Abstract
Most oil from oceanic spills converges on coastal ecosystems, such as mangrove forests, which are threatened with worldwide disappearance. Particular bacteria that inhabit the rhizosphere of local plant species can stimulate plant development through various mechanisms; it would be advantageous if these would also be capable of degrading oil. Such bacteria may be important in the preservation or recuperation of mangrove forests impacted by oil spills. This study aimed to compare the bacterial structure, isolate and evaluate bacteria able to degrade oil and stimulate plant growth, from the rhizospheres of three mangrove plant species. These features are particularly important taking into account recent policies for mangrove bioreme-diation, implying that oil degradation as well as plant maintenance and health are key targets. Fifty-seven morphotypes were isolated from the mangrove rhizospheres on Bushneil-Haas (BH) medium supplemented with oil as the sole carbon source and tested for plant growth promotion. Of this strains, 60% potentially fixed nitrogen, 16% showed antimicrobial activity, 84% produced siderophores, 51% had the capacity to solubilize phosphate, and 33% produced the indole acetic acid hormone. Using gas chromatography, we evaluated the oil-degrading potential of ten selected strains that had different morphologies and showed Plant Growth Promoting Rhizobacteria (PGPR) features. The ten tested strains showed a promising degradation profile for at least one compound present in the oil. Among degrader strains, 46% had promising PGPR potential, having at least three of the above capacities. These strains might be used as a consortium, allowing the concomitant degradation of oil and stimulation of mangrove plant survival and maintenance.
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References
Altschul, S., W. Gish, W. Miller, E. Myers, and D. Lipman. 1990. Basic local alignment search tool. J. Mol. Biol. 215, 403–410.
Bakken, L.R. and V. Lindahl. 1995. Recovery of bacterial cells from soil. In J.D. van Elsas and J.T. Trevors (ed.), Nucleic acids in the environment: Methods and applications, pp. 9–27. Springer-Verlag, Heidelberg, Germany.
Barbier, E.B., E.W. Koch, B.R. Siliman, S.D. Hacker, E. Wolanski, J. Primavera, E.F. Granek, and et al. 2008. Coastal ecosystembased management with nonlinear ecological functions and values. Science 318, 321–323.
Barbieri, P., T. Zanelli, E. Galli, and G. Zanelli. 1986. Wheat inoculation with Azospirillum brasilense Sp6 and some mutants altered in nitrogen fixation and indole-3-acetic acid production. FEMS Microbiol. Lett. 36, 87–90.
Bashan, Y. and G. Holguin. 1997. Azospirillum plant relationships environmental and physiological advances (1990–1996). Can. J. Microbiol. 43, 103–121.
Bashan, Y. and G. Holguin. 2002. Plant growth-promoting bacteria: A potential tool for arid mangrove reforestation. Trees 16, 159–166.
Bent, E., S. Tuzun, C.P. Chanway, and S. Eneback. 2001. Alterations in plant growth and in root hormone levels of lodgepole pinesinoculated with rhizobacteria. Can. J. Microbiol. 47, 793–800.
Brito, E.M., R. Guyoneaud, M. Goni-Urriza, A. Ranchou-Peyruse, A. Verbaere, M.A.C. Crapez, J.C.A. Wasserman, and R. Duran. 2006. Characterization of hydrocarbonoclastic bacterial communities from mangrove sediments in Guanabara bay, Brazil. Res. Microbiol. 157, 752–762.
Burd, G.I., D.G. Dixon, and B.R. Glick. 2000. Plant growth-promoting bacteria that decrease heavy metal toxicity in plants. Can. J. Microbiol. 46, 237–245.
Burns, K.A., S. Codi, and N.C. Duke. 2000. Gladstone, Australia field studies: Weathering and degradation of hydrocarbons in oiled mangrove and salt marsh sediments with and without the application of an experimental bioremediation protocol. Mar. Pollut. Bull. 41, 392–402.
Burns, K.A., S. Levings, and S. Garrity. 1993. How many years before mangrove ecosystem recover from catastrophic oil spills? Mar. Pollut. Bull. 26, 239–248.
Cheng, Z., Y.Y.C. Wei, W.W.L. Sung, B.R. Glick, and B.J. McConkey. 2009. Proteomic analysis of the response of the plant growth-promoting bacterium Pseudomonas putida UW4 to nickel stress. Proteome Sci. 7, 18.
Costa, R., M. Götz, N. Mrotzek, G. Berg, J. Lottmann, and K. Smalla. 2006. Effects of site and plant species on rhizosphere community structure as revealed by molecular analysis of different microbial guilds. FEMS Microbiol. Ecol. 56, 236–249.
