Institute of Microbiology and Dahlem Centre of Plant Sciences, Department of Biology, Chemistry, Pharmacy, Freie Universität Berlin, Berlin, Germany.
School of Biological Sciences, University of Canterbury, Christchurch, 8011, New Zealand.
ISME J. 2023 Sep;17(9):1445-1454. doi: 10.1038/s41396-023-01459-0. Epub 2023 Jun 24.
The phyllosphere is densely colonised by microbial communities, despite sparse and heterogeneously distributed resources. The limitation of resources is expected to drive bacterial competition resulting in exclusion or coexistence based on fitness differences and resource overlap between individual colonisers. We studied the impact of resource competition by determining the effects of different bacterial colonisers on the growth of the model epiphyte Pantoea eucalypti 299R (Pe299R). Resource overlap was predicted based on genome-scale metabolic modelling. By combining results of metabolic modelling and pairwise competitions in the Arabidopsis thaliana phyllosphere and in vitro, we found that ten resources sufficed to explain fitness of Pe299R. An effect of both resource overlap and phylogenetic relationships was found on competition outcomes in vitro as well as in the phyllosphere. However, effects of resource competition were much weaker in the phyllosphere when compared to in vitro experiments. When investigating growth dynamics and reproductive success at the single-cell resolution, resource overlap and phylogenetic relationships are only weakly correlated with epiphytic Pe299R reproductive success, indicating that the leaf's spatial heterogeneity mitigates resource competition. Although the correlation is weak, the presence of competitors led to the development of Pe299R subpopulations that experienced different life histories and cell divisions. In some in planta competitions, Pe299R benefitted from the presence of epiphytes despite high resource overlap to the competitor strain suggesting other factors having stronger effects than resource competition. This study provides fundamental insights into how bacterial communities are shaped in heterogeneous environments and a framework to predict competition outcomes.
叶片表面密集地定植着微生物群落，尽管资源稀少且分布不均。资源的限制预计会导致细菌竞争，从而根据个体定植者之间的适应性差异和资源重叠，导致排斥或共存。我们通过确定不同细菌定植者对模式生附生菌 Pantoea eucalypti 299R（Pe299R）生长的影响来研究资源竞争的影响。基于基因组规模的代谢建模来预测资源重叠。通过将代谢建模的结果与拟南芥叶片表面和体外的成对竞争相结合，我们发现十种资源足以解释 Pe299R 的适应性。在体外和叶片表面都发现了资源重叠和系统发育关系对竞争结果的影响。然而，与体外实验相比，叶片表面的资源竞争影响要弱得多。当以单细胞分辨率研究生长动态和生殖成功率时，资源重叠和系统发育关系与生附生 Pe299R 的生殖成功率仅呈弱相关，表明叶片的空间异质性减轻了资源竞争。尽管相关性较弱，但存在竞争者导致 Pe299R 亚群的形成，这些亚群经历了不同的生活史和细胞分裂。在一些体内竞争中，尽管与竞争者菌株的资源重叠很高，但 Pe299R 仍受益于竞争者的存在，这表明其他因素的影响比资源竞争更强。这项研究为了解细菌群落如何在异质环境中形成以及预测竞争结果提供了基本的见解。
