Skip to main content

Advertisement

Log in

Verrucomicrobial elevational distribution was strongly influenced by soil pH and carbon/nitrogen ratio

  • Soils, Sec 3 • Remediation and Management of Contaminated or Degraded Lands • Research Article
  • Published:
Journal of Soils and Sediments Aims and scope Submit manuscript

Abstract

Purpose

The bacterial phylum Verrucomicrobia plays important roles in biogeochemical cycling processes, while the ecology of this phylum is still unclear. Previous elevational studies mainly focused on whole bacterial communities, while no study exclusively picked out Verrucomicrobia. Our objectives were to investigate the abundance, diversity and community composition of soil Verrucomicrobia across an elevation gradient on Changbai Mountain.

Materials and methods

In total, 24 soil samples representing six elevation gradients were collected. Primer set 515F/806R was used for PCR amplifications and sequencing was conducted on an Illumina HiSeq2000 platform. Data sets comprising of Verrucomicrobial phylum were culled from all quality sequences for the further analyses of Verrucomicrobial diversity and community composition.

Results and discussion

The relative abundance of Verrucomicrobia accounted for ~20% of the total bacterial communities, and Spartobacteria and DA101 were the most dominant class and genus, respectively. Verrucomicrobia community composition differed significantly among elevations, while the Verrucomicrobia diversity showed no apparent trend along elevation although the richness of some classes or genera significantly changed with elevation. The Verrucomicrobial community composition, diversity, and relative abundance of specific classes or genera were significantly correlated with soil pH and carbon/nitrogen ratio (C:N ratio).

Conclusions

These results indicated that Verrucomicrobia were abundant in Changbai Mountain soils, and Verrucomicrobial elevational distribution was strongly influenced by soil pH and C:N ratio. Our results also provide potential evidence that the dominant genus DA101 occupies different ecological niches and performs oligotrophic life history strategy in soil environment.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Barns SM, Cain EC, Sommerville L, Kuske CR (2007) Acidobacteria phylum sequences in uranium-contaminated subsurface sediments greatly expand the known diversity within the phylum. Appl Environ Microbiol 73:3113–3116

    Article  CAS  Google Scholar 

  • Bergen B, Herlemann DPR, Labrenz M, Jürgens K (2014) Distribution of the verrucomicrobial clade Spartobacteria along a salinity gradient in the Baltic Sea. Environ Microbiol Rep 6:625–630

    Article  CAS  Google Scholar 

  • Bergmann GT, Bates ST, Eilers KG, Lauber CL, Caporaso JG, Walters WA, Knight R, Fierer N (2011) The under-recognized dominance of verrucomicrobia in soil bacterial communities. Soil Biol Biochem 43:1450–1455

    Article  CAS  Google Scholar 

  • Brewer T, Handley K, Carini P, Gibert J, Fierer N (2016) Genome reduction in an abundant and ubiquitous soil bacterial lineage. bio Rxiv 2016:053942

    Google Scholar 

  • Bryant JA, Lamanna C, Morlon H, Kerkhoff AJ, Enquist BJ, Green JL (2008) Colloquium paper: microbes on mountainsides: contrasting elevational patterns of bacterial and plant diversity. Proc Natl Acad Sci U S A 1:11505–11511

    Article  Google Scholar 

  • Buckley DH, Schmidt TM (2001) Environmental factors influencing the distribution of rRNA from verrucomicrobia in soil. FEMS Microbiol Ecol 35:105–112

    Article  CAS  Google Scholar 

  • Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena 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, Tumbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows integration and 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, Huntley J, Fierer N, Owens SM, Betley J, Fraser L, Bauer M, Gormley N, Gilbert JA, Smith G, Knight R (2012) Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J 6:1621–1624

    Article  CAS  Google Scholar 

  • Dunfield PF, Yuryev A, Senin P, Smirnova AV, Stott MB, Hou S, Ly B, Saw JH, Zhou Z, Ren Y, Wang J, Mountain BW, Crowe MA, Weatherby TM, Bodelier PL, Liesack W, Feng L, Wang L, Alam M (2007) Methane oxidation by an extremely acidophilic bacterium of the phylum verrucomicrobia. Nature 450:879–882

    Article  CAS  Google Scholar 

  • Felske A, Akkermans ADL (1998) Prominent occurrence of ribosomes from an uncultured bacterium of the Verrucomicrobiales cluster in grassland soils. Lett Appl Microbiol 26:219–223

    Article  CAS  Google Scholar 

  • Fierer N, Ladau J, Clemente JC, Leff JW, Owens SM, Pollard KS, Knight R, Gilbert JA, McCulley RL (2013) Reconstructing the microbial diversity and function of pre-agricultural tallgrass prairie soils in the United States. Science 342:621–624

