Abstract
The sampling sites situated in southwest Slovakia are according to environmental monitoring of Slovakia a part of strongly disturbed environment by heavy metals, mainly by high nickel concentrations. The aim of the present study was to characterise a complete microbial assemblage from a dump containing heavy-metal-contaminated waste as well as from farmland situated nearby this dump by using shotgun sequencing of 16S rDNA amplicons. It was found that nickel influenced both species richness and diversity and that microbiota of both samples differed significantly (Bray-Curtis dissimilarity 0.73) at genus level mainly by abundances of sequences from particular genera and occurrences of the unique genera in individual bacterial communities. In spite of these differences between microbial assemblages, both samples shared many bacterial genera that might constitute the specific nickel-resistant bacterial niche, and it was possible to delineate the core microbiome of our two samples at species level. The core set of 30 species, represented by the phyla Proteobacteria, Firmicutes, Actinobacteria, Bacteroidetes and Cyanobacteria, suggest that these species might form a “core microbiome” of the specific nickel-resistant bacterial niche.
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Abbreviations
- B-C:
-
Bray-Curtis dissimilarity coefficient
- bp:
-
base pair
- Chao 1, Chao 1 index (species richness estimator):
-
CzcA, heavy metal efflux pump (cobalt-zinc-cadmium resistance)
- D:
-
dominance
- H’:
-
Shanon-Wiener diversity index
- I:
-
numbers of reads
- J’:
-
equitability
- nccA:
-
heavy-metal-resistance determinant (nickel-cobalt-cadmium resistance)
- PAHs:
-
polycyclic aromatic hydrocarbons
- PCBs:
-
polychlorinated biphenyls
- R:
-
species richness
- S:
-
Simpson’s index
References
Bohuš P. & Klinda J. 2010. Environmentálna regionalizácia Slovenskej republiky. MZP SR, Bratislava, SAZP, Banská Bystrica. (in Slovak)
Bray J.R. & Curtis J.T. 1957. An ordination of upland forest communities of southern Wisconsin. Ecol. Monogr. 27: 325–349.
Chao A. 1984. Nonparametric estimation of the number of classes in a community. Scand. J. Stat. 11: 265–270.
Cho J., Vergin K., Morris R. & Giovannoni S. 2004. Lentisphaera araneosa gen. nov., sp. nov, a transparent exopolymer producing marine bacterium, and the description of a novel bacterial phylum, Lentisphaerae. Environ. Microbiol. 6: 611–621.
Chodak M., Golebiewski M., Morawska-Ploskonka J., Kuduk K. & Niklińska M. 2013. Diversity of microorganisms from forest soils differently polluted with heavy metals. Appl. Soil. Ecol. 64: 7–14.
DeSantis T.Z., Hugenholtz P., Keller K., Brodie E.L., Larsen N., Piceno Y.M., Phan R. & Andersen G.L. 2006. Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl. Environ. Microbiol. 72: 5069–5072.
Edgar R.C., Haas B.J., Clemente J.C., Quince C. & Knight R. 2011. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27: 2194–2200.
Erbe J.L., Taylor K.B. & Hall L.M. 1995. Metalloregulation of the cyanobacterial smt locus: identification of SmtB binding sites and direct interaction with metals. Nucleic Acids Res. 23: 2472–2478.
Golebiewski M., Deja-Sikora E., Cichosz M., Tretyn A. & Wró-bel B. 2014. 16S rDNA pyrosequencing analysis of bacterial community in heavy metals polluted soils. Microb. Ecol. 67: 635–647.
Harichová J., Karelová E., Pangallo D. & Ferianc P. 2012. Structure analysis of bacterial community and their heavy-metal resistance determinants in the heavy-metal-contaminated soil sample. Biologia 67: 1038–1048.
Harper D.A.T. (ed.) 1999. Numerical Paleobiology. Computer-Based Modelling and Analysis of Fossils and their Distributions. John Wiley & Sons, Chichester, New York, Weinheim, Brisbane, Singapore, Toronto, 468 pp.
Hur M., Kim Y., Song H.-R, Kim J.M., Choi Y.I. & Yi H. 2011. Effect of genetically modified poplars on soil microbial communities during the phytoremediation of waste mine tailings. Appl. Environ. Microbiol. 77: 7611–7619.
Iyaka A.Y. 2011. Nickel in soils: a review of its distribution and impacts. Sci. Res. Essays 6: 6774–6777.
Janssen P.H. 2006. Identifying the dominant soil bacterial taxa in libraries of 16S rRNA and 16S rRNA genes. Appl. Environ. Microbiol. 72: 1719–1728.
Karelová E., Harichová J., Stojnev T., Pangallo D. & Ferianc P. 2011. The isolation of heavy-metal resistant culturable bacteria and resistance determinants from a heavy-metal-contaminated site. Biologia 66: 18–26.
Keller M. & Zengler K. 2004. Tapping into microbial diversity. Nat. Rev. Microbiol. 2: 141–150.
Khan S., Hesham A.E.L., Qiao M., Rehman S. & He J.Z. 2010. Effect of Cd and Pb on soil microbial community structure and activities. Environ. Sci. Polut. Res. 17: 288–296.
Liu H.Y., Probs A. & Liao B. 2005. Metal contamination of soils and crops affected by the Chenzhou lead/zinc mine spill (Hunan, China). Sci. Total Environ. 339: 153–166.
