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Environmental and genetic factors that contribute to Escherichia coli K-12 biofilm formation

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Abstract

Biofilms are communities of bacteria whose formation on surfaces requires a large portion of the bacteria’s transcriptional network. To identify environmental conditions and transcriptional regulators that contribute to sensing these conditions, we used a high-throughput approach to monitor biofilm biomass produced by an isogenic set of Escherichia coli K-12 strains grown under combinations of environmental conditions. Of the environmental combinations, growth in tryptic soy broth at 37°C supported the most biofilm production. To analyze the complex relationships between the diverse cell-surface organelles, transcriptional regulators, and metabolic enzymes represented by the tested mutant set, we used a novel vector-item pattern-mining algorithm. The algorithm related biofilm amounts to the functional annotations of each mutated protein. The pattern with the best statistical significance was the gene ontology ‘pyruvate catabolic process,’ which is associated with enzymes of acetate metabolism. Phenotype microarray experiments illustrated that carbon sources that are metabolized to acetyl-coenzyme A, acetyl phosphate, and acetate are particularly supportive of biofilm formation. Scanning electron microscopy revealed structural differences between mutants that lack acetate metabolism enzymes and their parent and confirmed the quantitative differences. We conclude that acetate metabolism functions as a metabolic sensor, transmitting changes in environmental conditions to biofilm biomass and structure.

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Acknowledgments

The authors thank the Coli Genetic Stock Center (Yale University, New Haven, CT) for strains and Dr. Philip Matsumura (University of Illinois at Chicago, Chicago IL) for plasmid pXL27. Dr. Jayma Moore (NDSU) performed the scanning electron microscopy at the Electron Microscopy Center. In the VMS Department, KV was funded by the North Dakota Agricultural Experiment Station. BMP, SK, and PS were funded by ADVANCE/FORWARD through grant HRD-0811239 from the National Science Foundation. Equipment was purchased from a seed grant from ND EPSCoR through grant EPS-0447679 from the NSF. In addition, BMP and PS were funded by an earmark grant on Agrosecurity: Disease Surveillance and Public Health provided through the Unites States Department of Agriculture-APHIS. In the Computer Science Department, AD and JW were funded by grant IDM-0415190 from the NSF. JW was also supported by the Center for Nanoscale Science and Engineering. At CNSE, SJS and DC were funded by grant N00014-06-1-0952 from the Office of Naval Research. At Loyola University, AJW was funded by grant GM066130 from the National Institute of General Medical Sciences.

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Authors and Affiliations

  1. Department of Veterinary and Microbiological Sciences, North Dakota State University, PO Box 6050-Dept 7690, Fargo, ND, 58108-6050, USA

    Birgit M. Prüß, Karan Verma, Priyankar Samanta, Preeti Sule, Sunil Kumar & Shelley M. Horne

  2. Department of Computer Sciences, North Dakota State University, Fargo, ND, 58108-6050, USA

    Jianfei Wu & Anne Denton

  3. Center for Nanoscale Science and Engineering, North Dakota State University, Fargo, ND, 58108-6050, USA

    Jianfei Wu, David Christianson & Shane J. Stafslien

  4. Department of Microbiology and Immunology, Loyola University Chicago, Maywood, IL, 60153, USA

    Alan J. Wolfe

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  1. Birgit M. Prüß
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  2. Karan Verma
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  3. Priyankar Samanta
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Correspondence to Birgit M. Prüß.

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Communicated by Sebastian Suerbaum.

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Prüß, B.M., Verma, K., Samanta, P. et al. Environmental and genetic factors that contribute to Escherichia coli K-12 biofilm formation. Arch Microbiol 192, 715–728 (2010). https://doi.org/10.1007/s00203-010-0599-z

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  • DOI: https://doi.org/10.1007/s00203-010-0599-z

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