Skip to main content
Log in

Illumina Sequencing of 16S rRNA Tag Revealed Spatial Variations of Bacterial Communities in a Mangrove Wetland

  • Environmental Microbiology
  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

The microbial community plays an essential role in the high productivity in mangrove wetlands. A proper understanding of the spatial variations of microbial communities will provide clues about the underline mechanisms that structure microbial groups and the isolation of bacterial strains of interest. In the present study, the diversity and composition of the bacterial community in sediments collected from four locations, namely mudflat, edge, bulk, and rhizosphere, within the Mai Po Ramsar Wetland in Hong Kong, SAR, China were compared using the barcoded Illumina paired-end sequencing technique. Rarefaction results showed that the bulk sediment inside the mature mangrove forest had the highest bacterial α-diversity, while the mudflat sediment without vegetation had the lowest. The comparison of β-diversity using principal component analysis and principal coordinate analysis with UniFrac metrics both showed that the spatial effects on bacterial communities were significant. All sediment samples could be clustered into two major groups, inner (bulk and rhizosphere sediments collected inside the mangrove forest) and outer mangrove sediments (the sediments collected at the mudflat and the edge of the mangrove forest). With the linear discriminate analysis scores larger than 3, four phyla, namely Actinobacteria, Acidobacteria, Nitrospirae, and Verrucomicrobia, were enriched in the nutrient-rich inner mangrove sediments, while abundances of Proteobacteria and Deferribacterias were higher in outer mangrove sediments. The rhizosphere effect of mangrove plants was also significant, which had a lower α-diversity, a higher amount of Nitrospirae, and a lower abundance of Proteobacteria than the bulk sediment nearby.

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.

Institutional subscriptions

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

Similar content being viewed by others

References

  1. Aburto-Oropeza O, Ezcurra E, Danemann G, Valdez V, Murray J, Sala E (2008) Mangroves in the Gulf of California increase fishery yields. P Natl Acad Sci USA 105:10456–10459

    Article  CAS  Google Scholar 

  2. Zhou HW, Wong AHY, Yu RMK, Park YD, Wong YS, Tam NFY (2009) Polycyclic aromatic hydrocarbon-induced structural shift of bacterial communities in mangrove sediment. Microb Ecol 58:153–160

    Article  PubMed  CAS  Google Scholar 

  3. Sahoo K, Dhal NK (2009) Potential microbial diversity in mangrove ecosystems: a review. Indian J Mar Sci 38(2):249–256

    CAS  Google Scholar 

  4. Lopez-Fuentes E, Ruiz-Valdiviezo VM, Martinez-Romero E, Gutierrez-Miceli FA, Dendooven L, Rincon-Rosales R (2012) Bacterial community in the roots and rhizosphere of Hypericum silenoides Juss. 1804. Afr J Microbiol Res 6:2704–2711

    Article  CAS  Google Scholar 

  5. Doornbos RF, van Loon LC, Bakker PAHM (2012) Impact of root exudates and plant defense signaling on bacterial communities in the rhizosphere. A review. Agron Sustain Dev 32:227–243

    Article  Google Scholar 

  6. Guo CL, Zhou HW, Wong YS, Tam NFY (2005) Isolation of PAH-degrading bacteria from mangrove sediments and their biodegradation potential. Mar Pollut Bull 51:1054–1061

    Article  PubMed  CAS  Google Scholar 

  7. Zhou HW, Guo CL, Wong YS, Tam NFY (2006) Genetic diversity of dioxygenase genes in polycyclic aromatic hydrocarbon-degrading bacteria isolated from mangrove sediments. FEMS Microbiol Lett 262:148–157

    Article  PubMed  CAS  Google Scholar 

  8. Staley JT, Konopka A (1985) Measurement of in situ activities of nonphotosynthetic microorganisms in aquatic and terrestrial habitats. Annu Rev Microbiol 39:321–346

    Article  PubMed  CAS  Google Scholar 

  9. Holguin G, Guzman MA, Bashan Y (1992) Two new nitrogen-fixing bacteria from the rhizosphere of mangrove trees: their isolation, identification and in vitro interaction with rhizosphere Staphylococcus sp. FEMS Microbiol Ecol 101:207–216

