Abstract
A highly arsenic-metabolizing bacterial strain was isolated from an agricultural field known for arsenic contamination near Munshiganj (Bangladesh). Based on 16S rRNA gene analysis, the strain was identified as Micrococcus luteus and designated as strain BPB1. Arsenate and arsenite minimal inhibitory concentrations of 650 mM and 7.5 mM, respectively, were observed for strain BPB1, slightly higher than the figures observed in its close relative M. luteus DSM 20030T. Such observations were consistent with the presence of arsenic-metabolizing genes in the genome of M. luteus. We describe this strain as having an MSH/Mrx-dependent class of arsenate reductase, and an arsenite transporter family in the ACR3(1) group. Besides an intracellular arsenic resistance mechanism, experiments carried out using field emission scanning electron microscopy-energy dispersive X-ray spectroscopy (FESEM-EDS) and Fourier transform infrared spectroscopy (FTIR) demonstrated the ability of BPB1 to sequester arsenate in extracellular polymeric substances on its cell surface.
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References
Aaltonen EK, Silow M (2008) Transmembrane topology of the Acr3 family arsenite transporter from Bacillus subtilis. Biochim Biophys Acta 1778:963–973. doi:10.1016/j.bbamem.2007.11.011
Abruzzi RC, Dedavid BA, Pires MJR, Ferrarini SF (2013) Relationship between density and anatomical structure of different species of Eucalyptus and identification of preservatives. Mater Res 16:1428–1438
Achour AR, Bauda P, Billard P (2007) Diversity of arsenite transporter genes from arsenic-resistant soil bacteria. Res Microbiol 158:128–137. doi:10.1016/j.resmic.2006.11.006
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 107:145–156. doi:10.1111/j.1365-2672.2009.04188.x
Bhattacharya P et al (2009) Groundwater chemistry and arsenic mobilization in the Holocene flood plains in south-central Bangladesh. Environ Geochem Health 31(Suppl 1):23–43. doi:10.1007/s10653-008-9230-5
Bhattacharya P, Welch AH, Stollenwerk KG, McLaughlin MJ, Bundschuh J, Panaullah G (2007) Arsenic in the environment: biology and chemistry. Sci Total Environ 379:109–120. doi:10.1016/j.scitotenv.2007.02.037
Branco R, Chung AP, Morais PV (2008) Sequencing and expression of two arsenic resistance operons with different functions in the highly arsenic-resistant strain Ochrobactrum tritici SCII24T. BMC Microbiol 8:95. doi:10.1186/1471-2180-8-95
Carlin A, Shi W, Dey S, Rosen BP (1995) The ars operon of Escherichia coli confers arsenical and antimonial resistance. J Bacteriol 177:981–986
Chen Y, Dey S, Rosen BP (1996) Soft metal thiol chemistry is not involved in the transport of arsenite by the Ars pump. J Bacteriol 178:911–913
Chen Z, Zhu YG, Liu WJ, Meharg AA (2005) Direct evidence showing the effect of root surface iron plaque on arsenite and arsenate uptake into rice (Oryza sativa) roots. New Phytol 165:91–97. doi:10.1111/j.1469-8137.2004.01241.x
Davies JA et al (2007) The GacS sensor kinase controls phenotypic reversion of small colony variants isolated from biofilms of Pseudomonas aeruginosa PA14. FEMS Microbiol Ecol 59:32–46. doi:10.1111/j.1574-6941.2006.00196.x
Efron B, Halloran E, Holmes S (1996) Bootstrap confidence levels for phylogenetic trees. Proc Natl Acad Sci USA 93:13429–13434
Flanagan SV, Johnston RB, Zheng Y (2012) Arsenic in tube well water in Bangladesh: health and economic impacts and implications for arsenic mitigation. Bull World Health Organ 90:839–846. doi:10.2471/blt.11.101253
Fu HL et al (2009) Properties of arsenite efflux permeases (Acr3) from Alkaliphilus metalliredigens and Corynebacterium glutamicum. J Biol Chem 284:19887–19895. doi:10.1074/jbc.M109.011882
