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Peer-reviewedCC BY 4.0Molecular Biology and Evolution

Unilateral cross-feeding constrains adaptive evolution, even in the producer without direct fitness effects

Abstract

Cross-feeding interactions are pervasive in microbial communities and profoundly shape community structure, stability, and function. While previous studies have explored how cross-feeding affects evolvability, this work has predominantly focused on bidirectional mutualistic interactions in engineered auxotrophic systems where both partners reciprocally exchange essential metabolites. However, most metabolic interactions in natural microbial communities are unidirectional, with organisms feeding on the metabolic waste products of other species. Our study addresses this gap by examining how a unidirectional cross-feeding interaction affects the evolutionary dynamics of both the producer (Acinetobacter johnsonii) and consumer (Pseudomonas putida) over 800 generations of experimental evolution. We found that co-culture constrained adaptive evolution in both species. Co-cultures exhibited lower πN/πS ratios (0.75 for P. putida; 1.04 for A. johnsonii) than monocultures (1.44 and 2.02, respectively), indicating stronger purifying selection against nonsynonymous mutations in the community context. Lineage tracking through whole genome sequencing of populations and clones revealed greater lineage diversity and complexity in monocultures, with more mutations showing significant parallelism across replicate populations. Additionally, P. putida evolved increased dependence on its partner; co-culture-evolved P. putida grew significantly worse than its ancestor when A. johnsonii was removed. These findings indicate that ecological interactions can reshape fitness landscapes and constrain adaptive evolution even when fitness benefits are unidirectional, with implications for understanding microbial community stability and predicting evolutionary dynamics in complex communities.

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BibTeX
@article{altameemi2026unilateral,
  title = {{Unilateral cross-feeding constrains adaptive evolution, even in the producer without direct fitness effects}},
  author = {Zahraa Al-Tameemi and Thibault Rosazza and Alejandra Rodríguez-Verdugo},
  journal = {Molecular Biology and Evolution},
  year = {2026},
  month = oct,
  doi = {10.1093/molbev/msag263},
  url = {https://doi.org/10.1093/molbev/msag263},
  note = {CC BY 4.0},
}
RIS
TY  - JOUR
TI  - Unilateral cross-feeding constrains adaptive evolution, even in the producer without direct fitness effects
AU  - Zahraa Al-Tameemi
AU  - Thibault Rosazza
AU  - Alejandra Rodríguez-Verdugo
PY  - 2026
DA  - 2026/10/21
JO  - Molecular Biology and Evolution
DO  - 10.1093/molbev/msag263
UR  - https://doi.org/10.1093/molbev/msag263
AB  - Cross-feeding interactions are pervasive in microbial communities and profoundly shape community structure, stability, and function. While previous studies have explored how cross-feeding affects evolvability, this work has predominantly focused on bidirectional mutualistic interactions in engineered auxotrophic systems where both partners reciprocally exchange essential metabolites. However, most metabolic interactions in natural microbial communities are unidirectional, with organisms feeding on the metabolic waste products of other species. Our study addresses this gap by examining how a unidirectional cross-feeding interaction affects the evolutionary dynamics of both the producer (Acinetobacter johnsonii) and consumer (Pseudomonas putida) over 800 generations of experimental evolution. We found that co-culture constrained adaptive evolution in both species. Co-cultures exhibited lower πN/πS ratios (0.75 for P. putida; 1.04 for A. johnsonii) than monocultures (1.44 and 2.02, respectively), indicating stronger purifying selection against nonsynonymous mutations in the community context. Lineage tracking through whole genome sequencing of populations and clones revealed greater lineage diversity and complexity in monocultures, with more mutations showing significant parallelism across replicate populations. Additionally, P. putida evolved increased dependence on its partner; co-culture-evolved P. putida grew significantly worse than its ancestor when A. johnsonii was removed. These findings indicate that ecological interactions can reshape fitness landscapes and constrain adaptive evolution even when fitness benefits are unidirectional, with implications for understanding microbial community stability and predicting evolutionary dynamics in complex communities.
SN  - 0737-4038
SN  - 1537-1719
ER  -