This Article
Right arrow Full Text
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Christensen, B. B.
Right arrow Articles by Molin, S.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Christensen, B. B.
Right arrow Articles by Molin, S.
Agricola
Right arrow Articles by Christensen, B. B.
Right arrow Articles by Molin, S.

 Previous Article  |  Next Article 

Applied and Environmental Microbiology, May 2002, p. 2495-2502, Vol. 68, No. 5
0099-2240/02/$04.00+0     DOI: 10.1128/AEM.68.5.2495-2502.2002
Copyright © 2002, American Society for Microbiology. All Rights Reserved.

Metabolic Commensalism and Competition in a Two-Species Microbial Consortium

Bjarke B. Christensen,1,2 Janus A. J. Haagensen,1 Arne Heydorn,1 and Søren Molin1*

BioCentrum-DTU, Molecular Microbial Ecology Group, Technical University of Denmark, DK-2800 Lyngby,1 Division of Microbiological Safety, Danish Veterinary and Food Administration, DK-2860 Søborg, Denmark2

Received 23 October 2001/ Accepted 6 February 2002

We analyzed metabolic interactions and the importance of specific structural relationships in a benzyl alcohol-degrading microbial consortium comprising two species, Pseudomonas putida strain R1 and Acinetobacter strain C6, both of which are able to utilize benzyl alcohol as their sole carbon and energy source. The organisms were grown either as surface-attached organisms (biofilms) in flow chambers or as suspended cultures in chemostats. The numbers of CFU of P. putida R1 and Acinetobacter strain C6 were determined in chemostats and from the effluents of the flow chambers. When the two species were grown together in chemostats with limiting concentrations of benzyl alcohol, Acinetobacter strain C6 outnumbered P. putida R1 (500:1), whereas under similar growth conditions in biofilms, P. putida R1 was present in higher numbers than Acinetobacter strain C6 (5:1). In order to explain this difference, investigations of microbial activities and structural relationships were carried out in the biofilms. Insertion into P. putida R1 of a fusion between the growth rate-regulated rRNA promoter rrnBP1 and a gfp gene encoding an unstable variant of the green fluorescent protein made it possible to monitor the physiological activity of P. putida R1 cells at different positions in the biofilms. Combining this with fluorescent in situ hybridization and scanning confocal laser microscopy showed that the two organisms compete or display commensal interactions depending on their relative physical positioning in the biofilm. In the initial phase of biofilm development, the growth activity of P. putida R1 was shown to be higher near microcolonies of Acinetobacter strain C6. High-pressure liquid chromatography analysis showed that in the effluent of the Acinetobacter strain C6 monoculture biofilm the metabolic intermediate benzoate accumulated, whereas in the biculture biofilms this was not the case, suggesting that in these biofilms the excess benzoate produced by Acinetobacter strain C6 leaks into the surrounding environment, from where it is metabolized by P. putida R1. After a few days, Acinetobacter strain C6 colonies were overgrown by P. putida R1 cells and new structures developed, in which microcolonies of Acinetobacter strain C6 cells were established in the upper layer of the biofilm. In this way the two organisms developed structural relationships allowing Acinetobacter strain C6 to be close to the bulk liquid with high concentrations of benzyl alcohol and allowing P. putida R1 to benefit from the benzoate leaking from Acinetobacter strain C6. We conclude that in chemostats, where the organisms cannot establish in fixed positions, the two strains will compete for the primary carbon source, benzyl alcohol, which apparently gives Acinetobacter strain C6 a growth advantage, probably because it converts benzyl alcohol to benzoate with a higher yield per time unit than P. putida R1. In biofilms, however, the organisms establish structured, surface-attached consortia, in which heterogeneous ecological niches develop, and under these conditions competition for the primary carbon source is not the only determinant of biomass and population structure.

* Corresponding author. Mailing address: BioCentrum-DTU, Molecular Microbial Ecology Group, Building 301, The Technical University of Denmark, DK-2800 Lyngby, Denmark. Phone: 45 45 25 25 13. Fax: 45 45 88 73 28. E-mail: imsm{at}pop.dtu.dk.

Applied and Environmental Microbiology, May 2002, p. 2495-2502, Vol. 68, No. 5
0099-2240/02/$04.00+0     DOI: 10.1128/AEM.68.5.2495-2502.2002
Copyright © 2002, American Society for Microbiology. All Rights Reserved.



