Skip to main content

Advertisement

Log in

Pyrosequencing-Based Seasonal Observation of Prokaryotic Diversity in Pneumatophore-Associated Soil of Avicennia marina

  • Published:
Current Microbiology Aims and scope Submit manuscript

Abstract

Pneumatophores are aerial roots developing from the main roots of mangrove plants away from the gravity. The below ground pneumatophore-associated soil prokaryotic community of Avicennia marina was studied by amplicon pyrosequencing (39,378 reads) during monsoon and summer seasons. Apart from the most dominant phylum Proteobacteria in both seasons, the second most were Acidobacteria (summer) and Cyanobacteria/Chloroplast (monsoon). Similarly, Acidobacteria_Gp10 and Cyanobacteria were the second most abundant at class level during summer and monsoon, respectively. Archaeal phylum Thaumarchaeota was the most abundant followed by Crenarchaeota and Euryarchaeota. The classes detected in our study were Thermoprotei, Halobacteria, and Methanomicrobia. The highest richness and diversity were observed during summer for bacteria, whereas the same phenomena for archaea in monsoon at 97 % sequence similarity. To the best of our knowledge, this is the first attempt to catalog the prokaryotic diversity of pnueumatophore-associated soil.

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

Similar content being viewed by others

References

  1. Alfaro-Espinoza G, Ullrich MS (2014) Marinobacterium mangrovicola sp. nov., a marine nitrogen-fixing bacterium isolated from mangrove roots of Rhizophora mangle. Int J Syst Evol Microbiol 64:3988–3993

    Article  PubMed  CAS  Google Scholar 

  2. Alongi DM, Christoffersen P, Tirendi F (1993) The influence of forest type on microbial-nutrient relationships in tropical mangrove sediments. J Exp Mar Biol Ecol 171:201–223

    Article  Google Scholar 

  3. Alongi DM, Trott LA, Wattayakorn G, Clough BF (2002) Below-ground nitrogen cycling in relation to net canopy production in mangrove forests of southern Thailand. Mar Biol 140:855–864

    Article  CAS  Google Scholar 

  4. Andreote FD, Jiménez DJ, Chaves D et al (2012) The microbiome of Brazilian mangrove sediments as revealed by metagenomics. PLoS One 7:e38600

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  5. Barnard RL, Osborne CA, Firestone MK (2013) Responses of soil bacterial and fungal communities to extreme desiccation and rewetting. ISME J 7:2229–2241

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  6. Bolhuis H, Stal LJ (2011) Analysis of bacterial and archaeal diversity in coastal microbial mats using massive parallel 16S rRNA gene tag sequencing. ISME J 5:1701–1712

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  7. Boone DR, Mathrani IM, Liu Y et al (1993) Isolation and characterization of Methanohalophilus portucalensis sp. nov. and DNA reassociation study of the genus Methanohalophilus. Int J Syst Bacteriol 43:430–437

    Article  Google Scholar 

  8. Cao H, Li M, Hong Y, Gu J-D (2011) Diversity and abundance of ammonia-oxidizing archaea and bacteria in polluted mangrove sediment. Syst Appl Microbiol 34:513–523

    Article  PubMed  CAS  Google Scholar 

  9. Cleary DFR, Smalla K, Mendonça-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  PubMed Central  CAS  Google Scholar 

  10. Cole JR, Wang Q, Cardenas E et al (2009) The ribosomal database project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res 37:D141–D145

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  11. Cui H-L, Gao X, Yang X, Xu X-W (2011) Halolamina pelagica gen. nov., sp. nov., a new member of the family Halobacteriaceae. Int J Syst Evol Microbiol 61:1617–1621

    Article  PubMed  CAS  Google Scholar 

  12. Delong EF (1992) Archaea in coastal marine environments. Proc Natl Acad Sci USA 89:5689

    Article  Google Scholar 

  13. Dos Santos HF, Cury JC, do Carmo FL et al (2011) Mangrove bacterial diversity and the impact of oil contamination revealed by pyrosequencing: bacterial proxies for oil pollution. PLoS One 6:e16943

