Screening and genome analysis of arsenite-oxidizing strain Bosea sp. AS-1
Author:
  • Article
  • | |
  • Metrics
  • |
  • Reference [48]
  • |
  • Related [20]
  • | | |
  • Comments
    Abstract:

    [Objective] In this study, we aimed to characterize the community structure of arsenite-oxidizing bacteria in Xikuangshan of Hunan Province, and the whole genome of an arsenite-antimonite-oxidizing strain Bosea sp. AS-1 (Abbreviation:AS-1). [Methods] Arsenite-oxidizing bacterial strains were isolated from the samples collected in Xikuangshan, and 16S rRNA genes were sequenced for phylogenic analysis. Whole genome of strain AS-1 was sequenced and analyzed using relevant software and databases for genome assembly, gene prediction and functional annotation. [Results] The arsenite-oxidizing bacteria in Xikuangshan were mainly distributed in α-, β-, γ-Proteobacteria and Firmicutes. AS-1's genome contained one circular chromosome with a size of 5.536 Mb and two plasmids of 189.9 kb and 112.1 kb, respectively. Further analysis on AS-1's genomic data reveal many genes related to arsenic and antimony metabolism, as well as flagella formation, flagellar movement, and biofilm formation. These genes may be involved in AS-1's resistance to high level of arsenic and antimony in environment. Besides, several carbon-fixation genes and sulfur-oxidizing genes were also found in the genome of AS-1, suggesting that AS-1 may grow autotrophically and oxidize sulfur. [Conclusion] Subsequent experiments confirmed autotrophic growth of AS-1.

    Reference
    [1] Ali H, Khan E, Sajad MA. Phytoremediation of heavy metals-concepts and applications. Chemosphere, 2013, 91:869-881.
    [2] Feng RW, Wei CY, Tu SX, Ding YZ, Wang RG, Guo JK. The uptake and detoxification of antimony by plants:a review. Environmental and Experimental Botany, 2013, 96:28-34.
    [3] Filella M, Belzile N, Chen YW. Antimony in the environment:a review focused on natural waters:I. Occurrence. Earth-Science Reviews, 2002, 57(1/2):125-176.
    [4] Wang N, Lu XL, Wu MXJ, Wang M, Wang HM. Progress in microbial oxidation of As(III) and Sb(III). Microbiology China, 2017, 44(3):689-700. (in Chinese) 王年, 鲁小璐, 邬梦晓俊, 王猛, 王红梅. 微生物氧化As(III)和Sb(III)的研究进展. 微生物学通报, 2017, 44(3):689-700.
    [5] Reimann C, Matschullat J, Birke M, Salminen R. Antimony in the environment:lessons from geochemical mapping. Applied Geochemistry, 2010, 25(2):175-198.
    [6] Oremland RS, Stolz JF, Hollibaugh JT. The microbial arsenic cycle in Mono Lake, California. FEMS Microbiology Ecology, 2004, 48(1):15-27.
    [7] Quéméneur M, Heinrich-Salmeron A, Muller D, Lièvremont D, Jauzein M, Bertin PN, Garrido F, Joulian C. Diversity surveys and evolutionary relationships of aoxB genes in aerobic arsenite-oxidizing bacteria. Applied and Environmental Microbiology, 2008, 74(14):4567-4573.
    [8] Fan H, Su C, Wang Y, Yao J, Zhao K, Wang Y, Wang G. Sedimentary arsenite-oxidizing and arsenate-reducing bacteria associated with high arsenic groundwater from Shanyin, Northwestern China. Journal of Applied Microbiology, 2008, 105(2):529-539.
    [9] Wysocki R, Chéry CC, Wawrzycka D, Van-Hulle M, Cornelis R, Thevelein JM, Tamás MJ. The glycerol channel Fps1p mediates the uptake of arsenite and antimonite in Saccharomyces cerevisiae. Molecular Microbiology, 2001, 40(6):1391-1401.