Giri AK, Patel RK, Mahapatra SS, Mishra PC (2013) Biosorption of arsenic (III) from aqueous solution by living cells of Bacillus cereus. Environ Sci Pollut Res Int 20:1281–1291. doi:10.1007/s11356-012-1249-6
Giri AK, Patel RK, Mishra PC (2012) Biosorption of As(V) from aqueous solutions by living cells of Bacillus cereus. Water Sci Technol 66:1699–1707. doi:10.2166/wst.2012.332
Goldstein J et al (2012) Scanning electron microscopy and X-ray microanalysis: a text for biologists, materials scientists, and geologists. Springer, Berlin
Jia Y, Huang H, Zhong M, Wang F, Zhang L, Zhu Y (2013) Microbial arsenic methylation in soil and rice rhizosphere. Environ Sci Technol 47:3141–3148
Kim OS et al (2012) Introducing EzTaxon-e: a prokaryotic 16S rRNA gene sequence database with phylotypes that represent uncultured species. Int J Syst Evol Microbiol 62:716–721. doi:10.1099/ijs.0.038075-0
Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120
Lievremont D, Bertin PN, Lett MC (2009) Arsenic in contaminated waters: biogeochemical cycle, microbial metabolism and biotreatment processes. Biochimie 91:1229–1237. doi:10.1016/j.biochi.2009.06.016
Lin YF, Walmsley AR, Rosen BP (2006) An arsenic metallochaperone for an arsenic detoxification pump. Proc Natl Acad Sci USA 103:15617–15622. doi:10.1073/pnas.0603974103
Liu J, Gladysheva TB, Lee L, Rosen BP (1995) Identification of an essential cysteinyl residue in the ArsC arsenate reductase of plasmid R773. Biochemistry 34:13472–13476
Lopez-Maury L, Florencio FJ, Reyes JC (2003) Arsenic sensing and resistance system in the cyanobacterium Synechocystis sp. strain PCC 6803. J Bacteriol 185:5363–5371
Maldonado J et al (2010) Isolation and identification of a bacterium with high tolerance to lead and copper from a marine microbial mat in Spain. Ann Microbiol 60:113–120
Mohan D, Pittman CU Jr (2007) Arsenic removal from water/wastewater using adsorbents—a critical review. J Hazard Mater 142:1–53. doi:10.1016/j.jhazmat.2007.01.006
Mukhopadhyay R, Shi J, Rosen BP (2000) Purification andcharacterization of Acr2p, theSaccharomyces cerevisiaearsenate reductase.J Biol Chem275: 21149–21157
Muller D 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
Oden KL, Gladysheva TB, Rosen BP (1994) Arsenate reduction mediated by the plasmid-encoded ArsC protein is coupled to glutathione. Mol Microbiol 12:301–306
Ordonez E et al (2009) Arsenate reductase, mycothiol, and mycoredoxin concert thiol/disulfide exchange. J Biol Chem 284:15107–15116. doi:10.1074/jbc.M900877200
Raza FA, Faisal M (2013) Growth promotion of maize by desiccation tolerant ‘Micrococcus luteus’-chp37 isolated from Cholistan desert, Pakistan. Aust J Crop Sci 7:1693
Rose TM, Henikoff JG, Henikoff S (2003) CODEHOP (COnsensus-DEgenerate Hybrid Oligonucleotide Primer) PCR primer design. Nucleic Acids Res 31:3763–3766
Rosen BP (2002a) Biochemistry of arsenic detoxification. FEBS Lett 529:86–92
Rosen BP (2002b) Transport and detoxification systems for transition metals, heavy metals and metalloids in eukaryotic and prokaryotic microbes. Comp Biochem Physiol A Mol Integr Physiol 133:689–693
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425
Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning vol 2. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
Sandhya V, Ali SKZ, Grover M, Reddy G, Venkateswarlu B (2009) Alleviation of drought stress effects in sunflower seedlings by the exopolysaccharides producing Pseudomonas putida strain GAP-P45. Biol Fertil Soils 46:17–26. doi:10.1007/s00374-009-0401-z
Sato T, Kobayashi Y (1998) The ars operon in the skin element of Bacillus subtilis confers resistance to arsenate and arsenite. J Bacteriol 180:1655–1661