    Article  CAS  Google Scholar 

  • Fierer N, McCain CM, Meir P, Zimmermann M, Rapp JM, Silman MR, Knight R (2011) Microbes do not follow the elevational diversity patterns of plants and animals. Ecology 92:797–804

    Article  Google Scholar 

  • Freitas S, Hatosy S, Fuhrman JA, Huse SM, Welch DB, Sogin ML, Martiny AC (2012) Global distribution and diversity of marine verrucomicrobia. ISME J 6:1499–1505

    Article  CAS  Google Scholar 

  • Hanson CA, Fuhrman JA, Horner-Devine MC, Martiny JB (2012) Beyond biogeographic patterns: processes shaping the microbial landscape. Nat Rev Microbiol 10:497–506

    CAS  Google Scholar 

  • Hedlund BP, Gosink JJ, Staley JT (1997) Verrucomicrobia div. nov., a new division of the bacteria containing three new species of Prosthecobacter. Antonie Van Leeuwenhoek 72:29–38

    Article  CAS  Google Scholar 

  • Hedlund BP (2011) Phylum XXIII. Verrucomicrobia phyl. nov. In: Krieg NR, Ludwig W, Whitman WR, Hedlund BP, Paster BJ, Staley JT et al (eds) Bergey’s manual of systematic bacteriology. Williams & Wilkins, NewYork, pp 795–841

    Google Scholar 

  • Hugenholtz P, Goebel BM, Pace NR (1998) Impact of culture-independent studies on the emerging phylogenetic view of bacterial diversity. J Bacteriol 180:4765–4774

    CAS  Google Scholar 

  • Islam T, Jensen S, Reigstad LJ, Larsen O, Birkeland NK (2008) Methane oxidation at 55 °C and pH 2 by a thermoacidophilic bacterium belonging to the verrucomicrobia phylum. Proc Natl Acad Sci U S A 105:300–304

    Article  CAS  Google Scholar 

  • Janssen PH (2006) Identifying the dominant soil bacterial taxa in libraries of 16S rRNA and 16S rRNA genes. Appl Environ Microbiol 72:1719–1728

    Article  CAS  Google Scholar 

  • Janssen PH, Yates PS, Grinton BE, Taylor PM, Sait M (2002) Improved culturability of soil bacteria and isolation in pure culture of novel members of the divisions Acidobacteria, Actinobacteria, Proteobacteria, and Verrucomicrobia. Appl Environ Microbiol 68:2391–2396

    Article  CAS  Google Scholar 

  • Khadem AF, Pol A, Jetten MS, Op den Camp HJ (2010) Nitrogen fixation by the verrucomicrobial methanotroph “Methylacidiphilum fumariolicum” SolV. Microbiology 156:1052–1059

    Article  CAS  Google Scholar 

  • Liu J, Sui Y, Yu Z, Yao Q, Shi Y, Chu H, Jin J, Liu X, Wang G (2016) Diversity and distribution patterns of acidobacterial communities in the black soil zone of northeast China. Soil Biol Biochem 95:212–222

    Article  CAS  Google Scholar 

  • Martinez-Garcia M, Brazel DM, Swan BK, Arnosti C, Chain PS, Reitenga KG, Xie G, Poulton NJ, Lluesma Gomez M, Masland DE, Thompson B, Bellows WK, Ziervogel K, Lo CC, Ahmed S, Gleasner CD, Detter CJ, Stepanauskas R (2012) Capturing single cell genomes of active polysaccharide degraders: an unexpected contribution of verrucomicrobia. PLoS One 7:e35314

    Article  CAS  Google Scholar 

  • Martiny JB, Bohannan BJ, Brown JH, Colwell RK, Fuhrman JA, Green JL, Horner-Devine MC, Kane M, Krumins JA, Kuske CR, Morin PJ, Naeem S, Ovreas L, Reysenbach AL, Smith VH, Staley JT (2006) Microbial biogeography: putting microorganisms on the map. Nat Rev Microbiol 4:102–112

    Article  CAS  Google Scholar 

  • Naether A, Foesel BU, Naegele V, Wust PK, Weinert J, Bonkowski M, Alt F, Oelmann Y, Polle A, Lohaus G, Gockel S, Hemp A, Kalko EK, Linsenmair KE, Pfeiffer S, Renner S, Schoning I, Weisser WW, Wells K, Fischer M, Overmann J, Friedrich MW (2012) Environmental factors affect acidobacterial communities below the subgroup level in grassland and forest soils. Appl Environ Microbiol 78:7398–7406