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  14. Dromgoole FI (1988) Carbon dioxide fixation in aerial roots of the New Zealand mangrove Avicennia marina var. resinifera. N Z J Mar Freshw Res 22:617–619

    Article  Google Scholar 

  15. Elshahed MS, Najar FZ, Roe BA et al (2004) Survey of archaeal diversity reveals an abundance of halophilic archaea in a low-salt, sulfide- and sulfur-rich spring. Appl Environ Microbiol 70:2230–2239

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  16. Gomes NCM, Cleary DFR, Pinto FN et al (2010) Taking root: enduring effect of rhizosphere bacterial colonization in mangroves. PLoS One 5:e14065. doi:10.1371/journal.pone.0014065

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  17. Harbison P (1986) Mangrove muds: a sink and a source for trace metals. Mar Pollut Bull 17:246–250

    Article  CAS  Google Scholar 

  18. Herndl GJ, Reinthaler T, Teira E et al (2005) Contribution of Archaea to total prokaryotic production in the deep Atlantic Ocean. Appl Environ Microbiol 71:2303–2309

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  19. Hiiesalu I, Pärtel M, Davison J et al (2014) Species richness of arbuscular mycorrhizal fungi: associations with grassland plant richness and biomass. New Phytol 203:233–244

    Article  PubMed  CAS  Google Scholar 

  20. Jackson ML (1967) Soil chemical analysis. Prentice Hall of India Pvt Ltd, New Delhi

    Google Scholar 

  21. Jiang X-T, Peng X, Deng G-H et al (2013) Illumina sequencing of 16S rRNA tag revealed spatial variations of bacterial communities in a mangrove wetland. Microb Ecol 66:96–104

    Article  PubMed  Google Scholar 

  22. Jones RT, Robeson MS, Lauber CL et al (2009) A comprehensive survey of soil acidobacterial diversity using pyrosequencing and clone library analyses. ISME J 3:442–453

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  23. Vijaya Kumar KM, Kumara V (2013) Physico-chemical analysis of water quality of Kundapura mangrove forest, Karnataka, India. Glob J Biol Agric Heal Sci 2:111–118

    Google Scholar 

  24. Kale V, Björnsdóttir SH, Fridjónsson ÓH et al (2013) Litorilinea aerophila gen. nov., sp. nov., an aerobic member of the class Caldilineae, phylum Chloroflexi, isolated from an intertidal hot spring. Int J Syst Evol Microbiol 63:1149–1154

    Article  PubMed  CAS  Google Scholar 

  25. Kathiresan K, Bingham BL (2001) Biology of mangroves and mangrove ecosystems. Adv Mar Biol 40:81–251

    Article  Google Scholar 

  26. Kim KK, Lee KC, Lee J-S (2011) Halogranum salarium sp. nov., a halophilic archaeon isolated from sea salt. Syst Appl Microbiol 34:576–580

    Article  PubMed  CAS  Google Scholar 

  27. Kreuzwieser J, Buchholz J, Rennenberg H (2003) Emission of methane and nitrous oxide by australian mangrove ecosystems. Plant Biol 5:423–431

    Article  CAS  Google Scholar 

  28. Kristensen E, Flindt MR, Ulomi S et al (2008) Emission of CO2 and CH4 to the atmosphere by sediments and open waters in two Tanzanian mangrove forests. Mar Ecol Prog Ser 370:53–67

    Article  CAS  Google Scholar 

  29. Leininger S, Urich T, Schloter M et al (2006) Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature 442:806–809

    Article  PubMed  CAS  Google Scholar 

  30. Lino T, Mori K, Uchino Y et al (2010) Ignavibacterium album gen. nov., sp. nov., a moderately thermophilic anaerobic bacterium isolated from microbial mats at a terrestrial hot spring and proposal of Ignavibacteria classis nov., for a novel lineage at the periphery of green sulfur bacteria. Int J Syst Evol Microbiol 60:1376–1382

