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

Abstract

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 fermentativeEscherichia coliand phototrophicRhodopseudomonas palustris. In this coculture,E. colianaerobically ferments sugars into excreted organic acids as a carbon source forR. palustris. In return, a genetically engineeredR. palustrisstrain constitutively converts N 2into NH 4 +, providingE. coliwith 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 withR. palustris,E. coligene expression changes resembled a nitrogen starvation response under the control of the transcriptional regulator NtrC. By genetically disruptingE. coliNtrC, we determined that a nitrogen starvation response is important for a stable coexistence, especially at lowR. palustrisNH 4 +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 importantmore » for survival within cooperative cross-feeding relationships. IMPORTANCEMutualistic cross-feeding between microbes within multispecies communities is widespread. Studying how mutualistic interactions influence the physiology of each species involved is important for understanding how mutualisms function and persist in both natural and applied settings. Using a bacterial mutualism consisting ofRhodopseudomonas palustrisandEscherichia coligrowing cooperatively through bidirectional nutrient exchange, we determined that anE. colinitrogen starvation response is important for maintaining a stable coexistence. The lack of anE. colinitrogen starvation response ultimately destabilized the mutualism and, in some cases, led to community collapse after serial transfers. Our findings thus inform on the potential necessity of an alternative physiological state for mutualistic coexistence with another species compared to the physiology of species grown in isolation.« less

Authors:
; ; ; ; ; ; ; ;
Publication Date:
Research Org.:
Indiana Univ., Bloomington, IN (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1541703
DOE Contract Number:  
SC0008131
Resource Type:
Journal Article
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:
Biotechnology & Applied Microbiology; Microbiology

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.
@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 = {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 fermentativeEscherichia coliand phototrophicRhodopseudomonas palustris. In this coculture,E. colianaerobically ferments sugars into excreted organic acids as a carbon source forR. palustris. In return, a genetically engineeredR. palustrisstrain constitutively converts N2into NH4+, providingE. coliwith 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 withR. palustris,E. coligene expression changes resembled a nitrogen starvation response under the control of the transcriptional regulator NtrC. By genetically disruptingE. coliNtrC, we determined that a nitrogen starvation response is important for a stable coexistence, especially at lowR. palustrisNH4+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. IMPORTANCEMutualistic cross-feeding between microbes within multispecies communities is widespread. Studying how mutualistic interactions influence the physiology of each species involved is important for understanding how mutualisms function and persist in both natural and applied settings. Using a bacterial mutualism consisting ofRhodopseudomonas palustrisandEscherichia coligrowing cooperatively through bidirectional nutrient exchange, we determined that anE. colinitrogen starvation response is important for maintaining a stable coexistence. The lack of anE. colinitrogen starvation response ultimately destabilized the mutualism and, in some cases, led to community collapse after serial transfers. Our findings thus inform on the potential necessity of an alternative physiological state for mutualistic coexistence with another species compared to the physiology of species grown in isolation.},
doi = {10.1128/aem.00404-18},
journal = {Applied and Environmental Microbiology},
issn = {0099-2240},
number = 14,
volume = 84,
place = {United States},
year = {2018},
month = {5}
}