Duke, N.C., K.A. Burns, R.P.J. Swannell, O. Dalhaus, and R. Rupp. 2000. Dispersant use and a bioremediation strategy as alternate means of reducing impacts of large oil spills on mangroves: The Gladstone field trials. Mar. Pollut. Bull. 41, 403–412.
Duke, N.C., J.O. Meynecke, S. Dittmann, A.M. Ellison, K. Anger, U. Berguer, S. Cannicci, and et al. 2007. A world without mangroves? Science 317, 41–42.
Füchtenbusch, B., D. Wullbrandt, and A. Steinbuchel. 2000. Production of polyhydroxyalkanoic acids by Ralstonia eutropha and Pseudomonas oleovorans from an oil remaining from biotechnological rhamnose production. Appl. Microbiol. Biotechnol. 53, 167–172.
Garbeva, P., J.D. van Elsas, and J.A. Veen. 2007. Rhizosphere microbial community and its response to plant species and soil history. Plant Soil 302, 19–32.
Glick, B.R. 1995. The enhancement of plant growth by free-living bacteria. Can. J. Microbiol. 41, 109–117.
Gomes, N.C.M., L.R. Borges, R. Paranhos, F.N. Pinto, L.C. Mendonça-Hagler, and K. Smalla. 2008. Exploring the diversity of bacterial communities in sediments of urban mangrove forests. FEMS Microbiol. Ecol. 66, 96–109.
Gulati, A., P. Vyas, and R.C. Kasana. 2009. Plant growth-promoting and rhizosphere-competent Acinetobacter rhizosphaerae strain BIHB 723 from the cold deserts of the Himalayas. Curr. Microbiol. 58, 371–377.
Heuer, H. and K. Smalla. 1997. Application of denaturing gradient gel electrophoresis (DGGE) and temperature gradient gel electrophoresis for studying soil microbial communities, pp. 353–373. In J.D. van Elsas, J. Trevors, and E.M.H. Wellington (eds.) Modern Soil Microbiology. Marcel Dekker, New York, NY, USA.
Kang, S., G. Joo, M. Hamayun, C. Na, D. Shin, H.Y. Kim, J. Hong, and I. Lee. 2009. Gibberellin production and phosphate solubilization by newly isolated strain of Acinetobacter calcoaceticus and its effect on plant growth. Biotechnol. Lett. 31, 277–281.
Karakurt, H. and R. Aslantas. 2010. Effects of some plants growth promoting Rizobacteria (PGPR) strains on plant growth and leaf nutrient content of apple. J. Fruit. Ornam. Plant. Res. 102, 101–119.
Kathiresan, K. and B.L. Binghan. 2001. Biology of mangroves and mangrove ecosystems. Adv. Mar. Biol. 40, 81–251.
Kloepper, J.W., J. Leong, M. Teintze, and M.N. Schroth. 1980. Pseudomonas siderophores: a mechanism explaining disease-suppressive soils. Curr. Microbiol. 4, 317.
Kumar, S., K. Tamura, and M. Nei. 1993. MEGA: Molecular Evolutionary Genetics Analysis, Ver. 1.0. The Pennsylvania State University, Philadelphia, USA.
Li, H., Q. Zhao, M.C. Boufadel, and A.D. Venosa. 2007. A universal nutrient application strategym for the bioremediation of oil-polluted beaches. Mar. Pollut. Bull. 54, 1146–1161.
Lucy, M., E. Reed, and B.R. Glick. 2004. Application of free living plant growth-promoting rhizobacteria. Antonie van Leeuwenhoek 86, 1–25.
Lugtenberg, B.J., L. Dekkers, and G.V. Bloemberg. 2001. Molecular determinants of rhizosphere colonization by Pseudomonas. Annu. Rev. Phytopathol. 39, 461–490.
Maciel-Souza, M.C., A. Macrae, A.G.T. Volpon, P.S. Ferreira, and L.C. Mendonça-Hagler. 2006. Chemical and microbiological characterization of mangrove sediments after a large oil-spill in Guanabara Bay — RJ — Brazil. Braz. J. Microbiol. 37, 262–266.
Monteiro, J.M., R.E. Vollú, M.R.R. Coelho, C.S. Alviano, A.F. Blank, and L. Seldin. 2009. Comparison of the bacterial community and characterization of plant growth promoting Rhizobacteria from different genotypes of Chrysopogon zizanioides (L.) Roberty (Vetiver) Rhizospheres. J. Microbiol. 47, 1–8.
Mota, F.F., E.A. Gomes, I.E. Marriel, E. Paiva, and L. Seldin. 2008. Effect of liming on the structure of bacterial and fungal communities in bulk soil and rhizospheres of aluminum-tolerant and aluminum-sensitive maize (Zea mays L.) lines cultivated in Cerrado soil. J. Microbiol. Biotechnol. 18, 805–814.
