Skip to main content

Advertisement

Log in

The Selection Exerted by Oil Contamination on Mangrove Fungal Communities

  • Published:
Water, Air, & Soil Pollution Aims and scope Submit manuscript

Abstract

Mangrove ecosystems are tropical environments that are characterized by the interaction between the land and the sea. As such, this ecosystem is vulnerable to oil spills. Here, we show a culture-independent survey of fungal communities that are found in the sediments of the following two mangroves that are located on the coast of Sao Paulo State (Brazil): (1) an oil-spill-affected mangrove and (2) a nearby unaffected mangrove. Samples were collected from each mangrove forest at three distinct locations (transect from sea to land), and the samples were analyzed by quantitative PCR and internal transcribed spacer (ITS)-based PCR-DGGE analysis. The abundance of fungi was found to be higher in the oil-affected mangrove. Visual observation and correspondence analysis (CA) of the ITS-based PCR-DGGE profiles revealed differences in the fungal communities between the sampled areas. Remarkably, the oil-spilled area was quite distinct from the unaffected sampling areas. On the basis of the ITS sequences, fungi that are associated with the Basidiomycota and Ascomycota taxa were most common and belonged primarily to the genera Epicoccum, Nigrospora, and Cladosporium. Moreover, the Nigrospora fungal species were shown to be sensitive to oil, whereas a group that was described as “uncultured Basidiomycota” was found more frequently in oil-contaminated areas. Our results showed an increase in fungal abundance in the oil-polluted mangrove regions, and these data indicated potential fungal candidates for remediation of the oil-affected mangroves.

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

Similar content being viewed by others

References

  • Alongi, D. M. (1988). Bacterial productivity and microbial biomass in tropical mangrove sediments. Microbial Ecology, 15, 59–79.

    Article  Google Scholar 

  • Alongi, D. M. (2002). Present state and future of the world’s mangrove forests. Australian Institute Marine Science, 29, 331–349.

    Google Scholar 

  • Altschul, S. F., Madden, T. L., Schaffer, A. A., Zhang, J., Zhang, Z., Miller, W., & Lipman, D. J. (1997). Gapped BLAST and PSIBLAST: a new generation of protein database search programs. Nucleic Acids Research, 25, 3389–3402.

    Article  CAS  Google Scholar 

  • Ananda, K., & Sridhar, K. R. (2004). Diversity of filamentous fungi on decomposing leaf and woody litter of mangrove forests in the southwest coast of India. Current Science, 87, 1431–1437.

    Google Scholar 

  • Anderson, I. C., Campbell, C. D., & Prosser, J. I. (2003a). Diversity of fungi in organic soils under a moorland—Scots pine (Pinus Sylvestris L.) gradient. Environmental Microbiology, 5, 1121–1132.

    Article  Google Scholar 

  • Anderson, I. C., Campbell, C. D., & Prosser, J. I. (2003b). Potential bias of fungal 18S rDNA and internal transcribed spacer polymerase chain reaction primers for estimating fungal biodiversity in soil. Environmental Microbiology, 5, 36–47.

    Article  CAS  Google Scholar 

  • Andreote, F. D., Azevedo, J. L., & Araújo, W. L. (2009). Assessing the diversity of bacterial communities associated with plants. Brazilian Journal of Microbiology, 40, 417–432.

    Article  CAS  Google Scholar 

  • Aniszewski, E., Peixoto, R. S., Mota, F. F., Leite, S. G. F., & Rosado, A. S. (2010). Bioemulsifier production by Microbacterium sp. strains isolated from mangrove and their application to remove cadmiun and zinc from hazardous industrial residue. Brazilian Journal of Microbiology, 41, 235–245.

    Article  CAS  Google Scholar 

  • Arfi, Y., Buée, M., Marchand, C., Levasseur, A., & Record, E. (2012). Multiple markers pyrosequencing reveals highly diverse and host-specific fungal communities on the mangrove trees Avicennia marina and Rhizophora stylosa. FEMS Microbiology Ecology, 79, 433–444.

