Bisesi Ave T, Carlson Ross P, Cotner Lachlan, Harcombe William R
Department of Ecology, Evolution and Behavior, University of Minnesota, St. Paul, Minnesota, USA.
Department of Chemical and Biological Engineering, Montana State University, Bozeman, Montana, USA.
mSystems. 2025 Aug 15:e0014425. doi: 10.1128/msystems.00144-25.
Mobile genetic elements (MGEs) are ubiquitous in prokaryotes and exert significant influence on microbial communities, in part through their effects on host metabolism. While some MGEs directly alter host metabolism by introducing novel enzymes, all MGEs can indirectly change bacterial metabolism by redirecting intracellular host resources away from native bacterial processes toward MGE production. As a result, even when MGEs do not provide new metabolic functions, their carriage can influence host traits such as growth rate, nutrient uptake, and waste excretion, with consequences for how bacteria contribute to community and ecosystem functions. However, there are few empirical tests of how the indirect metabolic consequences of MGE carriage shape interactions between host and non-host bacterial species. We integrated genome-scale metabolic modeling with an obligate cross-feeding system to investigate the metabolic consequences of two MGEs in : the conjugative plasmid F128 and the filamentous phage M13. We examined the impact of these MGEs on interactions between bacteria in a multispecies cross-feeding community composed of , and . Both modeling and experiments suggested that MGE carriage can change the growth rate and excretion profile of . We also found that indirect changes to host metabolism induced by our MGEs increased the density of cross-feeding species. Our work emphasizes that microbes carrying MGEs can have different metabolisms than MGE-free cells, even when MGEs do not encode metabolic enzymes, and demonstrates that these metabolic shifts can have significant consequences for microbial community structure and function.IMPORTANCEMobile genetic elements (MGEs) often shape the structure and function of microbial communities by influencing the metabolism of bacterial cells. Though some MGEs change metabolism directly by transferring genetic material that provides access to novel niche space, all MGEs should alter host metabolism indirectly to some degree by shifting intracellular metabolic processes toward MGE replication. This study uses a combination of flux balance analysis and an system consisting of , , , and two MGEs in to investigate how MGEs change the community contributions of their hosts via metabolic conflict alone. Flux balance analysis suggests that MGEs can change intracellular demand for different metabolic processes, leading to shifts in the identities and concentrations of compounds that hosts externalize into the environment. This finding is supported by experimental results and extends our understanding of how MGEs shape the structure and function of microbial communities.
移动遗传元件（MGEs）在原核生物中普遍存在，并对微生物群落产生重大影响，部分原因是它们对宿主代谢的影响。虽然一些MGEs通过引入新酶直接改变宿主代谢，但所有MGEs都可以通过将细胞内宿主资源从原生细菌过程转移到MGE生产上，间接改变细菌代谢。因此，即使MGEs不提供新的代谢功能，它们的携带也会影响宿主特征，如生长速率、养分吸收和废物排泄，进而影响细菌对群落和生态系统功能的贡献方式。然而，关于MGE携带的间接代谢后果如何塑造宿主与非宿主细菌物种之间相互作用的实证研究很少。我们将基因组规模的代谢建模与专性交叉喂养系统相结合，以研究两种MGEs在大肠杆菌中的代谢后果：接合质粒F128和丝状噬菌体M13。我们研究了这些MGEs对由大肠杆菌、粪肠球菌和嗜麦芽窄食单胞菌组成的多物种交叉喂养群落中细菌间相互作用的影响。建模和实验均表明，MGE携带可改变大肠杆菌的生长速率和排泄谱。我们还发现，我们的MGEs诱导的宿主代谢间接变化增加了交叉喂养物种的密度。我们的工作强调，携带MGEs的微生物可能具有与无MGE细胞不同的代谢，即使MGEs不编码代谢酶，并证明这些代谢变化可能对微生物群落结构和功能产生重大影响。
重要性
移动遗传元件（MGEs）通常通过影响细菌细胞的代谢来塑造微生物群落的结构和功能。虽然一些MGEs通过转移提供进入新生态位空间途径的遗传物质直接改变代谢，但所有MGEs都应通过将细胞内代谢过程转向MGE复制，在一定程度上间接改变宿主代谢。本研究结合通量平衡分析和一个由大肠杆菌、粪肠球菌、嗜麦芽窄食单胞菌和两种MGEs组成的系统，以研究MGEs如何仅通过代谢冲突改变其宿主对群落的贡献。通量平衡分析表明，MGEs可改变细胞内对不同代谢过程的需求，导致宿主释放到环境中的化合物的种类和浓度发生变化。这一发现得到了实验结果的支持，并扩展了我们对MGEs如何塑造微生物群落结构和功能的理解。
