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Abstract Diverse ecosystems host microbial relationships that are stabilized by nutrient cross-feeding. Cross-feeding can involve metabolites that should hold value for the producer. Externalization of such communally valuable metabolites is often unexpected and difficult to predict. Previously, we discovered purine externalization by Rhodopseudomonas palustris by its ability to rescue an Escherichia coli purine auxotroph. Here we found that an E. coli purine auxotroph can stably coexist with R. palustris due to purine cross-feeding. We identified the cross-fed purine as adenine. Adenine was externalized by R. palustris under diverse growth conditions. Computational modeling suggested that adenine externalization occurs via diffusion across the cytoplasmic membrane. RNAseq analysis led us to hypothesize that adenine accumulation and externalization stem from a salvage pathway bottleneck at the enzyme encoded by apt. Ectopic expression of apt eliminated adenine externalization, supporting our hypothesis. A comparison of 49 R. palustris strains suggested that purine externalization is relatively common, with 16 strains exhibiting the trait. Purine externalization was correlated with the genomic orientation of apt, but apt orientation alone could not always explain purine externalization. Our results provide a mechanistic understanding of how a communally valuable metabolite can participate in cross-feeding. Our findings also highlight the challenge in identifying genetic signatures for metabolite externalization.
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Are Bacteria Leaky? Mechanisms of Metabolite Externalization in Bacterial Cross-Feeding
The metabolism of a bacterial cell stretches beyond its boundaries, often connecting with the metabolism of other cells to form extended metabolic networks that stretch across communities, and even the globe. Among the least intuitive metabolic connections are those involving cross-feeding of canonically intracellular metabolites. How and why are these intracellular metabolites externalized? Are bacteria simply leaky? Here I consider what it means for a bacterium to be leaky, and I review mechanisms of metabolite externalization from the context of cross-feeding. Despite common claims, diffusion of most intracellular metabolites across a membrane is unlikely. Instead, passive and active transporters are likely involved, possibly purging excess metabolites as part of homeostasis. Re-acquisition of metabolites by a producer limits the opportunities for cross-feeding. However, a competitive recipient can stimulate metabolite externalization and initiate a positive-feedback loop of reciprocal cross-feeding.
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- Award ID(s):
- 1749489
- PAR ID:
- 10476496
- Publisher / Repository:
- Annual Reviews
- Date Published:
- Journal Name:
- Annual Review of Microbiology
- Volume:
- 77
- Issue:
- 1
- ISSN:
- 0066-4227
- Page Range / eLocation ID:
- 277 to 297
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Diverse ecosystems host microbial relationships that are stabilized by nutrient cross-feeding. Cross-feeding can involve metabolites that should hold value for the producer. Externalization of such communally valuable metabolites is often unexpected and difficult to predict. Previously, we fortuitously discovered purine externalization by Rhodopseudomonas palustris by its ability to rescue growth of an Escherichia coli purine auxotroph. Here we found that an E. coli purine auxotroph can stably coexist with R. palustris due to purine cross-feeding. We identified the cross-fed purine as adenine. Adenine was externalized by R. palustris under diverse growth conditions. Computational models suggested that adenine externalization occurs via passive diffusion across the cytoplasmic membrane. RNAseq analysis led us to hypothesize that accumulation and externalization of adenine stems from an adenine salvage bottleneck at the enzyme encoded by apt. Ectopic expression of apt eliminated adenine externalization, supporting our hypothesis. A comparison of 49 R. palustris strains suggested that purine externalization is relatively common, with 15 of the strains exhibiting the trait. Purine externalization was correlated with the genomic orientation of apt orientation, but apt orientation alone could not explain adenine externalization in some strains. Our results provide a mechanistic understanding of how a communally valuable metabolite can participate in cross-feeding. Our findings also highlight the challenge in identifying genetic signatures for metabolite externalization.more » « less
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- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1146/annurev-micro-032521-023815
