Cross-feeding niches among commensal leaf bacteria are shaped by the interaction of strain-level diversity and resource availability

Abstract

Leaf microbiomes play crucial roles in plant health, making it important to understand the origins and functional relevance of their diversity. High strain-level leaf bacterial genetic diversity is known to be relevant for interactions with hosts, but little is known about its relevance for interactions with the multitude of diverse co-colonizing microorganisms. In leaves, nutrients like amino acids are major regulators of microbial growth and activity. Using metabolomics of leaf apoplast fluid, we found that different species of the plant genus Flaveria considerably differ in the concentrations of high-cost amino acids. We investigated how these differences affect bacterial community diversity and assembly by enriching leaf bacteria in vitro with only sucrose or sucrose + amino acids as possible carbon sources. Enrichments from F. robusta were dominated by Pantoea sp. and Pseudomonas sp., regardless of carbon source. The latter was unable to grow on sucrose alone but persisted in the sucrose-only enrichment thanks to exchange of diverse metabolites from Pantoea sp. Individual Pseudomonas strains in the enrichments had high genetic similarity but still displayed clear niche partitioning, enabling distinct strains to cross-feed in parallel. Pantoea strains were also closely related, but individuals enriched from F. trinervia fed Pseudomonas more poorly than those from F. robusta. This can be explained in part by the plant environment, since some cross-feeding interactions were selected for, when experimentally evolved in a poor (sucrose-only) environment but selected against in a rich (sucrose + amino acids) one. Together, our work shows that leaf bacterial diversity is functionally relevant in cross-feeding interactions and strongly suggests that the leaf resource environment can shape these interactions and thereby indirectly drive bacterial diversity.

Metabolic interaction models recapitulate leaf microbiota ecology

“…Leaf344) were also predicted to experience strongly positive outcomes in rare cases. These effects suggest a role of cross-fed amino or organic acids as valuable sources of metabolic complementation ( 65 ), which in addition to enabling highly versatile strains to outcompete a partner strain, can also facilitate the survival of specialized organisms.…”

Closely relatedBacteroidesof the murine intestinal microbiota affect each other’s growth positively or negatively

“…In comparison to in vitro conditions, the in vivo environment is not only more complex, but also subject to dynamic changes with potential effects on bacterial interactions. For example, host feeding could temporarily increase the nutrient content in the environment, which may reduce positive interactions mediated by cross-feeding (31, 32). Negative interactions may be more common in high-diversity communities, such as the in vivo environment, as a strain may be more likely to engage in negative interactions in the presence of other strains that potentially affect it adversely (33).…”

Metabolic resource overlap impacts on the competition of phyllosphere bacteria

“…Alternatively, these strains could engage in cooperative interactions such as cross-feeding, as observed between Pantoea spp. and Pseudomonas koreensis in the Flaveria robusta leaf apoplast [77]. However, further investigations are required to understand the mechanisms that result in beneficial interactions in the phyllosphere.…”