Department of Botany and Plant Pathology, Oregon State University, Corvallis, OR 97331, USA.
Curr Biol. 2020 Aug 17;30(16):3260-3266.e5. doi: 10.1016/j.cub.2020.06.011. Epub 2020 Jul 16.
The composition of host-associated microbiomes can have important consequences for host health and fitness [1-3]. Yet we still lack understanding of many fundamental processes that determine microbiome composition [4, 5]. There is mounting evidence that historical contingency during microbiome assembly may overshadow more deterministic processes, such as the selective filters imposed by host traits [6-8]. More specifically, species arrival order has been frequently shown to affect microbiome composition [9-12], a phenomenon known as priority effects [13-15]. However, it is less clear whether priority effects during microbiome assembly are consequential for the host [16] or whether intraspecific variation in host traits can alter the trajectory of microbiome assembly under priority effects. In a greenhouse inoculation experiment using the black cottonwood (Populus trichocarpa) foliar microbiome, we manipulated host genotype and the colonization order of common foliar fungi. We quantified microbiome assembly outcomes using fungal marker gene sequencing and measured susceptibility of the colonized host to a leaf rust pathogen, Melampsora × columbiana. We found that the effect of species arrival order on microbiome composition, and subsequent disease susceptibility, depended on the host genotype. Additionally, we found that microbiome assembly history can affect host disease susceptibility independent of microbiome composition at the time of pathogen exposure, suggesting that the interactive effects of species arrival order and host genotype can decouple community composition and function. Overall, these results highlight the importance of a key process underlying stochasticity in microbiome assembly while also revealing which hosts are most likely to experience these effects.
宿主相关微生物组的组成会对宿主的健康和适应能力产生重要影响[1-3]。然而，我们仍然缺乏对许多决定微生物组组成的基本过程的理解[4,5]。越来越多的证据表明，微生物组组装过程中的历史偶然性可能会超过更具决定性的过程，例如宿主特征所施加的选择过滤器[6-8]。更具体地说，物种到达顺序经常被证明会影响微生物组的组成[9-12]，这一现象被称为优先效应[13-15]。然而，目前尚不清楚微生物组组装过程中的优先效应是否对宿主有影响[16]，或者宿主特征的种内变异是否会改变优先效应下微生物组组装的轨迹。在一项使用黑棉白杨（Populus trichocarpa）叶片微生物组的温室接种实验中，我们操纵了宿主基因型和常见叶片真菌的定植顺序。我们使用真菌标记基因测序来量化微生物组组装的结果，并测量了定植宿主对叶锈病病原体 Melampsora × columbiana 的易感性。我们发现，物种到达顺序对微生物组组成以及随后的疾病易感性的影响取决于宿主基因型。此外，我们发现微生物组组装历史可以独立于病原体暴露时的微生物组组成影响宿主疾病易感性，这表明物种到达顺序和宿主基因型的相互作用可以使群落组成和功能解耦。总的来说，这些结果强调了微生物组组装随机性的一个关键过程的重要性，同时也揭示了哪些宿主最有可能经历这些影响。
