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Response of soil bacterial communities to lead and zinc pollution revealed by Illumina MiSeq sequencing investigation

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Abstract

Soil provides a critical environment for microbial community development. However, microorganisms may be sensitive to substances such as heavy metals (HMs), which are common soil contaminants. This study investigated bacterial communities using 16S ribosomal RNA (rRNA) gene fragment sequencing in geographic regions with and without HM pollution to elucidate the effects of soil properties and HMs on bacterial communities. No obvious changes in the richness or diversity of bacterial communities were observed between samples from mining and control areas. Significant differences in bacterial richness and diversity were detected between samples from different geographic regions, indicating that the basic soil characteristics were the most important factors affecting bacterial communities other than HMs. However, the abundances of several phyla and genera differed significantly between mining and control samples, suggesting that Zn and Pb pollution may impact the soil bacterial community composition. Moreover, regression analyses showed that the relative abundances of these phyla and genera were correlated significantly with the soil-available Zn and Pb contents. Redundancy analysis indicated that the soil K, ammoniacal nitrogen (NH4 +–N), total Cu, and available Zn and Cu contents were the most important factors. Our results not only suggested that the soil bacteria were sensitive to HM stresses but also indicated that other soil properties may affect soil microorganisms to a greater extent.

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References

  • Bansal S, Kapoor KK (2000) Vermicomposting of crop residues and cattle dung with Eisenia foetida. Bioresour Technol 73:95–98

    Article  CAS  Google Scholar 

  • Bardgett RD, Lovell RD, Hobbs PJ, Jarvis SC (1999) Seasonal changes in soil microbial communities along a fertility gradient of temperate grasslands. Soil Biol Biochem 31:1021–1030

    Article  CAS  Google Scholar 

  • Bates ST, Berg-Lyons D, Caporaso JG, Walters WA, Knight R, Fierer N (2011) Examining the global distribution of dominant archaeal populations in soil. ISME J 5:908–917

    Article  CAS  Google Scholar 

  • Berg J, Brandt KK, Al-Soud WA, Holm PE, Hansen LH, Sørensen SJ, Nybroe O (2012) Selection for Cu-tolerant bacterial communities with altered composition, but unaltered richness, via long-term Cu exposure. Appl Environ Microbiol 78:7438–7446

    Article  CAS  Google Scholar 

  • Bruins MR, Kapil S, Oehme FW (2000) Microbial resistance to metals in the environment. Ecotox Environ Safe 45:198–207

    Article  CAS  Google Scholar 

  • Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336

    Article  CAS  Google Scholar 

  • Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Lozupone CA, Turnbaugh PJ, Fierer N, Knight R (2011) Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc Natl Acad Sci U S A 1:4516–4522

    Article  Google Scholar 

  • Chen J, Wei F, Zheng C, Wu Y, Adriano DC (1991) Background concentrations of elements in soils of China. Water Air Soil Pollut 57:699–712

    Article  Google Scholar 

  • Chen X, Zhang LM, Shen JP, Xu ZH, He JZ (2010) Soil type determines the abundance and community structure of ammonia-oxidizing bacteria and archaea in flooded paddy soils. J Soils Sediments 10:1510–1516

    Article  CAS  Google Scholar 

  • Chen JH, He F, Zhang XH, Sun X, Zheng JF, Zheng JW (2014) Heavy metal pollution decreases microbial abundance, diversity and activity within particle-size fractions of a paddy soil. FEMS Microbiol Ecol 87:164–181

    Article  CAS  Google Scholar 

  • Chen C, Zhang J, Lu M, Qin C, Chen Y, Yang L, Huang Q, Wang J, Shen Z, Shen Q (2016) Microbial communities of an arable soil treated for 8 years with organic and inorganic fertilizers. Biol Fertil Soils 52:455–467

    Article  CAS  Google Scholar 

  • Chodak M, Gołębiewski M, Morawska-Płoskonka J, Kuduk K, Niklińska M (2013) Diversity of microorganisms from forest soils differently polluted with heavy metals. Appl Soil Ecol 64:7–14

    Article  Google Scholar 

  • Delmont TO, Francioli D, Jacquesson S, Laoudi S, Mathieu A, Nesme J, Ceccherini MT, Nannipieri P, Simonet P, Vogel TM (2014) Microbial community development and unseen diversity recovery in inoculated sterile soil. Biol Fertil Soils 50:1069–1076

    Article  CAS  Google Scholar 

  • Doran JW (1980) Soil microbial and biochemical changes associated with reduced tillage. Soil Sci Soc Am J 44:765–771

    Article  CAS  Google Scholar 

  • Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10:996–998

    Article  CAS  Google Scholar 

  • Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200

    Article  CAS  Google Scholar 

  • Etten EV (2005) Multivariate analysis of ecological data using CANOCO. Austral Eco 30:486–487

