Microbial cross-feeding is stabilized when a dependent mutant is segregated from its independent ancestor

Abstract

Microbial gene loss is hypothesized to be beneficial when gene function is costly, and the gene product can be replaced via cross-feeding from a neighbor. However, cross-fed metabolites are often only available at low concentrations, limiting the growth rates of gene-loss mutants that are dependent on those metabolites. Here we define conditions that support a loss of function mutant in a three-member bacterial community of: (i) N2-utilizing Rhodopseudomonas palustris as an NH4+ -excreting producer, (ii) N2-utilizing Vibrio natriegens as the ancestor, and (iii) a V. natriegens N2-utilizaton mutant that is dependent on the producer for NH4+. Using experimental and simulated cocultures, we found that the ancestor outcompeted the mutant due to low NH4+ availability under uniform conditions where both V. natriegens strains have equal access to nutrients. However, spatial structuring that separated the mutant from the ancestor, while maintaining access to NH4+ from the producer, allowed the mutant to avoid extinction. Counter to predictions, mutant enrichment under spatially structured conditions did not require a growth rate advantage from gene loss and the mutant coexisted with its ancestor. Thus, cross-feeding can originate from loss-of-function mutations that are otherwise detrimental, provided that the mutant can segregate from a competitive ancestor. Graphical abstract O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=118 SRC="FIGDIR/small/634601v1_ufig1.gif" ALT="Figure 1"> View larger version (25K): org.highwire.dtl.DTLVardef@1140808org.highwire.dtl.DTLVardef@1b72e8org.highwire.dtl.DTLVardef@14f70borg.highwire.dtl.DTLVardef@6707bb_HPS_FORMAT_FIGEXP M_FIG C_FIG