Seki H, Suzuki A, Maruyama H (2005) Biosorption of chromium(VI) and arsenic(V) onto methylated yeast biomass. J Colloid Interface Sci 281:261–266. doi:10.1016/j.jcis.2004.08.167
Severin KP (2004) Energy dispersive spectrometry of common rock forming minerals. Kluwer, Dordrecht
Srivastava NK, Majumder CB (2008) Novel biofiltration methods for the treatment of heavy metals from industrial wastewater. J Hazard Mater 151:1–8. doi:10.1016/j.jhazmat.2007.09.101
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739. doi:10.1093/molbev/msr121
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729
Tsai SL, Singh S, Chen W (2009) Arsenic metabolism by microbes in nature and the impact on arsenic remediation. Curr Opin Biotechnol 20:659–667. doi:10.1016/j.copbio.2009.09.013
van Geen A et al (2006) Impact of irrigating rice paddies with groundwater containing arsenic in Bangladesh. Sci Total Environ 367:769–777. doi:10.1016/j.scitotenv.2006.01.030
Vieira RH, Volesky B (2000) Biosorption: a solution to pollution? Int Microbiol 3:17–24
Villadangos AF et al (2010) Retention of arsenate using genetically modified coryneform bacteria and determination of arsenic in solid samples by ICP-MS. Talanta 80:1421–1427. doi:10.1016/j.talanta.2009.09.046
Villadangos AF et al (2011) Corynebacterium glutamicum survives arsenic stress with arsenate reductases coupled to two distinct redox mechanisms. Mol Microbiol 82:998–1014. doi:10.1111/j.1365-2958.2011.07882.x
Wei G, Fan L, Zhu W, Fu Y, Yu J, Tang M (2009) Isolation and characterization of the heavy metal resistant bacteria CCNWRS33-2 isolated from root nodule of Lespedeza cuneata in gold mine tailings in China. J Hazard Mater 162:50–56. doi:10.1016/j.jhazmat.2008.05.040
Weisburg WG, Barns SM, Pelletier DA, Lane DJ (1991) 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173:697–703
Wu J, Tisa LS, Rosen BP (1992) Membrane topology of the ArsB protein, the membrane subunit of an anion-translocating ATPase. J Biol Chem 267:12570–12576
Wysocki R, Bobrowicz P, Ulaszewski S (1997) The Saccharomyces cerevisiae ACR3 gene encodes a putative membrane protein involved in arsenite transport. J Biol Chem 272:30061–30066
Wysocki R, Clemens S, Augustyniak D, Golik P, Maciaszczyk E, Tamas MJ, Dziadkowiec D (2003) Metalloid tolerance based on phytochelatins is not functionally equivalent to the arsenite transporter Acr3p. Biochem Biophys Res Commun 304:293–300
Xia X et al (2008) Investigation of the structure and function of a Shewanella oneidensis arsenical-resistance family transporter. Mol Membr Biol 25:691–705. doi:10.1080/09687680802535930
Yang HC, Fu HL, Lin YF, Rosen BP (2012) Pathways of arsenic uptake and efflux. Curr Top Membr 69:325–358. doi:10.1016/b978-0-12-394390-3.00012-4
Young M et al (2010) Genome sequence of the Fleming strain of Micrococcus luteus, a simple free-living actinobacterium. J Bacteriol 192:841–860. doi:10.1128/jb.01254-09
Acknowledgements
The authors acknowledge the Department of Biotechnology (Government of India, New Delhi) for grant vide BT/PR10897/GBD/27/117/2008. V.K.B. acknowledges the University Grants Commission for the award of Research Fellowship (20-12/2009(ii)EU-IV). The authors acknowledge Barry P. Rosen, FIU College of Medicine for providing ars mutant strains.
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Vijay, V., Vandana, K.B., Mathan Kumar, R. et al. Genetic analysis of arsenic metabolism in Micrococcus luteus BPB1, isolated from the Bengal basin. Ann Microbiol 67, 79–89 (2017). https://doi.org/10.1007/s13213-016-1239-x
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DOI: https://doi.org/10.1007/s13213-016-1239-x