Biofilm form and function: carbon availability affects biofilm architecture, metabolic activity and planktonic cell yield

• Published in: Journal of applied microbiology 2011-02, Vol.110 (2), p.387-398
• Main Authors: Bester, E, Kroukamp, O, Hausner, M, Edwards, E.A, Wolfaardt, G.M
• Format: Article
• Language: English
• Subjects: biofilm biology; Biofilms - growth & development; Biological and medical sciences; Biomass; Biotransformation; Carbon - metabolism; carbon investment; carbon limitation; Fundamental and applied biological sciences. Psychology; Microbiology; Plankton - cytology; proliferation; Pseudomonas - cytology; Pseudomonas - growth & development; Pseudomonas - physiology
• ISSN: 1364-5072; 1365-2672
• DOI: 10.1111/j.1365-2672.2010.04894.x

Aims: To investigate carbon transformation by biofilms and changes in biofilm architecture, metabolic activity and planktonic cell yield in response to fluctuating carbon availability. Methods and Results: Pseudomonas sp. biofilms were cultured under alternating carbon-replete and carbon-limited conditions. A shift to medium without added carbon led to a 90% decrease in biofilm respiration rate and a 40% reduction in planktonic cell yield within 1 h. Attached cell division and progeny release were shown to contribute to planktonic cell numbers during carbon limitation. Development of a significantly enlarged biofilm surface area during carbon limitation facilitated a rapid increase in whole-biofilm metabolic activity, cell yield and biomass upon the re-introduction of carbon after 8 days of limitation. The cumulative number of planktonic cells (>10¹⁰ CFU) released from the biofilm during the cultivation period contained only 1·0% of the total carbon available to the biofilm, with 6·5% of the carbon retained in the biofilm and 54% mineralized to CO₂. Conclusions: Biofilm-derived planktonic cell yield is a proliferation mechanism. The rapid response of biofilms to environmental perturbations facilitates the optimal utilization of resources to promote both proliferation and survival. Biofilms function as efficient catalysts for environmental carbon transformation and mineralization. Significance and Impact of the study: A greater understanding of the relationship between biofilm form and function can inform strategies intended to control and/or promote biofilm formation.