    [10] Martin P, DeMel S, Shi J, Gladysheva T, Gatti DL, Rosen BP, Edwards BFP. Insights into the structure, solvation, and mechanism of ArsC arsenate reductase, a novel arsenic detoxification enzyme. Structure, 2001, 9(11):1071-1081.
    [11] Nakajima T, Hayashi K, Nagatomi R, Matsubara K, Moore JE, Millar BC, Matsuda M. Molecular identification of an arsenic four-gene operon in Campylobacter lari. Folia Microbiologica, 2013, 58(3):253-260.
    [12] Kashyap DR, Botero LM, Franck WL, Hassett DJ, McDermott TR. Complex regulation of arsenite oxidation in Agrobacterium tumefaciens. Journal of Bacteriology, 2006, 188(3):1081-1088.
    [13] Muller D, Médigue C, Koechler S, Barbe V, Barakat M, Talla E, Bonnefoy V, Krin E, Arsène-Ploetze F, Carapito C, Chandler M, Cournoyer B, Cruveiller S, Dossat C, Duval S, Heymann M, Leize E, Lieutaud A, Lièvremont D, Makita Y, Mangenot S, Nitschke W, Ortet P, Perdrial N, Schoepp B, Siguier P, Simeonova DD, Rouy Z, Segurens B, Turlin E, Vallenet D, van Dorsselaer A, Weiss S, Weissenbach J, Lett MC, Danchin A, Bertin PN. A tale of two oxidation states:bacterial colonization of arsenic-rich environments. PLoS Genetics, 2007, 3(4):e53.
    [14] Achour AR, Bauda P, Billard P. Diversity of arsenite transporter genes from arsenic-resistant soil bacteria. Research in Microbiology, 2007, 158(2):128-137.
    [15] Chauhan NS, Ranjan R, Purohit HJ, Kalia VC, Sharma R. Identification of genes conferring arsenic resistance to Escherichia coli from an effluent treatment plant sludge metagenomic library. FEMS Microbiology Ecology, 2009, 67(1):130-139.
    [16] Lialikova NN. Stibiobacter senarmontii-a new microorganism oxidizing antimony. Mikrobiologiia, 1974, 43(6):941-943.
    [17] Terry LR, Kulp TR, Wiatrowski H, Miller LG, Oremland SR. Microbiological oxidation of antimony(III) with oxygen or nitrate by bacteria isolated from contaminated mine sediments. Applied and Environmental Microbiology, 2015, 81(24):8478-8488.
    [18] Gourbal B, Sonuc N, Bhattacharjee H, Legare D, Sundar S, Ouellette M, Rosen BP, Mukhopadhyay R. Drug uptake and modulation of drug resistance in Leishmania by an aquaglyceroporin. The Journal of Biological Chemistry, 2004, 279(30):31010-31017.
    [19] Meng YL, Liu ZJ, Rosen BP. As(III) and Sb(III) uptake by GlpF and efflux by ArsB in Escherichia coli. The Journal of Biological Chemistry, 2004, 279(18):18334-18341.
    [20] Lehr CR, Kashyap DR, McDermott TR. New insights into microbial oxidation of antimony and arsenic. Applied and Environmental Microbiology, 2007, 73(7):2386-2389.
    [21] Li JX, Wang Q, Li MS, Yang BR, Shi MM, Guo W, McDermott TR, Rensing C, Wang GJ. Proteomics and genetics for identification of a bacterial antimonite oxidase in Agrobacterium tumefaciens. Environmental Science & Technology, 2015, 49(10):5980-5989.
    [22] Li JX, Yang BR, Shi MM, Yuan K, Guo W, Wang Q, Wang GJ. Abiotic and biotic factors responsible for antimonite oxidation in Agrobacterium tumefaciens GW4. Scientific Reports, 2017, 7:43225.
    [23] Li JX, Qiao ZX, Shi MM, Zhang YX, Wang GJ. Regulation of antimonite oxidation and resistance by the phosphate regulator PhoB in Agrobacterium tumefaciens GW4. Microbiological Research, 2019, 226:10-18.