Mason O.U., Hazen T.C., Borglin S., Chain P.S.G., Dubin-sky E.A., Fortney J.L., Han J., Holman H.Y.N., Hultman J., Lamendella R., Mackelprang R., Malfatti S., Tom L.M., Tringe S.G., Woyke T., Zhou J., Rubin E.M. & Jansson J.K. 2012. Metagenome, metatranscriptome and single-cell sequencing reveal microbial response to deepwater horizon oil spill. ISME J. 6: 1715–1727.
Michaeli E., Boltižiar M., Solár V. & Ivanová M. 2012. The landfill of industrial waste - lúženec near the former nickel smelter at Sereď town as an example of environmental load. Zivotné Prostredie 46: 63–68.
Nacke H., Thürmer A., Wollherr A., Will C., Hodac L., Herold N., Schöning I., Schrumpf M. & Daniel R. 2011. Pyrosequencing-based assessment of bacterial community structure along different management types in German forest and grassland soils. PLoS One 6: e17000.
Nešťák Ľ., Bejda M., Bezecný M., Hajdú Z. & Chmelo S. 2007. Územný plán mesta Sereď - zmeny a doplnky 9c. 02/2007, časť C - Komplexná charakteristika a hodnotenie vplyvov na životné prostredie vrátane zdravia, pp. 27–79. (in Slovak)
Nies D.H. 2003. Efflux-mediated heavy metal resistance in prokaryotes. FEMS Microbiol. Rev. 27: 313–339.
Ogilvie L.A. & Grant A. 2008. Linking pollution induced community tolerance (PICT) and microbial community structure in chronically metal polluted estuarine sediments. Mar. Environ. Res. 65: 187–198.
Ondov B.D., Bergman N.H. & Phillippy A.M. 2011. Interactive metagenomic visualization in a Web browser. BMC Bioinformatics 12: 385.
Pechrada J., Sajjaphan K. & Sadowsky M.J. 2010. Structure and diversity of arsenic-resistant bacteria in an old tin mine area of Thailand. J. Microbiol. Biotechnol. 20: 169–178.
Quero G.M., Cassin D., Botter M., Perini L. & Luna G.M. 2015. Patterns of benthic bacterial diversity in coastal areas contaminated by heavy metals, polycyclic aromatic hydrocarbons (PAHs) and polychlorinated biphenyls (PCBs). Front. Microbiol. 6: 1053.
Ranjard L., Lignier L. & Chaussod R. 2006. Cumulative effect of short-term polymetal contamination on soil bacterial community structure. Appl. Environ. Microbiol. 72: 1684–1687.
Remenár M., Karelová E., Harichová J., Zámocký M., Kamlárová A. & Ferianc P. 2015. Isolation of previously uncultivable bacteria from a nickel contaminated soil using a diffusion-chamber-based approach. Appl. Soil Ecol. 95: 115–127.
Schlegel H.G., Cosson J.-P. & Baker A.J.M. 1991. Nickel-hyperaccumulating plants provide a niche for nickel-resistant bacteria. Botanica Acta 104: 18–25.
Schloss P.D., Westcott S.L., Ryabin T., Hall J.R., Hartmann M., Hollister E.B., Lesniewski R.A., Oakley B.B., Parks D.H., Robinson C.J., Sahl J.W., Stres B., Thallinger G.G., Van Horn D.J. & Weber C.F. 2009. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 75: 7537–7541.
Sheik C.S., Mitchell T.W., Rizvi F.Z., Rehman Y., Faisal M., Hasnain S., McInerney M.J. & Krumholz L.R. 2012. Exposure of soil microbial communities to chromium and arsenic alters their diversity and structure. PLoS One 7: e40059.
Szili-Kovács T. 2008. Effect of some metal salts on the cultivable part of soil microbial assemblage in a calcareous loam cropland 6 years after contamination. Acta Biologica Szegediensis 52: 201–204.
Štursa P., Uhlík O., Kurzawová V., Koubek J., Ionescu M., Strohalm M., Lovecká P., Macek T. & Macková M. 2009. Approaches for diversity analysis of cultivable and non-cultivable bacteria in real soil. Plant Soil Environ. 55: 389–396.
Thiyagarajan V., Lau S., Tsoi M., Zhang W. & Qian P.Y. 2010. Monitoring bacterial biodiversity in surface sediment using terminal restriction fragment length polymorphism analysis (T-RFLP): application to coastal environment, pp. 151–163. In: Ishimatsu A. & Lie H.J. (eds), Coastal Environmental and Ecosystem Issues of the East China Sea. Terrapub & Nagasaki University.
Turnbaugh P.J., Ley R.E., Hamady M., Fraser-Liggett C., Knight R. & Gordon J.I. 2007. The human microbiome project: exploring the microbial part of ourselves in a changing world. Nature 449: 804–810.
Wagner M. & Horn M. 2006. The planctomycetes, verrucomi-crobia, chlamydiae and sister phyla comprise a superphy-lum with biotechnological and medical relevance. Curr. Opin. Biotechnol. 17: 241–249.
Will C., Thürmer A., Wollherr A., Nacke H., Herold N., Schrumpf M., Gutknecht J., Wubet T., Buscot F. & Daniel R. 2010. Horizon-specific bacterial community composition of German grassland soils, as revealed by pyrosequencing-based analysis of 16S rRNA genes. Appl. Environ. Microbiol. 76: 6751–6759.
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Remenár, M., Harichová, J., Zámocký, M. et al. Metagenomics of a nickel-resistant bacterial community in an anthropogenic nickel-contaminated soil in southwest Slovakia. Biologia 72, 971–981 (2017). https://doi.org/10.1515/biolog-2017-0117
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DOI: https://doi.org/10.1515/biolog-2017-0117