    Article  Google Scholar 

  • Falkowski PG, Fenchel T, Delong EF (2008) The microbial engines that drive Earth’s biogeochemical cycles. Science 320:1034–1039

    Article  CAS  Google Scholar 

  • Frische T, Hoper H (2003) Soil microbial parameters and luminescent bacteria assays as indicators for in situ bioremediation of TNTcontaminated soils. Chemosphere 50:415–427

    Article  Google Scholar 

  • Frostegård Å, Tunlid A, Bååth E (1993) Phospholipid fatty acid composition, biomass, and activity of microbial communities from two soil types experimentally exposed to different heavy metals. Appl Environ Microbiol 59:3605–3617

    Google Scholar 

  • Fu F, Wang Q (2011) Removal of heavy metal ions from wastewaters: a review. J Environ Manag 92:407–418

    Article  CAS  Google Scholar 

  • Gans J, Wolinsky M, Dunbar J (2005) Computational improvements reveal great bacterial diversity and highmetal toxicity in soil. Science 309:1387–1390

    Article  CAS  Google Scholar 

  • Gołębiewski M, Deja-Sikora E, Cichosz M, Tretyn A, Wróbel B (2014) 16S rDNA pyrosequencing analysis of bacterial community in heavy metals polluted soils. Microb Ecol 67:635–647

    Article  Google Scholar 

  • Hobman J, Yamamoto K, Oshima T (2007) Transcriptomic responses of bacterial cells to sublethal metal ion stress. In: Nies D, Silver S (eds) Molecular microbiology of heavy metals. Microbiology monographs. Springer, Berlin, pp. 73–115

    Chapter  Google Scholar 

  • Hong C, Si Y, Xing Y, Li Y (2015) Illumina MiSeq sequencing investigation on the contrasting soil bacterial community structures in different iron mining areas. Environ Sci Pollut Res 22:10788–10799

    Article  CAS  Google Scholar 

  • Hu HW, Zhang LM, Dai Y, Di HJ, He JZ (2013) pH-dependent distribution of soil ammonia oxidizers across a large geographical scale as revealed by high-throughput pyrosequencing. J Soils Sediments 13:1439–1449

    Article  Google Scholar 

  • Kabata A, Pendias H (2001) Trace elements in soils and plants. CRC, Washington DC

    Google Scholar 

  • Kasassi A, Rakimbei P, Karagiannidis A, Zabaniotou A, Tsiouvaras K, Nastis A, Tzafeiropoulou K (2008) Soil contamination by heavy metals: measurements from a closed unlined landfill. Biores Technol 99:8578–8584

    Article  CAS  Google Scholar 

  • Khan S, Hesham AE, Qiao M, Rehman S, He JZ (2010) Effects of Cd and Pb on soil microbial community structure and activities. Environ Sci Pollut Res 17:288–296

    Article  CAS  Google Scholar 

  • Landa M, Cottrell MT, Kirchman DL, Blain S, Obernosterer I (2013) Changes in bacterial diversity in response to dissolved organic matter supply in a continuous culture experiment. Aquat Microb Ecol 69:157–168

    Article  Google Scholar 

  • Landa M, Cottrell MT, Kirchman DL, Kaiser K, Medeiros PM, Tremblay L, Batailler N, Caparros J, Catala P, Escoubeyrou K, Oriol L, Blain S, Obernosterer I (2014) Phylogenetic and structural response of heterotrophic bacteria to dissolved organic matter of different chemical composition in a continuous culture study. Environ Microbiol 16:1668–1681

    Article  CAS  Google Scholar 

  • Lanzén A, Simachew A, Gessesse A, Chmolowska D, Jonassen I, Øvreås L (2013) Surprising prokaryotic and eukaryotic diversity, community structure and biogeography of Ethiopian soda lakes. PLoS One 8:e72577

    Article  Google Scholar 

  • Lauber CL, Hamady M, Knight R, Fierer N (2009) Pyrosequencing-based assessment of soil pH as a predictor of soil bacterial community structure at the continental scale. Appl Environ Microbiol 75:5111–5120

    Article  CAS  Google Scholar 

  • Li J, Hu HW, Ma YB, Wang JT, Liu YR, He JZ (2015) Long-term nickel exposure altered the bacterial community composition but not diversity in two contrasting agricultural soils. Environ Sci Pollut Res 22:10496–10505

    Article  CAS  Google Scholar 

  • Lorenz N, Hintemann T, Kramarewa T, Katayama A, Yasuta T, Marschner P, Kandeler E (2006) Response of microbial activity and microbial community composition in soils to long-term arsenic and cadmium exposure. Soil Biol Biochem 38:1430–1437