    Article  CAS  Google Scholar 

  31. Lugomela C, Bergman B (2002) Biological N2-fixation on mangrove pneumatophores: preliminary observations and perspectives. Ambio 31:612–613

    Article  PubMed  Google Scholar 

  32. Mochimaru H, Tamaki H, Hanada S et al (2009) Methanolobus profundi sp. nov., a methylotrophic methanogen isolated from deep subsurface sediments in a natural gas field. Int J Syst Evol Microbiol 59:714–718

    Article  PubMed  CAS  Google Scholar 

  33. Moor C, Lymberopoulou T, Dietrich VJ (2001) Determination of heavy metals in soils, sediments and geological materials by ICP-AES and ICP-MS. Microchim Acta 136:123–128

    Article  CAS  Google Scholar 

  34. Mukherjee A, De M, Das S et al (2012) Rate of salt excretion by salt excreting mangroves of sundarban under varying environmental conditions. Glob Adv Res J Environ Sci Toxicol 1:1–9

    CAS  Google Scholar 

  35. Naether A, Foesel BU, Naegele V et al (2012) Environmental factors affect acidobacterial communities below the subgroup level in grassland and forest soils. Appl Environ Microb 78:7398–7406

    Article  CAS  Google Scholar 

  36. Nielsen T, Andersen F (2003) Phosphorus dynamics during decomposition of mangrove (Rhizophora apiculata) leaves in sediments. J Exp Mar Biol Ecol 293:73–88

    Article  CAS  Google Scholar 

  37. Ovreås L, Forney L, Daae FL et al (1997) Distribution of bacterioplankton in meromictic Lake Saelenvannet, as determined by denaturing gradient gel electrophoresis of PCR-amplified gene fragments coding for 16S rRNA. Appl Environ Microbiol 63:3373

    Google Scholar 

  38. Pelegri SP, Rivera-Monroy VH, Twilley RR (1997) A comparison of nitrogen fixation (acetylene reduction) among three species of mangrove litter, sediments, and pneumatophores in south Florida, USA. Hydrobiologia 356:73–79

    Article  CAS  Google Scholar 

  39. Pester M, Rattei T, Flechl S et al (2012) amoA-based consensus phylogeny of ammonia-oxidizing archaea and deep sequencing of amoA genes from soils of four different geographic regions. Environ Microbiol 14:525–539

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  40. Pires ACC, Cleary DFR, Almeida A et al (2012) Denaturing gradient gel electrophoresis and barcoded pyrosequencing reveal unprecedented archaeal diversity in mangrove sediment and rhizosphere samples. Appl Environ Microbiol 78:5520–5528

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  41. Purvaja R, Ramesh R, Frenzel P (2004) Plant-mediated methane emission from an Indian mangrove. Glob Chang Biol 10:1825–1834

    Article  Google Scholar 

  42. Quaiser A, Ochsenreiter T, Lanz C et al (2003) Acidobacteria form a coherent but highly diverse group within the bacterial domain: evidence from environmental genomics. Mol Microbiol 50:563–575

    Article  PubMed  CAS  Google Scholar 

  43. Ren J, Yan B, Hong K (2012) Comparison of bacterial and archaeal community of mangrove soil under different vegetation in Dongzhaigang, Hainan Island. Acta Microbiol Sin 52:736–743

    CAS  Google Scholar 

  44. Rhoades JD, Manteghi NA, Shouse PJ et al (1989) Soil electrical conductivity and soil salinity: new formulations and calibrations. Soil Sci Soc Am J 53:433–439

    Article  Google Scholar 

  45. Santra SC, Pal UC, Maity H et al (1988) Blue-green algae in saline habitats of West Bengal: a systematic account. Biol Membr 14:81–108