    CAS  Google Scholar 

  10. Bashan Y, Holguin G, Lifshitz R (1993) Isolation and characterization of plant growth-promoting rhizobacteria. In: Glick BR, Thompson JE (eds) Isolation and characterization of plant growth-promoting rhizobacteria. CRC Press, Boca Raton, FL, pp 331–245

    Google Scholar 

  11. Muyzer G, Smalla K (1998) Application of denaturing gradient gel electrophoresis (DGGE) and temperature gradient gel electrophoresis (TGGE) in microbial ecology. Anton Leeuw Int J G 73:127–141

    Article  CAS  Google Scholar 

  12. Urakawa H, Yoshida T, Nishimura M, Ohwada K (2000) Characterization of depth-related population variation in microbial communities of a coastal marine sediment using 16S rDNA-based approaches and quinone profiling. Environ Microbiol 2:542–554

    Article  PubMed  CAS  Google Scholar 

  13. Liang JB, Chen YQ, Lan CY, Tam NFY, Zan QJ, Huang LN (2007) Recovery of novel bacterial diversity from mangrove sediment. Mar Biol 150:739–747

    Article  Google Scholar 

  14. Heuer H, Krsek M, Baker P, Smalla K, Wellington EMH (1997) Analysis of actinomycete communities by specific amplification of genes encoding 16S rRNA and gel-electrophoretic separation in denaturing gradients. Appl Environ Microbiol 63:3233–3241

    PubMed  CAS  Google Scholar 

  15. dos Santos HF, Cury JC, do Carmo FL, dos Santos AL, Tiedje J, van Elsas JD, Rosado AS, Peixoto RS (2011) Mangrove bacterial diversity and the impact of oil contamination revealed by pyrosequencing: bacterial proxies for oil pollution. PLoS One 6:e16943

    Article  PubMed  Google Scholar 

  16. Andreote FD, Jimenez DJ, Chaves D, Dias ACF, Luvizotto DM, Dini-Andreote F, Fasanella CC, Lopez MV, Baena S, Taketani RG et al (2012) The microbiome of Brazilian mangrove sediments as revealed by metagenomics. PLoS One 7:e38600

    Article  PubMed  CAS  Google Scholar 

  17. Cleary DFR, Smalla K, Mendonca-Hagler LCS, Gomes NCM (2012) Assessment of variation in bacterial composition among microhabitats in a mangrove environment using DGGE fingerprints and barcoded pyrosequencing. PLoS One 7:e29380

    Article  PubMed  CAS  Google Scholar 

  18. Wang Y, Sheng HF, He Y, Wu JY, Jiang YX, Tam NFY, Zhou HW (2012) Comparison of the levels of bacterial diversity in freshwater, intertidal wetland, and marine sediments by using millions of Illumina tags. Appl Environ Microbiol 78:8264–8271

    Article  PubMed  CAS  Google Scholar 

  19. Qin P, Wong YS, Tam NFY (2000) Emergy evaluation of Mai Po mangrove marshes. Ecol Eng 16:271–280

    Article  Google Scholar 

  20. Tam NFY, Wong YS (2002) Conservation and sustainable exploitation of mangroves in Hong Kong. Trees-Struct Funct 16:224–229

    Article  Google Scholar 

  21. Zhou HW, Li DF, Tam NFY, Jiang XT, Zhang H, Sheng HF, Qin J, Liu X, Zou F (2011) BIPES, a cost-effective high-throughput method for assessing microbial diversity. ISME J 5:741–749

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  23. Uroz S, Buee M, Murat C, Frey-Klett P, Martin F (2010) Pyrosequencing reveals a contrasted bacterial diversity between oak rhizosphere and surrounding soil. Env Microbiol Rep 2:281–288

    Article  CAS  Google Scholar 

  24. Gomes NCM, Cleary DFR, Pinto FN, Egas C, Almeida A, Cunha A, Mendonca-Hagler LCS, Smalla K (2010) Taking root: enduring effect of rhizosphere bacterial colonization in mangroves. PLoS One 5:e14065

