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Title: Enhanced nutrient uptake is sufficient to drive emergent cross-feeding between bacteria in a synthetic community

Abstract

Abstract Interactive microbial communities are ubiquitous, influencing biogeochemical cycles and host health. One widespread interaction is nutrient exchange, or cross-feeding, wherein metabolites are transferred between microbes. Some cross-fed metabolites, such as vitamins, amino acids, and ammonium (NH4+), are communally valuable and impose a cost on the producer. The mechanisms that enforce cross-feeding of communally valuable metabolites are not fully understood. Previously we engineered a cross-feeding coculture between N2-fixing Rhodopseudomonas palustris and fermentative Escherichia coli. Engineered R. palustris excretes essential nitrogen as NH4+ to E. coli, while E. coli excretes essential carbon as fermentation products to R. palustris. Here, we sought to determine whether a reciprocal cross-feeding relationship would evolve spontaneously in cocultures with wild-type R. palustris, which is not known to excrete NH4+. Indeed, we observed the emergence of NH4+ cross-feeding, but driven by adaptation of E. coli alone. A missense mutation in E. coli NtrC, a regulator of nitrogen scavenging, resulted in constitutive activation of an NH4+ transporter. This activity likely allowed E. coli to subsist on the small amount of leaked NH4+ and better reciprocate through elevated excretion of fermentation products from a larger E. coli population. Our results indicate that enhanced nutrient uptake by recipients, rather thanmore » increased excretion by producers, is an underappreciated yet possibly prevalent mechanism by which cross-feeding can emerge.« less

Authors:
; ; ; ; ORCiD logo; ; ORCiD logo
Publication Date:
Sponsoring Org.:
USDOE
OSTI Identifier:
2281251
Resource Type:
Published Article
Journal Name:
The ISME Journal
Additional Journal Information:
Journal Name: The ISME Journal Journal Volume: 14 Journal Issue: 11; Journal ID: ISSN 1751-7362
Publisher:
Oxford University Press
Country of Publication:
United Kingdom
Language:
English

Citation Formats

Fritts, Ryan K., Bird, Jordan T., Behringer, Megan G., Lipzen, Anna, Martin, Joel, Lynch, Michael, and McKinlay, James B. Enhanced nutrient uptake is sufficient to drive emergent cross-feeding between bacteria in a synthetic community. United Kingdom: N. p., 2020. Web. doi:10.1038/s41396-020-00737-5.
Fritts, Ryan K., Bird, Jordan T., Behringer, Megan G., Lipzen, Anna, Martin, Joel, Lynch, Michael, & McKinlay, James B. Enhanced nutrient uptake is sufficient to drive emergent cross-feeding between bacteria in a synthetic community. United Kingdom. https://doi.org/10.1038/s41396-020-00737-5
Fritts, Ryan K., Bird, Jordan T., Behringer, Megan G., Lipzen, Anna, Martin, Joel, Lynch, Michael, and McKinlay, James B. Wed . "Enhanced nutrient uptake is sufficient to drive emergent cross-feeding between bacteria in a synthetic community". United Kingdom. https://doi.org/10.1038/s41396-020-00737-5.
@article{osti_2281251,
title = {Enhanced nutrient uptake is sufficient to drive emergent cross-feeding between bacteria in a synthetic community},
author = {Fritts, Ryan K. and Bird, Jordan T. and Behringer, Megan G. and Lipzen, Anna and Martin, Joel and Lynch, Michael and McKinlay, James B.},
abstractNote = {Abstract Interactive microbial communities are ubiquitous, influencing biogeochemical cycles and host health. One widespread interaction is nutrient exchange, or cross-feeding, wherein metabolites are transferred between microbes. Some cross-fed metabolites, such as vitamins, amino acids, and ammonium (NH4+), are communally valuable and impose a cost on the producer. The mechanisms that enforce cross-feeding of communally valuable metabolites are not fully understood. Previously we engineered a cross-feeding coculture between N2-fixing Rhodopseudomonas palustris and fermentative Escherichia coli. Engineered R. palustris excretes essential nitrogen as NH4+ to E. coli, while E. coli excretes essential carbon as fermentation products to R. palustris. Here, we sought to determine whether a reciprocal cross-feeding relationship would evolve spontaneously in cocultures with wild-type R. palustris, which is not known to excrete NH4+. Indeed, we observed the emergence of NH4+ cross-feeding, but driven by adaptation of E. coli alone. A missense mutation in E. coli NtrC, a regulator of nitrogen scavenging, resulted in constitutive activation of an NH4+ transporter. This activity likely allowed E. coli to subsist on the small amount of leaked NH4+ and better reciprocate through elevated excretion of fermentation products from a larger E. coli population. Our results indicate that enhanced nutrient uptake by recipients, rather than increased excretion by producers, is an underappreciated yet possibly prevalent mechanism by which cross-feeding can emerge.},
doi = {10.1038/s41396-020-00737-5},
journal = {The ISME Journal},
number = 11,
volume = 14,
place = {United Kingdom},
year = {Wed Aug 12 00:00:00 EDT 2020},
month = {Wed Aug 12 00:00:00 EDT 2020}
}

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