Bacterial cross-feeding can promote gene retention by lowering gene expression costs

Gene loss is expected in microbial communities when the benefit of obtaining a biosynthetic precursor from a neighbor via cross-feeding outweighs the cost of retaining a biosynthetic gene. However, gene cost primarily comes from expression, and many biosynthetic genes are only expressed when needed. Thus, one can conversely expect cross-feeding to repress biosynthetic gene expression and promote gene retention by lowering gene cost. Here we examined long-term bacterial cocultures pairing Escherichia coli and Rhodopseudomonas palustris for evidence of gene loss or retention in response to cross-feeding of non-essential adenine. Although R. palustris continued to externalize adenine in long-term cultures, E. coli did not accumulate mutations in purine synthesis genes, even after 700 generations. E. coli purine synthesis gene expression was low in coculture, suggesting that gene repression removed selective pressure for gene loss. In support of this explanation, R. palustris also had low transcript levels for iron-scavenging siderophore genes in coculture, likely because E. coli facilitated iron acquisition by R. palustris. R. palustris siderophore gene mutations were correspondingly rare in long-term cocultures but were prevalent in monocultures where transcript levels were high. Our data suggests that cross-feeding does not always drive gene loss, but can instead promote gene retention by repressing costly expression.