Department of Evolutionary Ecology and Genetics, Kiel University, Kiel, Germany.
Institute of Ecology and Evolution, University of Oregon, Eugene, OR, USA.
ISME J. 2023 Nov;17(11):1953-1965. doi: 10.1038/s41396-023-01507-9. Epub 2023 Sep 6.
Most animals and plants have associated microorganisms, collectively referred to as their microbiomes, which can provide essential functions. Given their importance, host-associated microbiomes have the potential to contribute substantially to adaptation of the host-microbiome assemblage (the "metaorganism"). Microbiomes may be especially important for rapid adaptation to novel environments because microbiomes can change more rapidly than host genomes. However, it is not well understood how hosts and microbiomes jointly contribute to metaorganism adaptation. We developed a model system with which to disentangle the contributions of hosts and microbiomes to metaorganism adaptation. We established replicate mesocosms containing the nematode Caenorhabditis elegans co-cultured with microorganisms in a novel complex environment (laboratory compost). After approximately 30 nematode generations (100 days), we harvested worm populations and associated microbiomes, and subjected them to a common garden experiment designed to unravel the impacts of microbiome composition and host genetics on metaorganism adaptation. We observed that adaptation took different trajectories in different mesocosm lines, with some increasing in fitness and others decreasing, and that interactions between host and microbiome played an important role in these contrasting evolutionary paths. We chose two exemplary mesocosms (one with a fitness increase and one with a decrease) for detailed study. For each example, we identified specific changes in both microbiome composition (for both bacteria and fungi) and nematode gene expression associated with each change in fitness. Our study provides experimental evidence that adaptation to a novel environment can be jointly influenced by host and microbiome.
大多数动植物都有与其相关的微生物，这些微生物统称为它们的微生物组，它们可以提供重要的功能。鉴于其重要性，宿主相关的微生物组有可能对宿主-微生物组组合（“元生物体”）的适应做出重大贡献。微生物组对于快速适应新环境可能尤为重要，因为微生物组的变化速度比宿主基因组更快。然而，宿主和微生物组如何共同促进元生物体的适应还不太清楚。我们开发了一个模型系统，可以将宿主和微生物组对元生物体适应的贡献分开。我们建立了复制的中观系统，其中包含秀丽隐杆线虫（Caenorhabditis elegans）与微生物在新的复杂环境（实验室堆肥）中共培养。大约 30 代线虫（100 天）后，我们收获了线虫种群和相关的微生物组，并将它们置于一个共同的花园实验中，该实验旨在揭示微生物组组成和宿主遗传对元生物体适应的影响。我们观察到适应在不同的中观系统线中采取了不同的轨迹，有些适应度增加，有些适应度降低，宿主和微生物组之间的相互作用在这些相反的进化路径中起着重要作用。我们选择了两个具有代表性的中观系统（一个适应度增加，一个适应度降低）进行详细研究。对于每个例子，我们确定了微生物组组成（细菌和真菌）和线虫基因表达的具体变化，这些变化与适应度的每个变化相关。我们的研究提供了实验证据，表明对新环境的适应可以同时受到宿主和微生物组的影响。
