Overflow metabolism provides a selective advantage to Escherichia coli in mixed cultures

Yasir, Muhammad, Thomson, Nicholas M., Turner, A. Keith, Webber, Mark A. and Charles, Ian G. (2024) Overflow metabolism provides a selective advantage to Escherichia coli in mixed cultures. Annals of Microbiology, 74. ISSN 1590-4261

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Abstract

Purpose: It has previously been shown that organic acids produced by Escherichia coli suppress the growth of Pseudomonas aeruginosa in co-cultures under conditions of glucose excess, due to overflow metabolism. Inactivation of genes involved in central carbon metabolism favours fermentation of glucose over respiration and therefore increases production of organic acid by-products such as acetate and lactate. We sought to extend and refine the list of genes known to contribute to the metabolic balance between respiration and fermentation, to better understand the role of overflow metabolism in competitive survival of E. coli. Methods: We confirmed the previous finding that E. coli excludes P. aeruginosa from co-cultures by producing organic acids in the presence of glucose. Using a genome-wide transposon screen we identified E. coli genes that are important for survival in co-cultures with P. aeruginosa, both with and without glucose supplementation. Results: Central carbon metabolism was the dominant gene function under selection in our experimental conditions, indicating that the observed inhibition is a side-effect of overflow metabolism adopted by E. coli as a response to high glucose concentrations. The presence of a competing species increased the selective pressure for central carbon metabolism genes, with 31 important for growth in the presence of P. aeruginosa and glucose, while only 9 were significant for pure E. coli cultures grown with glucose. In our experiments, each transposon mutant was competed against all others in the pool, suggesting that overflow metabolism provides benefits to individual E. coli cells in addition to competitive inhibition derived from acidification of the growth medium. Conclusion: Co-culture assays using transposon mutant libraries can provide insight into the selective pressures present in mixed species competition. This work demonstrates central carbon metabolism is the dominant gene function under selection in E. coli for aerobic growth in glucose and a side-effect of this is overflow metabolism which can inhibit growth of bystander species.

Item Type: Article
Additional Information: Availability of data and materials: The datasets generated and analysed during the current study are available in the Array Express repository under accession number E-MTAB-13391 (https://www.ebi.ac.uk/biostudies/arrayexpress). Funding information: This work was funded by the Biotechnology and Biological Sciences Research Council Institute Strategic Programme Microbes in the Food Chain BB/R012504/1 and its constituent project BBS/E/F/000PR10349.
Uncontrolled Keywords: competition,mixed acid fermentation,overflow metabolism,tradis-xpress,warburg effect,applied microbiology and biotechnology ,/dk/atira/pure/subjectarea/asjc/2400/2402
Faculty \ School: Faculty of Medicine and Health Sciences > Norwich Medical School
UEA Research Groups: Faculty of Medicine and Health Sciences > Research Centres > Norwich Institute for Healthy Aging
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Depositing User: LivePure Connector
Date Deposited: 23 Oct 2024 09:30
Last Modified: 25 Oct 2024 15:30
URI: https://ueaeprints.uea.ac.uk/id/eprint/97120
DOI: 10.1186/s13213-024-01760-z

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