    Article  Google Scholar 

  • Barr, D. P., & Aust, S. D. (1994). Mechanisms white rot fungi use to degrade pollutants. Environmental Science and Technology, 28, 78A–87A.

    CAS  Google Scholar 

  • Das, S., Lyla, P. S., & Ajmal-Khan, S. (2006). Marine microbial diversity and ecology: importance and future perspectives. Current Science, 90, 1325–1335.

    CAS  Google Scholar 

  • Dias, A. C. F., Andreote, F. D., Dini-Andreote, F., Lacava, P. T., Sá, A. L. B., Melo, I. S., Azevedo, J. L., & Araújo, W. L. (2009). Diversity and biotechnological potential of culturable bacteria from Brazilian mangrove sediment. World Journal of Microbiology and Biotechnology, 25, 1305–1311.

    Article  CAS  Google Scholar 

  • Dias, A. C. F., Andreote, F. D., Rigonato, J., Fiore, M. F., Melo, I. S., & Araújo, W. L. (2010). The bacterial diversity in a Brazilian non-disturbed mangrove sediment. Antonie Van Leeuwenhoek, 98, 541–551.

    Article  Google Scholar 

  • Dias, A. C. F., Dini-Andreote, F., Taketani, R. G., Tsai, S. M., Azevedo, J. L., Melo, I. S., & Andreote, F. D. (2011). Archaeal communities in sediments of three contrasting mangroves. Journal of Soils and Sediments, 11, 1466–1476.

    Article  Google Scholar 

  • Embley, T. M. (2006). Multiple secondary origins of the anaerobic lifestyle in eukaryotes. Philosophical Transactions of the Royal Society B: Biological Sciences, 361, 1055–1067.

    Article  CAS  Google Scholar 

  • Felsenstein, J. (1985). Confidence limits on phylogenies: an approach using the bootstrap. Evolution, 39, 783–791.

    Article  Google Scholar 

  • Ferreira, T. O., Otero, X. L., Souza, V. S., Jr., Vidal-Torrado, P., Macías, F., & Firme, L. P. (2010). Spatial patterns of soil attributes and components in a mangrove system in Southeast Brazil (São Paulo). Journal of Soil and Sediments, 10, 995–1006.

    Article  CAS  Google Scholar 

  • Field, J. A., DeJong, E., Costa, G. F., & DeBont, J. A. M. (1992). Biodegradation of polycyclic aromatic hydrocarbons by new isolates of white rot fungi. Applied and Environmental Microbiology, 58, 2219–2226.

    CAS  Google Scholar 

  • Fierer, N., Jackson, J. A., Vilgalys, R., & Jackson, R. B. (2005). Assessment of soil microbial community structure by use of taxon-specific quantitative PCR assays. Applied and Environmental Microbiology, 71, 4117–4120.

    Article  CAS  Google Scholar 

  • Gomes, N. C. M., Cleary, D. F. R., Pinto, F. N., Egas, C., Almeida, A., et al. (2010). Taking root: enduring effect of rhizosphere bacterial colonization in mangroves. PLoS One, 5, e14065.

    Article  Google Scholar 

  • Harms, H., Schlosser, D., & Wick, L. Y. (2011). Untapped potential: exploiting fungi in bioremediation of hazardous chemicals. Nature Review Microbiology, 9, 177–192.

    Article  CAS  Google Scholar 

  • Holguin, G., Vazquez, P., & Bashan, Y. (2001). The role of sediment microorganisms in the productivity, conservation, and rehabilitation of mangrove ecosystems: an overview. Biology and Fertility of Soils, 33, 265–278.

    Article  CAS  Google Scholar 

  • Hussain, Q., Liu, Y., Zhang, A., Pan, G., Li, L., Zhang, X., Song, X., Cui, L., & Jin, Z. (2011). Variation of bacterial and fungal community structures in the rhizosphere of hybrid and standard rice cultivars and linkage to CO2 flux. FEMS Microbiology Ecology, 78, 116–128.

