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Journal of Soils and Sediments

, Volume 11, Issue 8, pp 1466–1476 | Cite as

Archaeal communities in the sediments of three contrasting mangroves

  • Armando Cavalcante Franco Dias
  • Francisco Dini-Andreote
  • Rodrigo Gouvêa Taketani
  • Siu Mui Tsai
  • João Lúcio Azevedo
  • Itamar Soares de Melo
  • Fernando Dini AndreoteEmail author
SEDIMENTS, SEC 4 • SEDIMENT-ECOLOGY INTERACTIONS • RESEARCH ARTICLE

Abstract

Purpose

This study evaluates the presence and diversity of 16S rRNA (rrs) and amoA genes from archaea in three mangrove sediments under different stages of preservation (one pristine mangrove, one affected by anthropogenic activity, and another contaminated by an oil spill) in the state of São Paulo (Brazil).

Materials and methods

A combination of DGGE, coupled with ordination analysis, and clone libraries of both targeted genes (rrs and amoA) was used to infer the diversity and phylogeny of archaeal communities in the mangrove analyzed samples.

Results and discussion

The DGGE combined with multivariate analysis revealed, based on the ribosomal gene, differences in archaeal communities according to environmental parameters such as mangrove location, anthropogenic activity, and oil contamination. The profiles based on the amoA gene were more similar than those obtained for the gene rrs, with the only difference statistically observed for the community found in the mangrove under anthropogenic pressure. Furthermore, phylogenetic analysis revealed most archaeal groups affiliated to sequences belonging to the Thaumarchaeota (53.1%, 24 OTUs) and Euryarchaeota (29.6%, 14 OTUs) phyla, in addition to 14 sequences affiliated to an unclassified Archaea (16.1%, 8 OTUs). Concerning the analysis of the amoA gene, mangroves harbored sequences affiliated with those previously described in water column and soil/sediment samples, besides two possible clusters specifically found in mangroves.

Conclusions

The findings are that the mangroves act as a reservoir for archaeal diversity, are possibly involved in nitrogen transformation in this ecosystem, and are affected by distinct pressures caused by anthropogenic activities.

Keywords

16S rRNA Ammonium processing amoA Euryarchaeota Thaumarchaeota 

Notes

Acknowledgments

This study was supported by a grant from the State of São Paulo Research Foundation (FAPESP/BIOTA 2004/13910-6). F.D. Andreote received a postdoctoral fellowship from FAPESP (2007/56360-4), and R.G. Taketani was a recipient of a postdoctoral grant from CNPq. Also, A.C.F. Dias received a graduate fellowship (2008/54013-8). We also thank the support from the Oceanographic Institute (IO, USP, São Paulo), especially Dr. Ricardo P. Menghini and João L. Silva for their support in mangrove expeditions and samplings.