    Article  PubMed  Google Scholar 

  25. Huse SM, Dethlefsen L, Huber JA, Welch DM, Relman DA, Sogin ML (2008) Exploring microbial diversity and taxonomy using SSU rRNA hypervariable tag sequencing. PLoS Genet 4:e1000255

    Article  PubMed  Google Scholar 

  26. Gomes NCM, Borges LR, Paranhos R, Pinto FN, Mendonca-Hagler LCS, Smalla K (2008) Exploring the diversity of bacterial communities in sediments of urban mangrove forests. FEMS Microbiol Ecol 66:96–109

    Article  CAS  Google Scholar 

  27. Lozupone C, Lladser ME, Knights D, Stombaugh J, Knight R (2011) UniFrac: an effective distance metric for microbial community comparison. ISME J 5:169–172

    Article  PubMed  Google Scholar 

  28. Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS, Huttenhower C (2011) Metagenomic biomarker discovery and explanation. Genome Biol 12:R60

    Article  PubMed  Google Scholar 

  29. Sogin ML, Morrison HG, Huber JA, Mark Welch D, Huse SM, Neal PR, Arrieta JM, Herndl GJ (2006) Microbial diversity in the deep sea and the underexplored “rare biosphere”. P Natl Acad Sci USA 103:12115–12120

    Article  CAS  Google Scholar 

  30. Hayatsu M, Tago K, Saito M (2008) Various players in the nitrogen cycle: diversity and functions of the microorganisms involved in nitrification and denitrification. Soil Sci Plant Nutr 54:33–45

    Article  CAS  Google Scholar 

  31. Castro HF, Williams NH, Ogram A (2000) Phylogeny of sulfate-reducing bacteria. FEMS Microbiol Ecol 31:1–9

    PubMed  CAS  Google Scholar 

  32. Miroshnichenko ML, Kostrikina NA, L'Haridon S, Jeanthon C, Hippe H, Stackebrandt E, Bonch-Osmolovskaya EA (2002) Nautilia lithotrophica gen. nov., sp nov., a thermophilic sulfur-reducing epsilon-proteobacterium isolated from a deep-sea hydrothermal vent. Int J Syst Evol Microbiol 52:1299–1304

    Article  PubMed  CAS  Google Scholar 

  33. Sachdev D, Nema P, Dhakephalkar P, Zinjarde S, Chopade B (2010) Assessment of 16S rRNA gene-based phylogenetic diversity and promising plant growth-promoting traits of Acinetobacter community from the rhizosphere of wheat. Microbiol Res 165:627–638

    Article  PubMed  CAS  Google Scholar 

  34. Jiang XT, Zhang H, Sheng HF, Wang Y, He Y, Zou F, Zhou HW (2012) Two-stage clustering (TSC): a pipeline for selecting operational taxonomic units for the high-throughput sequencing of PCR amplicons. PLoS One 7:e30230

    Article  PubMed  CAS  Google Scholar 

  35. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ et al (2009) Introducing Mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by the National Natural Science Foundation of China (NSFC 31270152), the Guangdong Natural Science Foundation (no. S2011010004136), the Program for New Century Excellent Talents in University (NCET-11-0921), and Educational Commission of Guangdong Province, China (2012KJCX0031). The authors would also like to acknowledge the financial support from the State Key Laboratory in Marine Pollution, City University of Hong Kong.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Hong-Wei Zhou or Nora Fung-Yee Tam.

Electronic Supplementary Material

Below is the link to the electronic supplementary material.

ESM 1

PDF 116 kb

Rights and permissions

Reprints and permissions

About this article

Cite this article

Jiang, XT., Peng, X., Deng, GH. et al. Illumina Sequencing of 16S rRNA Tag Revealed Spatial Variations of Bacterial Communities in a Mangrove Wetland. Microb Ecol 66, 96–104 (2013). https://doi.org/10.1007/s00248-013-0238-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-013-0238-8

Keywords

Navigation