11
Tuffin, I. M., De Groot, P., Deane, S. M., and Rawlings, D. E. (2005). An unusual Tn21-like transposon containing an ars operon is present in highly arsenic-resistant strains of the biomining bacterium Acidithiobacillus caldus. Microbiology 151(Pt 9), 3027-3039. doi: 10.1099/mic.0.28131-0
Tuffin, I. M., Hector, S. B., Deane, S. M., and Rawlings, D. E. (2006). Resistance determinants of a highly arsenic-resistant strain of Leptospirillum ferriphilum isolated from a commercial biooxidation tank. Appl. Environ. Microbiol. 72, 2247-2253. doi: 10.1128/AEM.72.3.2247-2253.2006
Wang, G., Kennedy, S. P., Fasiludeen, S., Rensing, C., and DasSarma, S. (2004). Arsenic resistance in Halobacterium sp. strain NRC-1 examined by using an improved gene knockout system. J. Bacteriol. 186, 3187-3194. doi: 10.1128/JB.186.10.3187-3194.2004
Wang, L., Chen, S., Xiao, X., Huang, X., You, D., Zhou, X., et al. (2006). arsRBOCT arsenic resistance system encoded by linear plasmid pHZ227 in Streptomyces sp. strain FR-008. Appl. Environ. Microbiol. 72, 3738-3742. doi: 10.1128/AEM.72.5.3738-3742.2006
Wang, L., Jeon, B., Sahin, O., and Zhang, Q. (2009). Identification of an arsenic resistance and arsenicsensing system in Campylobacter jejuni. Appl. Environ. Microbiol. 75, 5064-5073. doi: 10.1128/AEM.00149-09
Wu, B., Song, J., and Beitz, E. (2010). Novel channel enzyme fusion proteins confer arsenate resistance. J. Biol. Chem. 285, 40081-40087. doi: 10.1074/jbc. M110.184457
Wu, G., Huang, L. Q., Jiang, H. C., Peng, Y., Guo, W., Chen, Z. Y., et al. (2017). Thioarsenate formation coupled with anaerobic arsenite oxidation by a sulfate-reducing bacterium isolated from a hot spring. Front. Microbiol. 8:1336. doi: 10.3389/fmicb.2017.01336
Yan, Y., Ye, J., Xue, X. M., and Zhu, Y. G. (2015). Arsenic demethylation by a C. As lyase in cyanobacterium Nostoc sp. PCC 7120. Environ. Sci. Technol. 49, 14350-14358. doi: 10.1021/acs.est.5b03357
Yang, H. C., Cheng, J., Finan, T. M., Rosen, B. P., and Bhattacharjee, H. (2005). Novel pathway for arsenic detoxification in the legume symbiont Sinorhizobium meliloti. J. Bacteriol. 187, 6991-6997. doi: 10.1128/JB.187.20.6991-6997.2005
Yang, H. C., Fu, H. L., Lin, Y. F., and Rosen, B. P. (2012). Pathways of arsenic uptake and efflux. Curr. Top. Membr. 69, 325-358. doi: 10.1016/B978-0-12-394390-3.00012-4
Yang, H. C., and Rosen, B. P. (2016). New mechanisms of bacterial arsenic resistance. Biomed. J. 39, 5-13. doi: 10.1016/j.bj.2015.08.003
Yang, Y., Wu, S., Lilley, R. M., and Zhang, R. (2015). The diversity of membrane transporters encoded in bacterial arsenic-resistance operons. PeerJ 3:e943. doi: 10.7717/peerj.943
Yoshinaga, M., and Rosen, B. P. (2014). A C. As lyase for degradation of environmental organoarsenical herbicides and animal husbandry growth promoters. Proc. Natl. Acad. Sci. U. S. A. 111, 7701-7706. doi: 10.1073/pnas.1403057111
Yuan, C., Lu, X., Qin, J., Rosen, B. P., and Le, X. C. (2008). Volatile arsenic species released from Escherichia coli expressing the AsIII S-adenosylmethionine methyltransferase gene. Environ. Sci. Technol. 42, 3201-3206. doi: 10.1021/es702910g
Zhao, C., Zhang, Y., Chan, Z., Chen, S., and Yang, S. (2015). Insights into arsenic multi-operons expression and resistance mechanisms in Rhodopseudomonas palustris CGA009. Front. Microbiol. 6:986. doi: 10.3389/fmicb.2015.00986
Zhu, Y. G., Yoshinaga, M., Zhao, F. J., and Rosen, B. P. (2014). Earth abides arsenic biotransformations. Annu. Rev. Earth Planet Sci. 42, 443-467. doi: 10.1146/annurev-earth-060313-054942