Mota, F.F., A. Nobrega, I.E. Marriel, E. Paiva, and L. Seldin. 2002. Genetic diversity of Paenibacillus polymyxa populations isolated from the rhizosphere of four cultivars of maize (Zea mays) planted in Cerrado soil. Appl. Soil Ecol. 20, 119–132.
Patten, C. and B.R. Glick. 1996. Bacterial biosynthesis of indole-3-acetic acid. Can. J. Microbiol. 42, 207–220.
Peixoto, R.S., R.F. Silva, and A.S. Rosado. 2009. Biorremediaçãoo de ambientes contaminados com petróleo e seus derivados. Microbiologia in foco 8, 17–30.
Poly, F., L.J. Monrozier, and R. Bally. 2001. Impovement in the RFLP procedure for studying the diversity of nifH genes in communities of nitrogen fixers in soil. Res. Microbiol. 152, 95–103.
Richard, J.Y. and T.M. Vogel. 1999. Characterization of a soil bacterial consortium capable of degrading diesel fuel. Int. Biodet. Biod. 44, 93–100.
Richter, B. and K. Smalla. 2007. Screening of rhizosphere and soil bacteria for transformability. Environ. Biosafety 6, 91–99.
Rodriguez, H., S. Vesely, S. Shah, and B.R. Glick. 2008. Isolation and characterization of nickel resistant Pseudomonas strains and their effect on the growth of non-transformed and transgenic canola plants. Curr. Microbiol. 57, 170–174.
Rojas, A., G. Holguin, B. Glick, and Y. Bashan. 2001. Synergism between Phyllobacterium sp. (N2-fixer) and Bacillus licheniformis (P-solubilizer), both from a semi-arid mangrove rhizosphere. FEMS Microbiol. Ecol. 35, 181–187.
Rosado, A.S., F.S. Azevedo, D.W.G. Cruz, and L. Seldin. 1998. Phenotypic and genetic diversity of Paenibacillus azotofixans strains isolated from rhizoplane or rhizosphere of different grasses. J. Appl. Microbiol. 84, 216–226.
Rosado, A.S. and L. Seldin. 1993. Production of a potentially novel anti-microbial substance by Bacillus polymyxa. World J. Microbiol. Biotechnol. 9, 521–528.
Santos, H.F., F.L. Carmo, J.E. Paes, A.S. Rosado, and R.S. Peixoto. 2010. Bioremediation of mangroves impacted by petroleum. Water Air Soil Poll. doi:10.1007/s11270-010-0536-4.
Schwyn, B. and J.B. Neilands. 1987. Universal chemical assay for the detection and determination of siderophores. Anal. Biochem. 160, 47–56.
Tang, Y.W. and J. Bonner. 1947. The enzymatic inactivation of indoleacetic acid. I. Some characteristics of the enzyme contained in pea seedlings. Arch. Biochem. 13, 11–25.
Timmusk, S., N. Grantcharov, and E.G.H. Wagner. 2005. Paenibacillus polymyxa invades plant roots and forms biofilms. Appl. Environ. Microbiol. 71, 7292–7300.
Thompson, J.D., T.J. Gibson, F. Plewniak, F. Jeanmouginm, and D.G. Higgins. 1997. The CLUSTAL X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25, 4876–4882.
Toledo, G., Y. Bashan, and A. Soeldner. 1995. In vitro colonization and increase in nitrogen fixation of seedling roots of black mangrove inoculated by a filamentous cyanobacteria. Can. J. Microbiol. 41, 1012–1020.
UNEP — United Nations Environment Programme. 1991. Determinations of petroleum hydrocarbons in sediments. Reference methods for marine pollution studies, n 20.
Vazquez, P., G. Holguin, M.E. Puente, A. Lopez-Cortes, and Y. Bashan. 2000. Phosphate-solubilizing microorganisms associated with the rhizosphere of mangroves in a semiarid coastal lagoon. Biol. Fertil. Soils 30, 460–468.
von der Weid, I., V. Artursson, L. Seldin, and J.K. Jansson. 2005. Antifungal and root surface colonization properties of GFP-tagged Paenibacillus brasilensis PB177. World J. Microbiol. Biotechnol. 21, 1591–1597.
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do Carmo, F.L., dos Santos, H.F., Martins, E.F. et al. Bacterial structure and characterization of plant growth promoting and oil degrading bacteria from the rhizospheres of mangrove plants. J Microbiol. 49, 535–543 (2011). https://doi.org/10.1007/s12275-011-0528-0
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DOI: https://doi.org/10.1007/s12275-011-0528-0