Putnam Emily E, May Robert, Freeman Nina, Arrigan Dillon, Boylan Andrew, Childs Laura H, Wolfe Benjamin E
Department of Biology, Tufts University, Medford, MA 20155, United States.
Department of Biology, Middlebury College, Middlebury, VT 05753, United States.
ISME J. 2025 Jan 2;19(1). doi: 10.1093/ismejo/wraf081.
Studies of microbial interactions often emphasize large, easily measurable growth differences and short-term ecological outcomes spanning just a few generations. However, more subtle interactions, such as those without obvious phenotypes, may play a significant role in shaping both the short-term ecological dynamics and the long-term evolutionary trajectories of microbial species. We used the cheese rind model microbiome to examine how two fungal species, Penicillium camemberti and Geotrichum candidum, impact global gene expression and genome evolution of the bacterium Pseudomonas carnis. Even though fungi had limited impacts on the growth of P. carnis, ~4-40% of its genome was differentially expressed, depending on the specific fungal partner. When we evolved this Pseudomonas strain alone or in co-culture with each of the fungi, we observed frequent mutations in global regulators of nitrogen regulation, secondary metabolite production, and motility, depending on the fungus. Strikingly, many strains with mutations in the nitrogen regulatory gene ntrB emerged when evolved alone or with G. candidum, but not with P. camemberti. Metabolomic and fitness experiments demonstrate that release of free amino acids by P. camemberti removes the fitness advantages conferred by ntrB mutations. Collectively, these results demonstrate that even in the absence of major short-term growth effects, fungi can have substantial impacts on the transcriptome and genomic evolution of bacterial species.
对微生物相互作用的研究通常强调显著的、易于测量的生长差异以及仅跨越几代的短期生态结果。然而，更微妙的相互作用，例如那些没有明显表型的相互作用，可能在塑造微生物物种的短期生态动态和长期进化轨迹方面发挥重要作用。我们使用奶酪外皮模型微生物群来研究两种真菌，即卡门青霉和白地霉，如何影响肉假单胞菌的全局基因表达和基因组进化。尽管真菌对肉假单胞菌的生长影响有限，但根据特定的真菌伙伴，其约4 - 40%的基因组存在差异表达。当我们单独培养或与每种真菌共培养这种假单胞菌菌株时，我们观察到，根据真菌的不同，氮调节、次生代谢产物产生和运动性的全局调节因子中频繁出现突变。引人注目的是，单独培养或与白地霉共培养时，许多氮调节基因ntrB发生突变的菌株出现了，但与卡门青霉共培养时则没有。代谢组学和适应性实验表明，卡门青霉释放游离氨基酸消除了ntrB突变赋予的适应性优势。总的来说，这些结果表明，即使在没有主要短期生长效应的情况下，真菌也会对细菌物种的转录组和基因组进化产生重大影响。
