Disentangling strictly self-serving mutations from win-win mutations in a mutualistic microbial community

Hart, Samuel F.M.; Pineda, Jose Mario Bello; Chen, Chi‐Chun; Green, Robin; Shou, Wenying

doi:10.1101/530287

Cited by 3 publications

(2 citation statements)

References 76 publications

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“…Additionally, there is a probable fitness cost for producers associated with increased nutrient excretion in well-mixed environments. Under well-mixed conditions, costless self-serving and mutually beneficial mutations, but not costly partner-serving mutations, are favored to evolve (34). Therefore mutations that improve a recipient’s ability to acquire key nutrients from producers, and thereby outcompete other recipient genotypes, can evolve rapidly (35).…”

Section: Discussionmentioning

confidence: 99%

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

Fritts

Bird

Behringer

et al. 2019

Preprint

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0Interactive microbial communities are ubiquitous on Earth. Within microbial 2 1 communities, nutrient exchange, also called cross-feeding, is widespread. Cross-2 2 feeding is thought to arise from the need to satisfy nutrient requirements of recipient 2 3 microbes, in many cases with producer microbes excreting costly, communally valuable 2 4 metabolites such as vitamins, amino acids, or ammonium. However, we possess an 2 5 incomplete understanding of the genetic basis and molecular mechanisms by which 2 6 cross-feeding of communally valuable metabolites evolves. Previously we engineered a 2 7 mutualistic cross-feeding relationship between N 2 -fixing Rhodopseudomonas palustris 2 8 and fermentative Escherichia coli. In this synthetic mutualism, genetically engineered R. 2 9palustris excretes essential nitrogen in the form of ammonium to E. coli, while E. coli 3 0 excretes essential carbon in the form of fermentation products to R. palustris. Here, we 3 1 used the same species, but with a wildtype strain of R. palustris not known to excrete 3 2 ammonium, to enrich for a nascent cross-feeding relationship. We found that emergent 3 3 ammonium cross-feeding relies not on a mutation in the producer R. palustris but rather 3 4 a single missense mutation in the recipient E. coli. This mutation in E. coli NtrC, the 3 5 master regulator of nitrogen scavenging, results in constitutive activation of an 3 6 ammonium transporter and likely allows E. coli to subsist on the small amount of 3 7 ammonium that leaks from WT R. palustris and reciprocate through the excretion of 3 8 organic acids. Overall, our results indicate that enhanced nutrient uptake by recipients, 3 9 rather than increased excretion by producers, is a plausible and possibly prevalent 4 0 mechanism by which cross-feeding interactions emerge. 4 1 4 2 3

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Section: Discussionmentioning

confidence: 99%

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

Fritts

Bird

Behringer

et al. 2019

Preprint

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“…Coculture evolution was described in an earlier study 12 . To revive a coculture, ~20 µL was scooped from the frozen sample using a sterile metal spatula, diluted ~10-fold into SD, and allowed to grow to moderate turbidity for 1-2 days.…”

Section: Evolutionmentioning

confidence: 99%

Metabolic excretion associated with nutrient-growth dysregulation promotes the rapid evolution of an overt metabolic defect

Green

Sonal

Wang

et al. 2018

Preprint

Self Cite

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In eukaryotes, conserved mechanisms ensure that cell growth is coordinated with nutrient availability. Overactive growth during nutrient limitation leads to rapid cell death. Here, we demonstrate that cells can adapt to this nutrient-growth imbalance by evolving major metabolic defects. Specifically, when yeast lysine auxotrophic mutant lyssuffered nutrient-growth imbalance in limited lysine, a sub-population repeatedly evolved to lose the ability to synthesize organosulfurs (lys -orgS -). Organosulfurs, mainly glutathione and glutathione conjugates, were released by lyscells during lysine limitation when nutrientgrowth is imbalanced, but not during glucose limitation when nutrient-growth is balanced. Limiting organosulfurs conferred a frequency-dependent fitness advantage to lys -orgSby eliciting a proper slow growth program including autophagy. Thus, nutrient-growth imbalance can trigger rapid niche construction, which in turn enables the selection of an overt metabolic defect to better tune cell growth to the metabolic environment.

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Pleiotropic win-win mutations can rapidly evolve in a nascent cooperative community despite unfavorable conditions

Hart

Chen

Shou

2020

Preprint

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Cooperation, paying a cost to benefit other individuals, is widespread. Cooperation can be promoted by pleiotropic “win-win” mutations which directly benefit self and partner. Previously, we showed that “partner-serving” should be defined as increased benefit supply rate per intake benefit (Hart & Pineda et al., 2019). Here, we report that “win-win” mutations can rapidly evolve even in nascent cooperation under conditions unfavorable for cooperation. Specifically, in a well-mixed environment we evolved engineered yeast cooperative communities where two strains exchanged costly metabolites lysine and hypoxanthine. Among cells that consumed lysine and released hypoxanthine, ecm21 mutations repeatedly arose. ecm21 is “self-serving”, improving self’s growth rate in limiting lysine. ecm21 is also “partner-serving”, increasing hypoxanthine release rate per lysine consumption and the steady state growth rate of partner. ecm21 also arose in monocultures evolving in lysine-limited chemostats. Thus, even without any pressure to maintain cooperation, pleiotropic win-win mutations may readily evolve.

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Disentangling strictly self-serving mutations from win-win mutations in a mutualistic microbial community

Cited by 3 publications

References 76 publications

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

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

Metabolic excretion associated with nutrient-growth dysregulation promotes the rapid evolution of an overt metabolic defect

Pleiotropic win-win mutations can rapidly evolve in a nascent cooperative community despite unfavorable conditions

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