Murphy Robert M, Sinotte Veronica M, Cuesta-Maté Ana, Renelies-Hamilton Justinn, Lenz-Strube Mikael, Poulsen Michael
Section for Ecology and Evolution, Department of Biology, University of Copenhagen, Copenhagen East, Denmark.
Center for Evolutionary Hologenomics, Globe Institute, University of Copenhagen, Copenhagen K, Denmark.
Anim Microbiome. 2024 Aug 6;6(1):44. doi: 10.1186/s42523-024-00332-5.
Microbiome assembly critically impacts the ability of hosts to access beneficial symbiont functions. Fungus-farming termites have co-evolved with a fungal cultivar as a primary food source and complex gut microbiomes, which collectively perform complementary degradation of plant biomass. A large subset of the bacterial community residing within termite guts are inherited (vertically transmitted) from parental colonies, while the fungal symbiont is, in most termite species, acquired from the environment (horizontally transmitted). It has remained unknown how the gut microbiota sustains incipient colonies prior to the acquisition of the fungal cultivar, and how, if at all, bacterial contributions are modulated by fungus garden establishment. Here, we test the latter by determining the composition and predicted functions of the gut microbiome using metabarcoding and shotgun metagenomics, respectively. We focus our functional predictions on bacterial carbohydrate-active enzyme and nitrogen cycling genes and verify compositional patterns of the former through enzyme activity assays. Our findings reveal that the vast majority of microbial functions are encoded in the inherited microbiome, and that the establishment of fungal gardens incurs only minor modulations of predicted bacterial capacities for carbohydrate and nitrogen metabolism. While we cannot rule out that other symbiont functions are gained post-fungus garden establishment, our findings suggest that fungus-farming termite hosts are equipped with a near-complete set of gut microbiome functions at the earliest stages of colony life. This inherited, incipient bacterial microbiome likely contributes to the high extent of functional specificity and coevolution observed between termite hosts, gut microbiomes, and the fungal cultivar.
微生物群落组装对宿主获取有益共生体功能的能力具有至关重要的影响。以真菌为食的白蚁与一种真菌品种共同进化，该真菌品种是其主要食物来源，同时它们还拥有复杂的肠道微生物群落，这些微生物共同对植物生物质进行互补性降解。白蚁肠道内的大部分细菌群落是从亲代蚁群遗传而来（垂直传播），而在大多数白蚁物种中，真菌共生体是从环境中获取的（水平传播）。在获取真菌品种之前，肠道微生物群如何维持初期蚁群，以及真菌菌圃的建立是否以及如何调节细菌的贡献，这些问题一直未明。在此，我们分别通过元条形码技术和鸟枪法宏基因组学来确定肠道微生物群落的组成和预测功能，以检验后者。我们将功能预测聚焦于细菌碳水化合物活性酶和氮循环基因，并通过酶活性测定来验证前者的组成模式。我们的研究结果表明，绝大多数微生物功能由遗传的微生物群落编码，并且真菌菌圃的建立只会对预测的细菌碳水化合物和氮代谢能力产生轻微调节。虽然我们不能排除在真菌菌圃建立后获得其他共生体功能的可能性，但我们的研究结果表明，以真菌为食的白蚁宿主在蚁群生活的最早阶段就配备了一套近乎完整的肠道微生物群落功能。这种遗传的初期细菌微生物群落可能有助于解释在白蚁宿主、肠道微生物群落和真菌品种之间观察到的高度功能特异性和共同进化现象。