    [24] Zhou JW, Nyirenda, MT, Xie LN, Li Y, Zhou BL, Zhu Y, Liu HL. Mine waste acidic potential and distribution of antimony and arsenic in waters of the Xikuangshan mine, China. Applied Geochemistry, 2017, 77:52-61.
    [25] Weeger W, Lièvremont D, Perret M, Lagarde F, Hubert JC, Leroy M, Lett MC. Oxidation of arsenite to arsenate by a bacterium isolated from an aquatic environment. Biometals, 1999, 12(2):141-149.
    [26] Rhine ED, Onesios KM, Serfes ME, Reinfelder JR, Young LY. Arsenic transformation and mobilization from minerals by the arsenite oxidizing strain WAO. Environmental Science & Technology, 2008, 42(5):1423-1429.
    [27] Salmassi TM, Venkateswaren K, Satomi M, Newman DK, Hering JG. Oxidation of arsenite by Agrobacterium albertimagni, AOL15, sp. nov., isolated from Hot Creek, California. Geomicrobiology Journal, 2002, 19(1):53-66.
    [28] Yamamura S, Amachi S. Microbiology of inorganic arsenic:from metabolism to bioremediation. Journal of Bioscience and Bioengineering, 2014, 118(1):1-9.
    [29] Liao VHC, Chu YJ, Su YC, Hsiao SY, Wei CC, Liu C, Liu CW, Liao CM, Shen WC, Chang FJ. Arsenite-oxidizing and arsenate-reducing bacteria associated with arsenic-rich groundwater in Taiwan. Journal of Contaminant Hydrology, 2011, 123(1/2):20-29.
    [30] Bhakat K, Chakraborty A, Islam E. Characterization of arsenic oxidation and uranium bioremediation potential of arsenic resistant bacteria isolated from uranium ore. Environmental Science and Pollution Research, 2019, 26(13):12907-12919.
    [31] Lugtu RT, Choi SC, Oh YS. Arsenite oxidation by a facultative chemolithotrophic bacterium SDB1 isolated from mine tailing. The Journal of Microbiology, 2009, 47(6):686-692.
    [32] Wang Q, Qin D, Zhang SZ, Wang L, Li JX, Rensing C, McDermott TR, Wang GJ. Fate of arsenate following arsenite oxidation in Agrobacterium tumefaciens GW4. Environmental Microbiology, 2015, 17(6):1926-1940.
    [33] Cai L, Rensing C, Li XY, Wang GJ. Novel gene clusters ch J, Lett MC, Danchin A, Bertin PN. A tale of two oxidation states:bacterial colonization of arsenic-rich environments. PLoS Genetics, 2007, 3(4):e53.
    [49] Marchal M, Briandet R, Koechler S, Kammerer B, Bertin PN. Effect of arsenite on swimming motility delays surface colonization in Herminiimonas arsenicoxydans. Microbiology, 2010, 156(8):2336-2342.
    [50] Clarke MB, Sperandio V. Transcriptional regulation of flhDC by QseBC and σ 28 (FliA) in enterohaemorrhagic Escherichia coli. Molecular Microbiology, 2005, 57(6):1734-1749.water using hypertolerant Bacillus L-148 sp.:a two-step process. Green Chemistry, 2019, 21(9):2245-2251.
    [36] Lu XL, Zhang YN, Liu CY, Wu MXJ, Wang HM. Characterization of the antimonite-and arsenite-oxidizing bacterium Bosea sp. AS-1 and its potential application in arsenic removal. Journal of Hazardous Materials, 2018, 359:527-534.
    [37] Walczak AB, Yee N, Young LY. Draft genome sequence of Bosea sp. WAO an arsenite and sulfide oxidizer isolated from a pyrite rock outcrop in New Jersey. Standards in Genomic Sciences, 2018, 13:6.
    [38] Shi KX, Wang Q, Fan X, Wang GJ. Proteomics and genetic analyses reveal the effects of arsenite oxidation on metabolic pathways and the roles of AioR in Agrobacterium tumefaciens GW4. Environmental Pollution, 2018, 235:700-709.
