Dynamic character displacement among a pair of bacterial phyllosphere commensals in situ

Abstract

Differences between species promote stable coexistence in a resource-limited environment. These differences can result from interspecies competition leading to character shifts, a process referred to as character displacement. While character displacement is often interpreted as a consequence of genetically fixed trait differences between species, it can also be mediated by phenotypic plasticity in response to the presence of another species. Here, we test whether phenotypic plasticity leads to a shift in proteome allocation during co-occurrence of two bacterial species from the abundant, leaf-colonizing families Sphingomonadaceae and Rhizobiaceae in their natural habitat. Upon mono-colonizing of the phyllosphere, both species exhibit specific and shared protein functions indicating a niche overlap. During co-colonization, quantitative differences in the protein repertoire of both bacterial populations occur as a result of bacterial coexistence in planta. Specifically, the Sphingomonas strain produces enzymes for the metabolization of xylan, while the Rhizobium strain reprograms its metabolism to beta-oxidation of fatty acids fueled via the glyoxylate cycle and adapts its biotin acquisition. We demonstrate the conditional relevance of cross-species facilitation by mutagenesis leading to loss of fitness in competition in planta. Our results show that dynamic character displacement and niche facilitation mediated by phenotypic plasticity can contribute to species coexistence.

Metabolic interaction models recapitulate leaf microbiota ecology

“…Our metabolic modeling predicted interaction outcomes on the basis of carbon sourceutilization capabilities. Further curation that integrates additional properties such as vitamin auxotrophies and storage (66), as well as metabolic shifts occurring from gene regulation (67,68), is likely to improve the quantitative predictive power of this framework (33,69). Moreover, although our predictions based on metabolic mechanisms are informative of key aspects underlying the assembly of plantassociated microbiomes, they do not consider additional factors that are known to shape leaf communities, such as signaling molecules, antagonistic interactions, or host immunity (5,(70)(71)(72)(73).…”

Simultaneous tracking of near-isogenic bacterial strains in syntheticArabidopsismicrobiota by chromosomally-integrated barcodes

“…Only a small number of genetic determinants in bacterial commensals influencing microbe-microbe and microbe-host interactions during plant microbiota establishment have thus far been identified (Getzke et al, 2023;Hemmerle et al, 2022;Liu et al, 2022). Bacterial DNA barcoding was applied to investigate antagonistic interactions of Pseudomonads leaf strains co-occurring on Arabidopsis (Shalev et al, 2022).…”

“…Establishment of the plant microbiota is dependent on microbe-microbe and microbehost interactions. Numerous factors influence the composition of these plantassociated microbial assemblages: edaphic factors such as soil pH or soil-derived nutrients (Castrillo et al, 2017;Harbort et al, 2020), microbial competition or cooperation for plant-derived carbohydrates (Berendsen et al, 2018;Hemmerle et al, 2022), specialized plant-or microbe-derived exometabolites (Getzke et al, 2023;Hu et al, 2018;Huang et al, 2019;Voges et al, 2019), including antimicrobials, or pathogen effectors released by co-colonizing phytopathogens (Snelders et al, 2021;Snelders et al, 2020).…”

The role of plasticity and stochasticity in coexistence

“…The role of phenotypic plasticity in altering the competition dynamics in plants (Pérez‐Ramos et al., 2019; Schwinning & Weiner, 1998), particularly when species invade a new habitat, has been of great interest (Davidson et al., 2011). At the microbial level, phenotypic plasticity—measured via proteome changes—was shown to decrease niche overlap between Rhizobium Leaf68 and Sphingomonas Leaf257 during co‐coloniziation of Arabidopsis thaliana , thus enabling their coexistence (Hemmerle et al., 2022). In contrast, the role of phenotypic plasticity in species coexistence in animal systems is little understood.…”