Abstract
The widespread use of metals influenced many researchers to examine the relationship between heavy metal toxicity and bacterial resistance. In this study, we have inoculated heavy metal-contaminated soil from Janghang region of South Korea in the nickel-containing media (20 mM Ni2+) for the enrichment. Among dozens of the colonies acquired from the several transfers and serial dilutions with the same concentrations of Ni, the strain Ni-2 was chosen for further studies. The isolates were identified for their phylogenetic affiliations using 16S rRNA gene analysis. The strain Ni-2 was close to Cupriavidus metallidurans and was found to be resistant to antibiotics of vancomycin, erythromycin, chloramphenicol, ampicillin, gentamicin, streptomycin, and kanamycin by disk diffusion method. Of the isolated strains, Ni-2 was sequenced for the whole genome, since the Ni-resistance seemed to be better than the other strains. From the genome sequence we have found that there was a total of 89 metal-resistance-related genes including 11 Ni-resistance genes, 41 heavy metal (As, Cd, Zn, Hg, Cu, and Co)-resistance genes, 22 cation-efflux genes, 4 metal pumping ATPase genes, and 11 metal transporter genes.
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References
Bisessar S (1982) Effect of heavy metals on microorganisms in soils near a secondary lead smelter. Water Air Soil Pollut 17:305–308
Bruins MR, Kapil S, Oehme FW (2000) Microbial resistance to metals in the environment. Ecotoxicol Environ Saf 45:198–207. https://doi.org/10.1006/eesa.1999.1860
Costa M, Klein CB (1999) Nickel carcinogenesis, mutation, epigenetics, or selection. Environ Health Perspect 107:A438–A439
Dekker L, Osborne TH, Santini JM (2014) Isolation and identification of cobalt- and caesium-resistant bacteria from a nuclear fuel storage pond. FEMS Microbiol Lett 359:81–84. https://doi.org/10.1111/1574-6968.12562
Filali BK, Taoufik J, Zeroual Y, Dzairi FZ, Talbi M, Blaghen M (2000) Waste water bacterial isolates resistant to heavy metals and antibiotics. Curr Microbiol 41:151–156. https://doi.org/10.1007/s0028400
Hausinger RP (1987) Nickel utilization by microorganisms. Microbiol Rev 51:22–42
Hong S-H, Koo S-Y, Kim S-H, Ryu H-W, Lee I-S, Cho K-S (2010) Rhizoremediation of petroleum and heavy metal-contaminated soil using rhizobacteria and Zea mays. Microbiol Biotechnol Lett 38:329–334
Iwig JS, Rowe JL, Chivers PT (2006) Nickel homeostasis in Escherichia coli—the rcnR-rcnA efflux pathway and its linkage to NikR function. Mol Microbiol 62:252–262. https://doi.org/10.1111/j.1365-2958.2006.05369.x
Janssen PJ et al (2010) The complete genome sequence of Cupriavidus metallidurans strain CH34, a master survivalist in harsh and anthropogenic environments. PLoS One 5:e10433. https://doi.org/10.1371/journal.pone.0010433
Jeong S-K, An J-S, Kim Y-J, Kim G-H, Choi S-I, Nam K-P (2011) Study on heavy metal contamination characteristics and plant bioavailability for soils in the Janghang smelter area. J Soil Groundw Environ 16:42–50
Lee I, Ouk Kim Y, Park SC, Chun J (2016) OrthoANI: an improved algorithm and software for calculating average nucleotide identity. Int J Syst Evol Microbiol 66:1100–1103. https://doi.org/10.1099/ijsem.0.000760
Liesegang H, Lemke K, Siddiqui RA, Schlegel HG (1993) Characterization of the inducible nickel and cobalt resistance determinant cnr from pMOL28 of Alcaligenes eutrophus CH34. J Bacteriol 175:767–778
Lodewyckx C, Taghavi S, Mergeay M, Vangronsveld J, Clijsters H, Dvd Lelie (2001) The effect of recombinant heavy metal-resistant endophytic bacteria on heavy metal uptake by their host plant. Int J Phytoremediation 3:173–187. https://doi.org/10.1080/15226510108500055
Ludwig W et al (2004) ARB: a software environment for sequence data. Nucleic Acids Res 32:1363–1371. https://doi.org/10.1093/nar/gkh293
Macomber L, Hausinger RP (2011) Mechanisms of nickel toxicity in microorganisms. Metallomics 3:1153–1162. https://doi.org/10.1039/C1MT00063B
Mikolay A, Nies DH (2009) The ABC-transporter AtmA is involved in nickel and cobalt resistance of Cupriavidus metallidurans strain CH34. Antonie Van Leeuwenhoek 96:183. https://doi.org/10.1007/s10482-008-9303-6