    Article  CAS  Google Scholar 

  • Parveen B, Mary I, Vellet A, Ravet V, Debroas D (2013) Temporal dynamics and phylogenetic diversity of free-living and particle-associated verrucomicrobia communities in relation to environmental variables in a mesotrophic lake. FEMS Microbiol Ecol 83:189–201

    Article  CAS  Google Scholar 

  • Pol A, Heijmans K, Harhangi HR, Tedesco D, Jetten MS, Op den Camp HJ (2007) Methanotrophy below pH 1 by a new verrucomicrobia species. Nature 450:874–878

    Article  CAS  Google Scholar 

  • R Development Core Team (2010) R: a language and environment for statistical computing. R Foundation for statistical computing, Vienna

    Google Scholar 

  • Ranjan K, Paula FS, Mueller RC, Jesus Eda C, Cenciani K, Bohannan BJ, Nusslein K, Rodrigues JL (2015) Forest-to-pasture conversion increases the diversity of the phylum verrucomicrobia in Amazon rainforest soils. Front Microbiol 6:779

    Article  Google Scholar 

  • Sangwan P, Kovac S, Davis KE, Sait M, Janssen PH (2005) Detection and cultivation of soil verrucomicrobia. Appl Environ Microbiol 71:8402–8410

    Article  CAS  Google Scholar 

  • Schlesner H, Jenkins C, Staley JT (2006) The phylum verrucomicrobia: a phylogenetically heterogeneous bacterial group. Prokaryotes 7:881–896

    Google Scholar 

  • Senechkin IV, Speksnijder AG, Semenov AM, van Bruggen AH, van Overbeek LS (2010) Isolation and partial characterization of bacterial strains on low organic carbon medium from soils fertilized with different organic amendments. Microb Ecol 60:829–839

    Article  Google Scholar 

  • Sharp CE, Smirnova AV, Graham JM, Stott MB, Khadka R, Moore TR, Grasby SE, Strack M, Dunfield PF (2014) Distribution and diversity of verrucomicrobia methanotrophs in geothermal and acidic environments. Environ Microbiol 16:1867–1878

    Article  CAS  Google Scholar 

  • Shen C, Liang W, Shi Y, Lin X, Zhang H, Wu X, Xie G, Chain PSG, Grogan P, Chu H (2014) Contrasting elevational diversity patterns between eukaryotic soil microbes and plants. Ecology 95:3190–3202

    Article  Google Scholar 

  • Shen C, Xiong J, Zhang H, Feng Y, Lin X, Li X, Liang W, Chu H (2013) Soil pH drives the spatial distribution of bacterial communities along elevation on Changbai Mountain. Soil Biol Biochem 57:204–211

    Article  CAS  Google Scholar 

  • Singh D, Lee-Cruz L, Kim W-S, Kerfahi D, Chun J-H, Adams JM (2014) Strong elevational trends in soil bacterial community composition on Mt. Halla, South Korea. Soil Biol Biochem 68:140–149

    Article  CAS  Google Scholar 

  • Wu T, Ayres E, Bardgett RD, Wall DH, Garey JR (2011) Molecular study of worldwide distribution and diversity of soil animals. Proc Natl Acad Sci U S A 108:17720–17725

    Article  CAS  Google Scholar 

  • Yuan Y, Si G, Wang J, Luo T, Zhang G (2014) Bacterial community in alpine grasslands along an altitudinal gradient on the Tibetan Plateau. FEMS Microbiol Ecol 87:121–132

    Article  CAS  Google Scholar 

  • Zhang Y, Cong J, Lu H, Li G, Qu Y, Su X, Zhou J, Li D (2014) Community structure and elevational diversity patterns of soil Acidobacteria. J Environ Sci (China) 26:1717–1724

    Article  Google Scholar 

Download references

Acknowledgements

We thank Wenju Liang and Xinyu Li for their assistance with soil sampling and Yu Shi and Yingying Ni for their assistance in lab analysis. We also thank Earth Microbiome Project (EMP) for the sample processing, sequencing, and core amplicon data analysis. This work was supported by the National Natural Science Foundation of China (41371254), the National Program on Key Basic Research Project (2014CB954002), and the Strategic Priority Research Program (XDB15010101, XDB15010302) of Chinese Academy of Sciences.

Conflict of interest

The authors declare that they no conflict of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Haiyan Chu.

Additional information

Responsible editor: Jianming Xu

Electronic supplementary material

ESM 1

(DOCX 450 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Shen, C., Ge, Y., Yang, T. et al. Verrucomicrobial elevational distribution was strongly influenced by soil pH and carbon/nitrogen ratio. J Soils Sediments 17, 2449–2456 (2017). https://doi.org/10.1007/s11368-017-1680-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11368-017-1680-x

Keywords

Navigation