References

  1. Andreote FD, Azevedo JL, Araújo WL (2009) Assessing the diversity of bacterial communities associated with plants. Braz J Microbiol 40:417–432CrossRefGoogle Scholar
  2. Beman JM, Popp BN, Francis CA (2008) Molecular and biogeochemical evidence for ammonia oxidation by marine Crenarchaeota in the Gulf of California. ISME J 2:429–441CrossRefGoogle Scholar
  3. Bernhard AE, Landry ZC, Blevins A, de la Torre JS, Giblin AE, Stahl DA (2010) Abundance of ammonia-oxidizing archaea and bacteria along an estuarine salinity gradient in relation to potential nitrification rates. Appl Environ Microbiol 76:1285–1289CrossRefGoogle Scholar
  4. Caffrey JM, Bano N, Kalanetra K, Hollibaugh JT (2007) Ammonia oxidation and ammonia-oxidizing bacteria and archaea from estuaries with differing histories of hypoxia. ISME J 1:660–662CrossRefGoogle Scholar
  5. Dias ACF, Andreote FD, Rigonato J, Fiore MF, Melo IS, Araújo WL (2010) The bacterial diversity in a Brazilian non-disturbed mangrove sediment. Antonie Van Leeuwenhoek 98:541–551CrossRefGoogle Scholar
  6. Erguder TH, Boon N, Wittebolle L, Marzorati M, Verstraete W (2009) Environmental factors shaping the ecological niches of ammonia oxidizing archaea. FEMS Microbiol Rev 33:855–869CrossRefGoogle Scholar
  7. Ferreira TO, Otero XL, Souza VS Jr, Vidal-Torrado P, Macías F, Firme LP (2010) Spatial patterns of soil attributes and components in a mangrove system in Southeast Brazil (São Paulo). J Soil Sediment 10:995–1006CrossRefGoogle Scholar
  8. Francis CA, Roberts KJ, Beman JM, Santoro AE, Oakley BB (2005) Ubiquity and diversity of ammonia-oxidizing archaea in water columns and sediments of the ocean. Proc Natl Acad Sci USA 102:14683–14688CrossRefGoogle Scholar
  9. Francis CA, Beman JM, Kuypers MMM (2007) New processes and players in the nitrogen cycle: the microbial ecology of anaerobic and archaeal ammonia oxidation. ISME J 1:19–27CrossRefGoogle Scholar
  10. Fuhrman JA, McCallum K, Davis AA (1992) Novel major archaebacterial group from marine plankton. Nature 356:148–149CrossRefGoogle Scholar
  11. Glaser K, Hack E, Inselsbacher E, Strauss J, Wanek W, Zechmeister-Boltenstern S, Sessitsch A (2010) Dynamics of ammonia-oxidizing communities in barley-planted bulk soil and rhizosphere following nitrate and ammonium fertilizer amendment. FEMS Microbiol Ecol 74:575–591CrossRefGoogle Scholar
  12. Gomes NCM, Borges LR, Paranhos R, Pinto FN, Mendonça-Hagler LCS, Smalla K (2008) Exploring the diversity of bacterial communities in sediments of urban mangrove forests. FEMS Microbiol Ecol 66:96–109CrossRefGoogle Scholar
  13. Holguin G, Vazquez P, Bashan Y (2001) The role of sediment microorganisms in the productivity, conservation, and rehabilitation of the mangrove ecosystems: an overview. Biol Fertil Soils 33:265–278CrossRefGoogle Scholar
  14. Karner MB, DeLong EF, Karl DM (2001) Archaeal dominance in the mesopelagic zone of the Pacific Ocean. Nature 409:507–510CrossRefGoogle Scholar
  15. Kathiresan K, Bingham BL (2001) Biology of mangroves and mangrove ecosystem. Adv Mar Biol 40:81–251CrossRefGoogle Scholar
  16. Li M, Cao H, Hong Y, Gu JD (2010) Spatial distribution and abundances of ammonia-oxidizing archaea (AOA) and ammonia-oxidizing bacteria (AOB) in mangrove sediments. Appl Microbiol Biotechnol 89:1243–1254CrossRefGoogle Scholar
  17. Lyimo TJ, Pol A, Jetten MS, den Camp HJ (2009) Diversity of methanogenic archaea in a mangrove sediment and isolation of a new Methanococcoides strain. FEMS Microbiol Lett 291:247–253CrossRefGoogle Scholar
  18. Muyzer G, de Waal EC, Uitterlinden AG (1993) Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl Environ Microbiol 59:695–700Google Scholar
  19. Nicol GW, Schleper C (2006) Ammonia-oxidising Crenarchaeota: important players in the nitrogen cycle? Trends Microbiol 14:207–212CrossRefGoogle Scholar
  20. Øvreas L, Forney L, Daae FL, Torsvik V (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 63:3367–3373Google Scholar
  21. Sahan E, Muyzer G (2008) Diversity and spatio-temporal distribution of ammonia-oxidizing Archaea and Bacteria in sediments of the Westerschelde estuary. FEMS Microbiol Ecol 64:175–186CrossRefGoogle Scholar
  22. Santoro AE, Francis CA, Sieyes NR, Boehm AB (2008) Shifts in the relative abundance of ammonia-oxidizing bacteria and archaea across physicochemical gradients in a subterranean estuary. Environ Microbiol 10:1068–1079CrossRefGoogle Scholar
  23. Schloss PD, Handelsman J (2005) Introducing DOTUR, a computer program for defining operational taxonomic units and estimating species richness. Appl Environ Microbiol 71:1501–1506CrossRefGoogle Scholar
  24. Sousa OV, Macrae A, Menezes FGR, Gomes NCM, Vieira RHSF, Mendonça-Hagler LCS (2006) The impact of shrimp farming effluent on bacterial communities in mangrove waters, Ceara, Brazil. Mar Pollut Bull 52:1725–1734CrossRefGoogle Scholar
  25. Strous M, Fuerst JA, Kramer EHM, Logemann S, Muyzer G, van de Pas-Schoonen KT, Webb R, Kuenen J, Jetten MSM (1999) Missing lithotroph identified as new planctomycete. Nature 400:446–449CrossRefGoogle Scholar
  26. Taketani RG, Franco NO, Rosado AS, van Elsas JD (2010a) Microbial community response to a simulated hydrocarbon spill in mangrove sediments. J Microbiol 48:7–15CrossRefGoogle Scholar
  27. Taketani RG, Yoshiura CA, Dias ACF, Andreote FD, Tsai SM (2010b) Diversity and identification of methanogenic archaea and sulphate-reducing bacteria in sediments from a pristine tropical mangrove. Antonie Van Leeuwenhoek 97:401–411CrossRefGoogle Scholar
  28. Treusch AH, Leininger S, Kletzin A, Schuster SC, Klenk H-P, Schleper C (2005) Novel genes for nitrite reductase and Amo-related proteins indicate a role of uncultivated mesophilic crearchaeota in nitrogen cycling. Environ Microbiol 7:1985–1995CrossRefGoogle Scholar
  29. Van Raij B, Cantarella H, Andrade JC, Quaggio JA (2001) Análise química para avaliação da fertilidade de solos tropicais. Campinas: Instituto Agronômico 285 pGoogle Scholar
  30. Woese CR, Kandler O, Wheels ML (1990) Towards a natural system of organisms: proposal for the domains archaea, bacteria, and eukarya. Proc Natl Acad Sci USA 87:4576–4579CrossRefGoogle Scholar
  31. Yan B, Hong K, Yu ZN (2006) Archaeal communities in mangrove soil characterized by 16S rRNA gene clones. J Microbiol 44:566–571Google Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Armando Cavalcante Franco Dias
    • 1
    • 3
  • Francisco Dini-Andreote
    • 1
    • 2
  • Rodrigo Gouvêa Taketani
    • 3
  • Siu Mui Tsai
    • 3
  • João Lúcio Azevedo
    • 3
  • Itamar Soares de Melo
    • 1
  • Fernando Dini Andreote
    • 4
    Email author
  1. 1.Laboratory of Environmental MicrobiologyCNPMA — Embrapa EnvironmentJaguariúnaBrazil
  2. 2.Department of Genetics, Escola Superior de Agricultura “Luiz de Queiroz” (ESALQ)University of São PauloPiracicabaBrazil
  3. 3.Center for Nuclear Energy in Agriculture, CENA/USPUniversity of São PauloPiracicabaBrazil
  4. 4.Department of Soil Science, Escola Superior de Agricultura “Luiz de Queiroz” (ESALQ)University of São PauloPiracicabaBrazil

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