    Google Scholar 

  46. Singh N, Kendall MM, Liu Y, Boone DR (2005) Isolation and characterization of methylotrophic methanogens from anoxic marine sediments in Skan Bay, Alaska: description of Methanococcoides alaskense sp. nov., and emended description of Methanosarcina baltica. Int J Syst Evol Microbiol 55:2531–2538

    Article  PubMed  CAS  Google Scholar 

  47. Soto-Ramírez N, Sánchez-Porro C, Rosas S et al (2007) Halomonas avicenniae sp. nov., isolated from the salty leaves of the black mangrove Avicennia germinans in Puerto Rico. Int J Syst Evol Microbiol 57:900–905

    Article  PubMed  CAS  Google Scholar 

  48. Sparling GP, Whale KN, Ramsay AJ (1985) Quantifying the contribution from the soil microbial biomass to the extractable P levels of fresh and air-dried soils. Soil Res 23:613–621

    Article  CAS  Google Scholar 

  49. Suzuki T, Nakamura T, Fuse H (2012) Isolation of two novel marine ethylene-assimilating bacteria, Haliea Species ETY-M and ETY-NAG, containing particulate methane monooxygenase-like genes. Microbes Environ 27:54–60. doi:10.1264/jsme2.ME11256

    Article  PubMed  PubMed Central  Google Scholar 

  50. Takai K, Abe M, Miyazaki M et al (2013) Sunxiuqinia faeciviva sp. nov., a facultatively anaerobic organoheterotroph of the Bacteroidetes isolated from deep subseafloor sediment. Int J Syst Evol Microbiol 63:1602–1609

    Article  PubMed  CAS  Google Scholar 

  51. Tedersoo L, Bahram M, Polme S et al (2014) Global diversity and geography of soil fungi. Science 346(80):1–10

    Google Scholar 

  52. Vazquez P, Holguin G, Puente ME et al (2000) Phosphate-solubilizing microorganisms associated with the rhizosphere of mangroves in a semiarid coastal lagoon. Biol Fertil Soils 30:460–468

    Article  CAS  Google Scholar 

  53. Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  54. Wang Y, Sheng H-F, He Y et al (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  PubMed Central  CAS  Google Scholar 

  55. Wang Y, Sheng HF, He Y et al (2012) Comparison of the levels of bacterial diversity in freshwater, intertidal wetland, and marine sediments by using millions of illumina tags. Appl Environ Microb 78:8264–8271

    Article  CAS  Google Scholar 

  56. Wuchter C, Abbas B, Coolen MJL et al (2006) Archaeal nitrification in the ocean. Proc Natl Acad Sci USA 103:12317–12322

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  57. Wuchter C, Schouten S, Boschker HTS, Sinninghe Damsté JS (2003) Bicarbonate uptake by marine Crenarchaeota. FEMS Microbiol Lett 219:203–207

    Article  PubMed  CAS  Google Scholar 

  58. Xu X-W, Wu Y-H, Wang C-S et al (2007) Haloferax larsenii sp. nov., an extremely halophilic archaeon from a solar saltern. Int J Syst Evol Microbiol 57:717–720

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

Author DSL thanks Lady Tata memorial trust, Mumbai for providing Junior (2012–2014) and Senior research scholarship (2014–2016).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Sundararaman Muthuraman.

Ethics declarations

Conflict of interest

The authors declare that there is no conflict of interest in this manuscript.

Electronic Supplementary Material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 34 kb)

Supplementary material 2 (PDF 33 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sanka Loganathachetti, D., Sadaiappan, B., Poosakkannu, A. et al. Pyrosequencing-Based Seasonal Observation of Prokaryotic Diversity in Pneumatophore-Associated Soil of Avicennia marina . Curr Microbiol 72, 68–74 (2016). https://doi.org/10.1007/s00284-015-0920-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00284-015-0920-9

Keywords

Navigation