    [39] Stolz JF, Oremland RS. Microbial metal and metalloid metabolism:advances and applications. Washington:ASM, 2011.
    [40] Härtig C, Lohmayer R, Kolb S, Horn MA, Inskeep WP, Planer-Friedrich B. Chemolithotrophic growth of the aerobic hyperthermophilic bacterium Thermocrinis ruber OC 14/7/2 on monothioarsenate and arsenite. FEMS Microbiology Ecology, 2014, 90(3):747-760.
    [41] Yuan HZ, Qin HL, Liu SL, Nie SA, Wei WX, Wu JS. Advances in research of molecular ecology of carbon fixation microorganism. Scientia Agricultura Sinica, 2011, 44(14):2951-2958. (in Chinese) 袁红朝, 秦红灵, 刘守龙, 聂三安, 魏文学, 吴金水. 固碳微生物分子生态学研究. 中国农业科学, 2011, 44(14):2951-2958.
    [42] Berg IA, Ramos-Vera WH, Petri A, Huber H, Fuchs G. Study of the distribution of autotrophic CO2 fixation cycles in Crenarchaeota. Microbiology, 2010, 156(1):256-269.
    [43] Ishii M, Miyake T, Satoh T, Sugiyama H, Oshima Y, Kodama T, Igarashi Y. Autotrophic carbon dioxide fixation in Acidianus brierleyi. Archives of Microbiology, 1996, 166(6):368-371.
    [44] Friedrich CG, Rother D, Bardischewsky F, Quentmeier A, Fischer J. Oxidation of reduced inorganic sulfur compounds by bacteria:emergence of a common mechanism? Applied and Environmental Microbiology, 2001, 67(7):2873-2882.
    [45] Bedmar EJ, Robles EF, Delgado MJ. The complete denitrification pathway of the symbiotic, nitrogen-fixing bacterium Bradyrhizobium japonicum. Biochemical Society Transactions, 2005, 33(1):141-144.
    [46] Andres J, Arsène-Ploetze F, Barbe V, Brochier-Armanet C, Cleiss-Arnold J, Coppée JY, Dillies MA, Geist L, Joublin A, Koechler S, Lassalle F, Marchal M, Médigue C, Muller D, Nesme X, Plewniak F, Proux C, Ramírez-Bahena MH, Schenowitz C, Sismeiro O, Vallenet D, Santini JM, Bertin PN. Life in an arsenic-containing gold mine:genome and physiology of the autotrophic arsenite-oxidizing bacterium Rhizobium sp. NT-26. Genome Biology and Evolution, 2013, 5(5):934-953.
    [47] Santini JM, Sly LI, Schnagl RD, Macy JM. A new chemolithoautotrophic arsenite-oxidizing bacterium isolated from a gold mine:phylogenetic, physiological, and preliminary biochemical studies. Applied and Environmental Microbiology, 2000, 66(1):92-97.
    [48] Muller D, Médigue C, Koechler S, Barbe V, Barakat M, Talla E, Bonnefoy V, Krin E, Arsène-Ploetze F, Carapito C, Chandler M, Cournoyer B, Cruveiller S, Dossat C, Duval S, Heymann M, Leize E, Lieutaud A, Lièvremont D, Makita Y, Mangenot S, Nitschke W, Ortet P, Perdrial N, Schoepp B, Siguier P, Simeonova DD, Rouy Z, Segurens B, Turlin E, Vallenet D, van Dorsselaer A, Weiss S, Weissenba
    Cited by
    Comments
    Comments
    分享到微博
    Submit
Get Citation

Chaoyang Liu, Li Xiang, Hongmei Wang, Xiaolu Lu. Screening and genome analysis of arsenite-oxidizing strain Bosea sp. AS-1. [J]. Acta Microbiologica Sinica, 2020, 60(11): 2538-2554

Copy
Share
Article Metrics
  • Abstract:525
  • PDF: 2174
  • HTML: 1936
  • Cited by: 0
History
  • Received:February 14,2020
  • Revised:April 12,2020
  • Online: November 03,2020
Article QR Code