Skip to main content

Novel 16S rDNA primers revealed the diversity and habitats-related community structure of sphingomonads in 10 different niches

Antonie van Leeuwenhoek volume 110, pages 877–889 (2017)Cite this article

Abstract

It is believed that sphingomonads are ubiquitously distributed in environments. However detailed information about their community structure and their co-relationship with environmental parameters remain unclear. In this study, novel sphingomonads-specific primers based on the 16S rRNA gene were designed to investigate the distribution of sphingomonads in 10 different niches. Both in silico and in-practice tests on pure cultures and environmental samples showed that Sph384f/Sph701r was an efficient primer set. Illumina MiSeq sequencing revealed that community structures of sphingomonads were significantly different among the 10 samples, although 12 sphingomonad genera were present in all samples. Based on RDA analysis and Monte Carlo permutation test, sphingomonad community structure was significantly correlated with limnetic and marine habitat types. Among these niches, the genus Sphingomicrobium showed strong positive correlation with marine habitats, whereas genera Sphingobium, Novosphingobium, Sphingopyxis, and Sphingorhabdus showed strong positive correlation with limnetic habitats. Our study provided direct evidence that sphingomonads are ubiquitously distributed in environments, and revealed for the first time that their community structure can be correlated with habitats.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  • Boersma FGH, Warmink JA, Andreote FA, van Elsas JD (2009) Selection of Sphingomonadaceae at the base of Laccaria Proxima and Russula Exalbicans fruiting bodies. Appl Environ Microbiol 75:1979–1989

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chung EJ, Jo EJ, Yoon HS, Song GC, Jeon CO, Chung YR (2011) Sphingomonas oryziterrae sp. nov. and Sphingomonas jinjuensis sp. nov. isolated from rhizosphere soil of rice (Oryza sativa L.). Int J Syst Evol Microbiol 61:2389–2394

    Article  PubMed  Google Scholar 

  • Delmotte N, Knief C, Chaffron S, Innerebner G, Roschitzki B, Schlapbach R, von Mering C, Vorholt JA (2009) Community proteogenomics reveals insights into the physiology of phyllosphere bacteria. PNAS 106:16428–16433

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  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  PubMed  PubMed Central  Google Scholar 

  • Enya J, Shinohara H, Yoshida S, Tsukiboshi T, Negishi H, Suyama K, Tsushima S (2007) Culturable leaf-associated bacteria on tomato plants and their potential as biological control agents. Microbiol Ecol 53:524–536

    Article  CAS  Google Scholar 

  • Glaeser SP, Kampfer P (2014) The family Sphingomonadaceae. In: Rosenberg E et al (eds) The prokaryotes—Alphaproteobacteria and Betaproteobacteria. Springer, Berlin, pp 641–707

    Google Scholar 

  • Haas BJ, Gevers D, Earl AM, Feldgarden M, Ward DV, Giannoukos G, Ciulla D, Tabbaa D, Highlander SK, Sodergren E (2011) Chimeric 16S rRNA sequence formation and detection in Sanger and 454-pyrosequenced PCR amplicons. Genome Res 21:494–504

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jogler M, Siemens H, Chen H, Bunk B, Sikorski J, Overmann J (2011) Identification and targeted cultivation of abundant novel freshwater sphingomonads and analysis of their population substructure. Appl Environ Microbiol 77:7355–7364

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kosako Y, Yabuuchi E, Naka T, Fujiwara N, Kobayashi K et al (2000) Proposal of Sphingomonadaceae fam. nov., consisting of Sphingomonas Yabuuchi et al. 1990, Erythrobacter Shiba and Shimidu 1982, Erythromicrobium Yurkov et al. 1994, Porphyrobacter Fuerst et al. 1993, Zymomonas Kluyver and van Niel 1936, and Sandaracinobacter Yurkov et al. 1997, with the type genus Sphingomonas Yabuuchi et al. 1990. Microbiol Immunol 44:563–575