    Article  CAS  Google Scholar 

  • Macdonald CA, Clark IM, Zhao FJ, Hirsch PR, Singh BK, McGrath SP (2011) Long-term impacts of zinc and copper enriched sewage sludge additions on bacterial, archaeal and fungal communities in arable and grassland soils. Soil Biol Biochem 43:932–941

    Article  CAS  Google Scholar 

  • Margesin R, Płaza GA, Kasenbacher S (2011) Characterization of bacterial communities at heavy-metal-contaminated sites. Chemosphere 82:1583–1588

    Article  CAS  Google Scholar 

  • Miransari M (2013) Soil microbes and the availability of soil nutrients. Acta Physiol Plant 5:3075–3084

    Article  Google Scholar 

  • Müller AK, Westergaard K, Christensen S, Sørensen SJ (2001) The effect of long-term mercury pollution on the soil microbial community. FEMS Microbiol Ecol 36:11–19

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Nies DH (2003) Efflux-mediated heavy metal resistance in prokaryotes. FEMS Microbiol Rev 27:313–339

    Article  CAS  Google Scholar 

  • Niklińska M, Chodak M, Laskowski R (2005) Characterization of the forest humus microbial community in a heavy metal polluted area. Soil Biol Biochem 37:2185–2194

    Article  Google Scholar 

  • Pereira LB, Vicentini R, Ottoboni LM (2014) Changes in the bacterial community of soil from a neutral mine drainage channel. PLoS One 9:e96605

    Article  Google Scholar 

  • Pérez-de-Mora A, Burgos P, Madejón E, Cabrera F, Jaeckel P, Schloter M (2006) Microbial community structure and function in a soil contaminated by heavy metals: effects of plant growth and different amendments. Soil Biol Biochem 38:327–341

    Article  Google Scholar 

  • Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microb 75:7537–7541

    Article  CAS  Google Scholar 

  • Shen JP, Xu ZH, He JZ (2014) Frontiers in the microbial processes of ammonia oxidation in soils and sediments. J Soils Sediments 14:1023–1029

    Article  CAS  Google Scholar 

  • Singh BK, Quince C, Macdonald CA, Khachane A, Thomas N, Al-Soud WA, Sørensen SJ, He ZL, White D, Sinclair A, Crooks B, Zhou JZ, Campbell CD (2014) Loss of microbial diversity in soils is coincident with reductions in some specialized functions. Environ Microbiol 16:2408–2420

    Article  Google Scholar 

  • Sørensen SJ, Bailey M, Hansen LH, Kroer N, Wuertz S (2005) Studying plasmid horizontal transfer in situ: a critical review. Nat Rev Microbiol 3:700–710

    Article  Google Scholar 

  • Ulrich A, Becker R (2006) Soil parent material is a key determinant of the bacterial community structure in arable soils. FEMS Microbiol Ecol 56:430–443

    Article  CAS  Google Scholar 

  • Valls M, de Lorenzo V (2002) Exploiting the genetic and biochemical capacities of bacteria for the remediation of heavy metal pollution. FEMS Microbiol Rev 26:327–338

    Article  CAS  Google Scholar 

  • Vishnivetskaya TA, Mosher JJ, Palumbo AV, Yang ZK, Podar M, Brown SD, Brooks SC, Gu B, Southworth GR, Drake MM, Brandt CC, Elias DA (2011) Mercury and other heavy metals influence bacterial community structure in contaminated Tennessee streams. Appl Environ Microbiol 77:302–311

    Article  CAS  Google Scholar 

  • Wani PA, Khan MS, Zaidi A (2007) Effect of metal tolerant plant growth promoting Bradyrhizobium sp. (vigna) on growth, symbiosis, seed yield and metal uptake by greengram plants. Chemosphere 70:36–45

    Article  CAS  Google Scholar 

  • Wcisło E, Ioven D, Kucharski R, Szdzuj J (2002) Human health risk assessment case study an abandoned metal smelter site in Poland. Chemosphere 47:507–515

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Zhao H, Xia B, Fan C, Zhao P, Shen S (2012) Human health risk from soil heavy metal contamination under different land uses near Dabaoshan mine, southern China. Sci Total Environ 417:45–54

    Article  Google Scholar 

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Acknowledgments

The research was funded by the National Natural Science Foundation of China (31400328 and 31501689) and the Science Foundation of Jiangsu Province, China (BK20140697 and BK20150670).

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Correspondence to Zhenguo Shen.

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Responsible Editor: Zhihong Xu

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Xu, X., Zhang, Z., Hu, S. et al. Response of soil bacterial communities to lead and zinc pollution revealed by Illumina MiSeq sequencing investigation. Environ Sci Pollut Res 24, 666–675 (2017). https://doi.org/10.1007/s11356-016-7826-3

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