Johnke J, Zimmermann J, Stegemann T, Langel D, Franke A, Thingholm L, Schulenburg H
Zoological Institute, Kiel University, Kiel, Germany.
Max Planck Institute for Evolutionary Biology, Ploen, Germany.
mSystems. 2025 Feb 18;10(2):e0153324. doi: 10.1128/msystems.01533-24. Epub 2025 Jan 10.
The microbiomes of host organisms and their direct source environments are closely linked and key for shaping microbial community dynamics. The relationship between these linked dynamics is largely unexplored because source substrates are usually unavailable. To address this current knowledge gap, we employed bacteriovorous nematodes as a unique model system, for which source substrates like rotting apples can be easily collected. We compared single host microbiomes with their corresponding apple source substrates, as well as nematode-free substrates, over a 2-year sampling period in the botanical garden in Kiel, Germany. We found that single worms have unique microbiomes, which overlap most strongly with nematodes from the same source apple. A comparison to previous, related work revealed that variation in microbiome composition of natural isolates is significantly influenced by the substrate type, from which worms were obtained (e.g., fruits or compost). Our current sampling further showed that microbiome assembly is mostly driven by dispersal limitation. Importantly, two independent analysis approaches consistently suggest that worm microbiomes significantly influence characteristics of the apple microbiomes, possibly indicating niche construction by nematodes. Moreover, combining apple microbiome and metabolome data, we identified individual microbes and specific compounds indicative of fruit ripening that are significantly associated with nematode presence. In conclusion, our study elucidates the complex relationship between host microbiomes and their directly connected substrate microbiomes. Our analyses underscore the significant influence of nematode microbiomes on shaping the apple microbiome and, consequently, the fruit's metabolic capacity, thereby enhancing our general understanding of host-microbiome interactions in their natural habitat.IMPORTANCEAlmost all complex organisms are host to a microbial community, the microbiome. This microbiome can influence diverse host functions, such as food processing, protection against parasites, or development. The relationship between host and microbiome critically depends on the assembly of the microbial community, which may be shaped by microbes in the directly linked environment, the source microbiome. This assembly process is often not well understood because of the unavailability of source substrates. Here, we used nematodes as a model system that facilitates a direct comparison of host and source microbiomes. Based on a 2-year sampling period, we identified (i) a clear link between assembly dynamics of host and source microbiomes, (ii) a significant influence of nematode microbiomes on apple microbiomes, and (iii) specific microbes and compounds that are associated with the presence of nematodes in the sampled substrates. Overall, our study enhances our understanding of microbiome assembly dynamics and resulting functions.
宿主生物的微生物群与其直接来源环境紧密相连，是塑造微生物群落动态的关键因素。由于通常无法获取来源底物，这些相互关联的动态之间的关系在很大程度上尚未得到探索。为了解决这一当前的知识空白，我们采用食细菌线虫作为独特的模型系统，对于该系统，可以轻松收集到诸如腐烂苹果等来源底物。在德国基尔植物园进行的为期两年的采样期内，我们将单个宿主的微生物群与其相应的苹果来源底物以及无菌虫底物进行了比较。我们发现单个线虫具有独特的微生物群，与来自同一来源苹果的线虫的微生物群重叠最为强烈。与之前的相关工作进行比较发现，天然分离株微生物群组成的变化受到获取线虫的底物类型（例如水果或堆肥）的显著影响。我们当前的采样进一步表明，微生物群的组装主要受扩散限制驱动。重要的是，两种独立的分析方法一致表明，线虫微生物群显著影响苹果微生物群的特征，这可能表明线虫进行了生态位构建。此外，结合苹果微生物群和代谢组数据，我们鉴定出了与线虫存在显著相关的、指示果实成熟的单个微生物和特定化合物。总之，我们的研究阐明了宿主微生物群与其直接相连的底物微生物群之间的复杂关系。我们的分析强调了线虫微生物群对塑造苹果微生物群以及进而对果实代谢能力的重大影响，从而增进了我们对其自然栖息地中宿主 - 微生物群相互作用的总体理解。
重要性
几乎所有复杂生物都寄生于一个微生物群落，即微生物群。这个微生物群可以影响多种宿主功能，如食物加工、抵御寄生虫或发育。宿主与微生物群之间的关系关键取决于微生物群落的组装，而这可能受到直接相连环境中的微生物，即来源微生物群的影响。由于无法获取来源底物，这个组装过程往往未被充分理解。在这里，我们使用线虫作为一个便于直接比较宿主和来源微生物群的模型系统。基于为期两年的采样期，我们确定了：（i）宿主和来源微生物群组装动态之间的明确联系；（ii）线虫微生物群对苹果微生物群的显著影响；以及（iii）与采样底物中线虫存在相关的特定微生物和化合物。总体而言，我们的研究增进了我们对微生物群组装动态及其产生的功能的理解。