This article has been cited by other articles:

  • Min, K. R., Rickard, A. H. (2009). Coaggregation by the Freshwater Bacterium Sphingomonas natatoria Alters Dual-Species Biofilm Formation. Appl. Environ. Microbiol. 75: 3987-3997 [Abstract] [Full Text]  
  • Slater, F. R., Bruce, K. D., Ellis, R. J., Lilley, A. K., Turner, S. L. (2008). Heterogeneous Selection in a Spatially Structured Environment Affects Fitness Tradeoffs of Plasmid Carriage in Pseudomonads. Appl. Environ. Microbiol. 74: 3189-3197 [Abstract] [Full Text]  
  • Barreiros, L., Fernandes, A., Ferreira, A. C. S., Pereira, H., Bastos, M. M. S. M., Manaia, C. M., Nunes, O. C. (2008). New insights into a bacterial metabolic and detoxifying association responsible for the mineralization of the thiocarbamate herbicide molinate. Microbiology 154: 1038-1046 [Abstract] [Full Text]  
  • Brenner, K., Karig, D. K., Weiss, R., Arnold, F. H. (2007). Engineered bidirectional communication mediates a consensus in a microbial biofilm consortium. Proc. Natl. Acad. Sci. USA 104: 17300-17304 [Abstract] [Full Text]  
  • Simoes, L. C., Simoes, M., Vieira, M. J. (2007). Biofilm Interactions between Distinct Bacterial Genera Isolated from Drinking Water. Appl. Environ. Microbiol. 73: 6192-6200 [Abstract] [Full Text]  
  • Merod, R. T., Warren, J. E., McCaslin, H., Wuertz, S. (2007). Toward Automated Analysis of Biofilm Architecture: Bias Caused by Extraneous Confocal Laser Scanning Microscopy Images. Appl. Environ. Microbiol. 73: 4922-4930 [Abstract] [Full Text]  
  • Hansen, S. K., Haagensen, J. A. J., Gjermansen, M., Jorgensen, T. M., Tolker-Nielsen, T., Molin, S. (2007). Characterization of a Pseudomonas putida Rough Variant Evolved in a Mixed-Species Biofilm with Acinetobacter sp. Strain C6. J. Bacteriol. 189: 4932-4943 [Abstract] [Full Text]  
  • Moons, P., Van Houdt, R., Aertsen, A., Vanoirbeek, K., Engelborghs, Y., Michiels, C. W. (2006). Role of Quorum Sensing and Antimicrobial Component Production by Serratia plymuthica in Formation of Biofilms, Including Mixed Biofilms with Escherichia coli. Appl. Environ. Microbiol. 72: 7294-7300 [Abstract] [Full Text]  
  • Laue, H., Schenk, A., Li, H., Lambertsen, L., Neu, T. R., Molin, S., Ullrich, M. S. (2006). Contribution of alginate and levan production to biofilm formation by Pseudomonas syringae.. Microbiology 152: 2909-2918 [Abstract] [Full Text]  
  • Peterson, S. B., Dunn, A. K., Klimowicz, A. K., Handelsman, J. (2006). Peptidoglycan from Bacillus cereus Mediates Commensalism with Rhizosphere Bacteria from the Cytophaga-Flavobacterium Group. Appl. Environ. Microbiol. 72: 5421-5427 [Abstract] [Full Text]  
  • Reisner, A., Holler, B. M., Molin, S., Zechner, E. L. (2006). Synergistic Effects in Mixed Escherichia coli Biofilms: Conjugative Plasmid Transfer Drives Biofilm Expansion.. J. Bacteriol. 188: 3582-3588 [Abstract] [Full Text]  
  • Bruhn, J. B., Haagensen, J. A. J., Bagge-Ravn, D., Gram, L. (2006). Culture Conditions of Roseobacter Strain 27-4 Affect Its Attachment and Biofilm Formation as Quantified by Real-Time PCR. Appl. Environ. Microbiol. 72: 3011-3015 [Abstract] [Full Text]  
  • Kives, J., Guadarrama, D., Orgaz, B., Rivera-Sen, A., Vazquez, J., SanJose, C. (2005). Interactions in Biofilms of Lactococcus lactis ssp. cremoris and Pseudomonas fluorescens Cultured in Cold UHT Milk. J DAIRY SCI 88: 4165-4171 [Abstract] [Full Text]  
  • Rice, S. A., Koh, K. S., Queck, S. Y., Labbate, M., Lam, K. W., Kjelleberg, S. (2005). Biofilm Formation and Sloughing in Serratia marcescens Are Controlled by Quorum Sensing and Nutrient Cues. J. Bacteriol. 187: 3477-3485 [Abstract] [Full Text]  
  • Egland, P. G., Palmer, R. J. Jr., Kolenbrander, P. E. (2004). Interspecies communication in Streptococcus gordonii-Veillonella atypica biofilms: Signaling in flow conditions requires juxtaposition. Proc. Natl. Acad. Sci. USA 101: 16917-16922 [Abstract] [Full Text]  
  • Yi, K., Rasmussen, A. W., Gudlavalleti, S. K., Stephens, D. S., Stojiljkovic, I. (2004). Biofilm Formation by Neisseria meningitidis. Infect. Immun. 72: 6132-6138 [Abstract] [Full Text]  
  • Kreft, J.-U. (2004). Biofilms promote altruism. Microbiology 150: 2751-2760 [Abstract] [Full Text]  


Copyright © 2009 by the American Society for Microbiology.   For an alternate route to Journals.ASM.org, visit: http://intl-journals.asm.org | More Info»