    Article  CAS  PubMed  Google Scholar 

  • Leung KT, Chang YJ, Gan YD, Peacock A, Macnaughton SJ, Stephen JR, Burkhalter RS, Flemming CA, White DC (1999) Detection of Sphingomonas spp. in soil by PCR and sphingolipid biomarker analysis. J Ind Microbiol Biotechnol 23:252–260

    Article  CAS  PubMed  Google Scholar 

  • Leys NMEJ, Ryngaert A, Bastiaens L, Verstraete W, Top EM, Springael D (2004) Occurrence and phylogenetic diversity of Sphingomonas strains in soils contaminated with polycyclic aromatic hydrocarbons. Appl Environ Microbiol 70:1944–1955

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Magoc T, Salzberg SL (2011) FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27:2957–2963

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Murakami Y, Otsuka S, Senoo K (2010) Abundance and community structure of sphingomonads in leaf residues and nearby bulk soil. Microbes Environ 25:183–189

    Article  PubMed  Google Scholar 

  • Newton RJ, Jones SE, Eiler A, McMahon KD, Bertilsson S (2011) A guide to the natural history of freshwater lake bacteria. Microbiol Mol Biol Rev 75:14–49

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rychlik W (2007) OLIGO 7 primer analysis software. Methods Mol Biol 402:35–59

    Article  CAS  PubMed  Google Scholar 

  • Stolz A (2009) Molecular characteristics of xenobiotic-degrading sphingomonads. Appl Microbiol Biotechnol 81:793–811

    Article  CAS  PubMed  Google Scholar 

  • Stolz A (2014) Degradative plasmids from sphingomonads. FEMS Microbiol Lett 350:9–19

    Article  CAS  PubMed  Google Scholar 

  • Sun DL, Jiang X, Wu QLL, Zhou NY (2013) Intragenomic heterogeneity of 16S rRNA genes causes overestimation of prokaryotic diversity. Appl Environ Microbiol 79:5962–5969

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ter Braak CJ, Smilauer P (2002) CANOCO reference manual and CanoDraw for Windows user’s guide: software for canonical community ordination (version4.5). www.canoco.com

  • Tippmann HF (2004) Analysis for free: comparing programs for sequence analysis. Brief Bioinform 5:82–87

    Article  CAS  PubMed  Google Scholar 

  • Vaz-Moreira I, Nunes OC, Manaia CM (2011) Diversity and antibiotic resistance patterns of Sphingomonadaceae isolates from drinking water. Appl Environ Micro 77:5697–5706

    Article  CAS  Google Scholar 

  • Videira SS, de Araujo JLS, Rodrigues LD, Baldani VLD, Baldani JI (2009) Occurrence and diversity of nitrogen-fixing Sphingomonas bacteria associated with rice plants grown in Brazil. FEMS Microbiol Lett 293:11–19

    Article  CAS  PubMed  Google Scholar 

  • Zhou LS, Li H, Zhang Y, Wang YF, Han SQ, Xu H (2012) Abundance and diversity of Sphingomonas in Shenfu petroleum-wastewater irrigation zone, China. Environ Sci Pollut 19:282–294

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported financially by the National Natural Science Foundation of China (21577121), the 973 Program (2014CB441103) and ZJNSF LY14B070010.

Author information

Authors and Affiliations

  1. Zhejiang Provincial Key Laboratory of Organic Pollution Process and Control, Department of Environmental Science, College of Environmental and Resource Sciences, Zhejiang University, Hangzhou, China

    Yili Huang, Hao Feng, Hang Lu & Yanhua Zeng

Authors
  1. Yili Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hao Feng
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Hang Lu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yanhua Zeng
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yili Huang.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 2270 kb)

Supplementary material 2 (XLSX 21 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Huang, Y., Feng, H., Lu, H. et al. Novel 16S rDNA primers revealed the diversity and habitats-related community structure of sphingomonads in 10 different niches. Antonie van Leeuwenhoek 110, 877–889 (2017). https://doi.org/10.1007/s10482-017-0860-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10482-017-0860-4

Keywords

  • Primer design
  • Sphingomonads
  • Illumina sequencing
  • Bacterial diversity
  • Species-habitats correlation