TY - JOUR
T1 - Noisy metabolism can promote microbial cross-feeding
AU - Lopez, Jaime G.
AU - Wingreen, Ned S.
N1 - Funding Information:
We thank Matt Black for useful discussions on possible experimental tests of the theory. JGL was supported by an NSF GRFP (DGE-1656466). This work was supported by the National Institutes of Health (R01 GM082938). This work was supported in part by the National Science Foundation, through the Center for the Physics of Biological Function (PHY-1734030).
Funding Information:
We thank Matt Black for useful discussions on possible experimental tests of the theory. JGL was supported by an NSF GRFP (DGE-1656466). This work was supported by the National Institutes of Health (R01 GM082938). This work was supported in part by the National Science Foundation, through the Center for the Physics of Biological Function (PHY-1734030). Funder Grant reference number Author National Science Foundation National Institutes of Health DGE-1656466 R01 GM082938 Jaime G Lopez Ned S Wingreen The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Publisher Copyright:
© Lopez and Wingreen.
PY - 2022/4
Y1 - 2022/4
N2 - Cross-feeding, the exchange of nutrients between organisms, is ubiquitous in microbial communities. Despite its importance in natural and engineered microbial systems, our understanding of how inter-species cross-feeding arises is incomplete, with existing theories limited to specific scenarios. Here, we introduce a novel theory for the emergence of such cross-feeding, which we term noise-averaging cooperation (NAC). NAC is based on the idea that, due to their small size, bacteria are prone to noisy regulation of metabolism which limits their growth rate. To compensate, related bacteria can share metabolites with each other to ‘average out’ noise and improve their collective growth. According to the Black Queen Hypothesis, this metabolite sharing among kin, a form of ‘leakage’, then allows for the evolution of metabolic interdependencies among species including de novo speciation via gene deletions. We first characterize NAC in a simple ecological model of cell metabolism, showing that metabolite leakage can in principle substantially increase growth rate in a community context. Next, we develop a generalized framework for estimating the potential benefits of NAC among real bacteria. Using single-cell protein abundance data, we predict that bacteria suffer from substantial noise-driven growth inefficiencies, and may therefore benefit from NAC. We then discuss potential evolutionary pathways for the emergence of NAC. Finally, we review existing evidence for NAC and outline potential experimental approaches to detect NAC in microbial communities.
AB - Cross-feeding, the exchange of nutrients between organisms, is ubiquitous in microbial communities. Despite its importance in natural and engineered microbial systems, our understanding of how inter-species cross-feeding arises is incomplete, with existing theories limited to specific scenarios. Here, we introduce a novel theory for the emergence of such cross-feeding, which we term noise-averaging cooperation (NAC). NAC is based on the idea that, due to their small size, bacteria are prone to noisy regulation of metabolism which limits their growth rate. To compensate, related bacteria can share metabolites with each other to ‘average out’ noise and improve their collective growth. According to the Black Queen Hypothesis, this metabolite sharing among kin, a form of ‘leakage’, then allows for the evolution of metabolic interdependencies among species including de novo speciation via gene deletions. We first characterize NAC in a simple ecological model of cell metabolism, showing that metabolite leakage can in principle substantially increase growth rate in a community context. Next, we develop a generalized framework for estimating the potential benefits of NAC among real bacteria. Using single-cell protein abundance data, we predict that bacteria suffer from substantial noise-driven growth inefficiencies, and may therefore benefit from NAC. We then discuss potential evolutionary pathways for the emergence of NAC. Finally, we review existing evidence for NAC and outline potential experimental approaches to detect NAC in microbial communities.
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U2 - 10.7554/eLife.70694
DO - 10.7554/eLife.70694
M3 - Article
C2 - 35380535
AN - SCOPUS:85128160809
SN - 2050-084X
VL - 11
JO - eLife
JF - eLife
M1 - e70694
ER -