An Escherichia coli Nitrogen Starvation Response Is Important for Mutualistic Coexistence with Rhodopseudomonas palustris

Journal Article · 04 May 2018 · Applied and Environmental Microbiology

DOI: https://doi.org/10.1128/aem.00404-18 · OSTI ID:1541703

McCully, Alexandra L. ^[1]; Behringer, Megan G. ^[2]; Gliessman, Jennifer R. ^[1]; Pilipenko, Evgeny V. ^[3]; Mazny, Jeffrey L. ^[1]; Lynch, Michael ^[2]; Drummond, D. Allan ^[3]; McKinlay, James B. ^[1]; Atomi, Haruyuki ^[4]

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1. Indiana Univ., Bloomington, IN (United States). Dept. of Biology
2. Arizona State Univ., Tempe, AZ (United States). School of Life Sciences, Biodesign Center for Mechanisms of Evolution
3. Univ. of Chicago, Chicago, IL (United States). Dept. of Biochemistry and Molecular Biology, Dept. of Human Genetics
4. Kyoto Univ., Kyoto (Japan)

Microbial mutualistic cross-feeding interactions are ubiquitous and can drive important community functions. Engaging in cross-feeding undoubtedly affects the physiology and metabolism of individual species involved. However, the nature in which an individual species' physiology is influenced by cross-feeding and the importance of those physiological changes for the mutualism have received little attention. We previously developed a genetically tractable coculture to study bacterial mutualisms. The coculture consists of fermentative Escherichia coli and phototrophic Rhodopseudomonas palustris. In this coculture, E. coli anaerobically ferments sugars into excreted organic acids as a carbon source for R. palustris. In return, a genetically engineered R. palustris strain constitutively converts N₂ into NH₄⁺, providing E. coli with essential nitrogen. Using transcriptome sequencing (RNA-seq) and proteomics, we identified transcript and protein levels that differ in each partner when grown in coculture versus monoculture. When in coculture with R. palustris, E. coli gene expression changes resembled a nitrogen starvation response under the control of the transcriptional regulator NtrC. By genetically disrupting E. coli NtrC, we determined that a nitrogen starvation response is important for a stable coexistence, especially at low R. palustris NH₄⁺ excretion levels. Destabilization of the nitrogen starvation regulatory network resulted in variable growth trends and, in some cases, extinction. Finally, our results highlight that alternative physiological states can be important for survival within cooperative cross-feeding relationships.

• Research Organization: Indiana Univ., Bloomington, IN (United States)
• Sponsoring Organization: USDOE Office of Science (SC)
• Grant/Contract Number: SC0008131
• OSTI ID: 1541703
• Journal Information: Applied and Environmental Microbiology, Vol. 84, Issue 14; ISSN 0099-2240
• Publisher: American Society for MicrobiologyCopyright Statement
• Country of Publication: United States
• Language: English