A purine salvage bottleneck leads to bacterial adenine cross-feeding

Abstract

AbstractDiverse 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 byRhodopseudomonas palustrisby its ability to rescue growth of anEscherichia colipurine auxotroph. Here we found that anE. colipurine auxotroph can stably coexist withR. palustrisdue to purine cross-feeding. We identified the cross-fed purine as adenine. Adenine was externalized byR. palustrisunder 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 byapt. Ectopic expression ofapteliminated adenine externalization, supporting our hypothesis. A comparison of 49R. palustrisstrains suggested that purine externalization is relatively common, with 15 of the strains exhibiting the trait. Purine externalization was correlated with the genomic orientation ofaptorientation, butaptorientation 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.