    Article  CAS  Google Scholar 

  • Kathiresan, K., & Bingham, B. L. (2001). Biology of Mangroves and Mangrove Ecosystems. Advances in Marine Biology, 40, 81–251.

    Article  Google Scholar 

  • Kimura, M. (1980). A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution, 16, 111–120.

    Article  CAS  Google Scholar 

  • Liang, J. B., Chen, Y. Q., Lan, C. Y., Tam, N. F. Y., Zan, Q. J., & Huang, L. N. (2007). Recovery of novel bacterial diversity from mangrove sediment. Marine Biology, 150, 739–747.

    Article  Google Scholar 

  • Raghukumar, S. (2004). The role of fungi in marine detrital processes. In N. Ramaiah (Ed.), Marine microbiology: facets and opportunities (pp. 91–101). Goa: National Institute of Oceanography.

    Google Scholar 

  • Rouske, J., Baath, E., Brookes, P. C., Lauber, C. L., Lozupone, C., Caporaso, J. G., Knight, R., & Fierer, N. (2010). Soil bacterial and fungal communities across a pH gradient in an arable soil. ISME Journal, 4, 1340–1351.

    Article  Google Scholar 

  • Saitou, N., & Nei, M. (1987). The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution, 4, 406–425.

    CAS  Google Scholar 

  • Santos, H. F., Carmo, F. L., Paes, J. E., Rosado, A. S., & Peixoto, R. S. (2011). Bioremediation of mangroves impacted by petroleum. Water, Air, and Soil Pollution, 216, 329–350.

    Article  CAS  Google Scholar 

  • Schloss, P. D., Westcott, S. L., Ryabin, T., Hall, J. R., Hartmann, M., Hollister, E. B., Lesniewski, R. A., Oakley, B. B., Parks, D. H., Robinson, C. J., Sahl, J. L., Stres, B., Thallinger, G. G., Van Horn, D. J., & Weber, C. F. (2009). Introducing mothur: open-source, plataform-independent, commuity-supported software for describing and comparing microbial communities. Applied and Environmental Microbiology, 75, 7537–7541.

    Article  CAS  Google Scholar 

  • Taketani, R. G., Franco, N. O., Rosado, A. S., & van Elsas, J. D. (2010). Microbial community response to a simulated hydrocarbon spill in mangrove sediments. Journal of Microbiology, 48, 7–15.

    Article  Google Scholar 

  • Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., & Kumar, S. (2011). MEGA5: Molecular Evolutionary Genetics Analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution, 28(10), 2731–2739.

    Article  CAS  Google Scholar 

  • Ter Braak, C. J. F. S., & Smilauer, P. (2002). CANOCO Reference manual and CanoDraw for Windows User’s Guide: Software for Canonical Community Ordination (version 4.5). 500 pp

  • Yan, B., Hong, K., & Yu, Z. N. (2006). Archaeal communities in mangrove soil characterized by 16S rRNA gene clones. Journal of Microbiology, 44, 566–571.

    CAS  Google Scholar 

Download references

Acknowledgments

This study was supported by a grant from the State of São Paulo Research Foundation (FAPESP/BIOTA 2004/13910-6). Also, C. C. Fasanella received a graduate fellowship from National Council for Scientific and Technological Development (CNPq, Brazil), and A.C.F. Dias (2008/54013-8) received a graduate fellowship. We also thank the support from João L. Silva for their support in mangrove expeditions and samplings and Msc. Francisco Dini-Andreote for the critical revision and discussion of the article.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Fernando Dini Andreote.

Electronic Supplementary Material

Below is the link to the electronic supplementary material.

ESM 1

(DOC 794 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Fasanella, C.C., Dias, A.C.F., Rigonato, J. et al. The Selection Exerted by Oil Contamination on Mangrove Fungal Communities. Water Air Soil Pollut 223, 4233–4243 (2012). https://doi.org/10.1007/s11270-012-1187-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11270-012-1187-4

Keywords

Navigation