An Escherichia coli nitrogen starvation response is important for mutualistic coexistence with Rhodopseudomonas palustris

Alexandra L. McCully, Megan G. Behringer, Jennifer R. Gliessman, Evgeny V. Pilipenko, Jeffrey L. Mazny, Michael Lynch, D. Allan Drummond, James B. McKinlay

Research output: Contribution to journalArticle

Abstract

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. Our results highlight that alternative physiological states can be important for survival within cooperative cross-feeding relationships.

Original languageEnglish (US)
Article numbere00404-18
JournalApplied and Environmental Microbiology
Volume84
Issue number14
DOIs
StatePublished - Jul 1 2018

Fingerprint

Rhodopseudomonas palustris
Rhodopseudomonas
coculture
Coculture Techniques
Starvation
starvation
coexistence
Nitrogen
Escherichia coli
nitrogen
physiology
mutualism
proteomics
RNA Sequence Analysis
monoculture
organic acid
excretion
Symbiosis
gene expression
RNA

Keywords

  • Coculture
  • Cross-feeding
  • Escherichia coli
  • Fermentation
  • Mutualism
  • Nitrogen fixation
  • Nitrogen starvation
  • NtrC
  • Photoheterotrophy
  • Rhodopseudomonas

ASJC Scopus subject areas

  • Biotechnology
  • Food Science
  • Applied Microbiology and Biotechnology
  • Ecology

Cite this

An Escherichia coli nitrogen starvation response is important for mutualistic coexistence with Rhodopseudomonas palustris. / McCully, Alexandra L.; Behringer, Megan G.; Gliessman, Jennifer R.; Pilipenko, Evgeny V.; Mazny, Jeffrey L.; Lynch, Michael; Drummond, D. Allan; McKinlay, James B.

In: Applied and Environmental Microbiology, Vol. 84, No. 14, e00404-18, 01.07.2018.

Research output: Contribution to journalArticle

McCully, AL, Behringer, MG, Gliessman, JR, Pilipenko, EV, Mazny, JL, Lynch, M, Drummond, DA & McKinlay, JB 2018, 'An Escherichia coli nitrogen starvation response is important for mutualistic coexistence with Rhodopseudomonas palustris', Applied and Environmental Microbiology, vol. 84, no. 14, e00404-18. https://doi.org/10.1128/AEM.00404-18
McCully, Alexandra L. ; Behringer, Megan G. ; Gliessman, Jennifer R. ; Pilipenko, Evgeny V. ; Mazny, Jeffrey L. ; Lynch, Michael ; Drummond, D. Allan ; McKinlay, James B. / An Escherichia coli nitrogen starvation response is important for mutualistic coexistence with Rhodopseudomonas palustris. In: Applied and Environmental Microbiology. 2018 ; Vol. 84, No. 14.
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