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Cross-feeding niches among commensal leaf bacteria are shaped by the interaction of strain-level diversity and resource availability
The ISME Journal ( IF 10.8 ) Pub Date : 2022-06-29 , DOI: 10.1038/s41396-022-01271-2
Mariana Murillo-Roos 1 , Hafiz Syed M Abdullah 1 , Mossaab Debbar 1 , Nico Ueberschaar 2 , Matthew T Agler 1
Affiliation  

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.



中文翻译:


共生叶细菌之间的交叉喂养生态位是由菌株水平多样性和资源可用性的相互作用形成的



叶子微生物组在植物健康中发挥着至关重要的作用,因此了解其多样性的起源和功能相关性非常重要。已知高菌株水平的叶细菌遗传多样性与宿主的相互作用有关,但对其与多种不同的共定殖微生物相互作用的相关性知之甚少。在叶子中,氨基酸等营养物质是微生物生长和活动的主要调节剂。利用叶质外体液的代谢组学,我们发现黄花属植物的不同物种在高成本氨基酸的浓度方面存在显着差异。我们通过仅用蔗糖或蔗糖+氨基酸作为可能的碳源在体外富集叶细菌,研究了这些差异如何影响细菌群落多样性和组装。 F.Robista的富集主要是Pantoea sp。和假单胞菌属,无论碳源如何。后者无法仅靠蔗糖生长,但由于来自菌属物种的多种代谢物的交换而坚持仅蔗糖富集。富集中的各个假单胞菌菌株具有高度的遗传相似性,但仍然表现出清晰的生态位划分,使得不同的菌株能够平行交叉饲养。泛菌菌株也密切相关,但来自F.trinervia的个体对假单胞菌的喂养效果比来自F.robusta的个体要差。这可以部分地用植物环境来解释,因为当在贫乏的(仅蔗糖)环境中进行实验进化时,选择了一些交叉取食相互作用,但在富含蔗糖+氨基酸的环境中进行了选择。 总之,我们的工作表明,叶子细菌多样性在交叉喂养相互作用中具有功能相关性,并强烈表明叶子资源环境可以塑造这些相互作用,从而间接驱动细菌多样性。

更新日期:2022-06-30
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