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

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 N 2 into NH 4 +, 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 NH 4 + excretion levels. Destabilization of the nitrogen starvation regulatory network resultedmore » 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.« less

Authors:
 [1];  [2];  [1];  [3];  [1];  [2];  [3];  [1];  [4]
  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)
Publication Date:
Research Org.:
Indiana Univ., Bloomington, IN (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1541703
Grant/Contract Number:  
SC0008131
Resource Type:
Accepted Manuscript
Journal Name:
Applied and Environmental Microbiology
Additional Journal Information:
Journal Volume: 84; Journal Issue: 14; Journal ID: ISSN 0099-2240
Publisher:
American Society for Microbiology
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; biotechnology & applied microbiology; microbiology; Escherichia coli; NtrC; Rhodopseudomonas; coculture; cross-feeding; fermentation; mutualism; nitrogen fixation; nitrogen starvation; photoheterotrophy

Citation Formats

McCully, Alexandra L., Behringer, Megan G., Gliessman, Jennifer R., Pilipenko, Evgeny V., Mazny, Jeffrey L., Lynch, Michael, Drummond, D. Allan, McKinlay, James B., and Atomi, Haruyuki. An Escherichia coli Nitrogen Starvation Response Is Important for Mutualistic Coexistence with Rhodopseudomonas palustris. United States: N. p., 2018. Web. doi: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., & Atomi, Haruyuki. An Escherichia coli Nitrogen Starvation Response Is Important for Mutualistic Coexistence with Rhodopseudomonas palustris. United States. doi: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., and Atomi, Haruyuki. Fri . "An Escherichia coli Nitrogen Starvation Response Is Important for Mutualistic Coexistence with Rhodopseudomonas palustris". United States. doi:10.1128/aem.00404-18. https://www.osti.gov/servlets/purl/1541703.
@article{osti_1541703,
title = {An Escherichia coli Nitrogen Starvation Response Is Important for Mutualistic Coexistence with Rhodopseudomonas palustris},
author = {McCully, Alexandra L. and Behringer, Megan G. and Gliessman, Jennifer R. and Pilipenko, Evgeny V. and Mazny, Jeffrey L. and Lynch, Michael and Drummond, D. Allan and McKinlay, James B. and Atomi, Haruyuki},
abstractNote = {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.},
doi = {10.1128/aem.00404-18},
journal = {Applied and Environmental Microbiology},
number = 14,
volume = 84,
place = {United States},
year = {2018},
month = {5}
}

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