Nakajima A, Horikoshi T, Sakaguchi T (1981) Studies on the accumulation of heavy metal elements in biological systems. Eur J Appl Microbiol Biotechnol 12:76–83. https://doi.org/10.1007/bf01970038
Niegowski D, Eshaghi S (2007) The CorA family: structure and function revisited. Cell Mol Life Sci 64:2564–2574. https://doi.org/10.1007/s00018-007-7174-z
Nies DH (2000) Heavy metal-resistant bacteria as extremophiles: molecular physiology and biotechnological use of Ralstonia sp CH34. Extremophiles 4:77–82. https://doi.org/10.1007/s007920050140
Nies DH (2003) Efflux-mediated heavy metal resistance in prokaryotes. FEMS Microbiol Rev 27:313–339
Noinaj N, Guillier M, Barnard TJ, Buchanan SK (2010) TonB-dependent transporters: regulation, structure, and function. Annu Rev Microbiol 64:43–60. https://doi.org/10.1146/annurev.micro.112408.134247
Pal A, Choudhuri P, Dutta S, Mukherjee PK, Paul AK (2004) Isolation and characterization of nickel-resistant microflora from serpentine soils of Andaman. World J Microbiol Biotechnol 20:881–886. https://doi.org/10.1007/s11274-004-2776-1
Quast C et al (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41:D590–D596. https://doi.org/10.1093/nar/gks1219
Rajbanshi A (2009) Study on heavy metal resistant bacteria in Guheswori sewage treatment plant. Our Nat 6:52–57
Rajkumar M, Nagendran R, Lee KJ, Lee WH, Kim SZ (2006) Influence of plant growth promoting bacteria and Cr6+ on the growth of Indian mustard. Chemosphere 62:741–748. https://doi.org/10.1016/j.chemosphere.2005.04.117
Roane TM, Kellogg ST (1996) Characterization of bacterial communities in heavy metal contaminated soils. Can J Microbiol 42:593–603
Sabry SA, Ghozlan HA, AbouZeid DM (1997) Metal tolerance and antibiotic resistance patterns of a bacterial population isolated from sea water. J Appl Microbiol 82:245–252. https://doi.org/10.1111/j.1365-2672.1997.tb02858.x
Schmidt T, Schlegel HG (1994) Combined nickel-cobalt-cadmium resistance encoded by the ncc locus of Alcaligenes xylosoxidans 31A. J Bacteriol 176:7045–7054
Shagol CC, Krishnamoorthy R, Kim K, Sundaram S, Sa T (2014) Arsenic-tolerant plant-growth-promoting bacteria isolated from arsenic-polluted soils in South Korea. Environ Sci Pollut Res Int 21:9356–9365. https://doi.org/10.1007/s11356-014-2852-5
Teeling H, Meyerdierks A, Bauer M, Amann R, Glöckner FO (2004) Application of tetranucleotide frequencies for the assignment of genomic fragments. Environ Microbiol 6:938–947. https://doi.org/10.1111/j.1462-2920.2004.00624.x
Tibazarwa C, Wuertz S, Mergeay M, Wyns L, van Der Lelie D (2000) Regulation of the cnr cobalt and nickel resistance determinant of Ralstonia eutropha (Alcaligenes eutrophus) CH34. J Bacteriol 182:1399–1409
von Rozycki T, Nies DH (2008) Cupriavidus metallidurans: evolution of a metal-resistant bacterium. Antonie Van Leeuwenhoek 96:115. https://doi.org/10.1007/s10482-008-9284-5
Wierzba S, Latala A (2010) Biosorption lead(II) and nikel(II) from an aqueous solution by bacterial biomass. Pol J Chem Technol 12:72–78. https://doi.org/10.2478/v10026-010-0038-6
Yoon SH, Ha SM, Lim J, Kwon S, Chun J (2017) A large-scale evaluation of algorithms to calculate average nucleotide identity. Antonie Van Leeuwenhoek 110:1281–1286. https://doi.org/10.1007/s10482-017-0844-4
Zhao X-Q, Wang R-C, Lu X-C, Lu J-J, Li J, Hu H (2012) Tolerance and biosorption of heavy metals by Cupriavidus metallidurans strain XXKD-1 isolated from a subsurface laneway in the Qixiashan Pb–Zn sulfide minery in eastern China. Geomicrobiol J 29:274–286. https://doi.org/10.1080/01490451.2011.619637
Acknowledgements
This research was supported by National Institute of Biological Resources, South Korea, and in part by “Basic Science Research Program” through the National Research Foundation of Korea (NRF) funded by the Ministry of Education (NRF-2016R1D1A3B01012231).
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Communicated by Erko Stackebrandt.
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Lee, S., Khanal, A., Cho, AH. et al. Cupriavidus sp. strain Ni-2 resistant to high concentration of nickel and its genes responsible for the tolerance by genome comparison. Arch Microbiol 201, 1323–1331 (2019). https://doi.org/10.1007/s00203-019-01700-5
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DOI: https://doi.org/10.1007/s00203-019-01700-5