Phylosymbiosis: Relationships and Functional Effects of Microbial Communities across Host Evolutionary History.

Phylosymbiosis: Relationships and Functional Effects of Microbial Communities across Host Evolutionary History.
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DOI:
10.1371/journal.pbio.2000225
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发表时间:
2016-11
期刊:
影响因子:
9.8
通讯作者:
Bordenstein SR
Bordenstein SR
中科院分区:
生物学1区
文献类型:
--
作者:
Brooks AW;Kohl KD;Brucker RM;van Opstal EJ;Bordenstein SR

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最近提出系统共生来描述生态进化模式,即宿主相关微生物群落的生态相关性与相关宿主物种的系统发育平行。在这里,我们通过表征来自四个不同类群(白鼠、果蝇、蚊子和黄蜂)的 24 种动物物种的微生物群,测试了高度控制条件下系统共生的普遍性及其功能意义,并重新评估了七种野生原始人类的系统共生关系。我们展示了三个关键发现。首先,种内微生物群变异始终小于种间微生物群变异,并且基于微生物群的模型可以在整个数据集中高精度地预测宿主物种起源。有趣的是,宿主进化枝分化的年龄与宿主进化枝内物种之间微生物群落的可区分性程度呈正相关,涵盖最近的宿主物种形成事件(约100万年前)到更遥远的相关宿主属(约1.08亿年前)。其次,对每组完整系统发育和微生物群树状图的拓扑一致性分析揭示了显着程度的系统共生,无论宿主进化枝年龄或分类学如何。第三,与驱动系统共生的宿主-微生物群相互作用的选择一致,当在密切相关和不同的宿主物种对之间进行种间微生物群移植时,会出现存活率和性能下降。总体而言,这些发现表明,动物微生物群落的组成和功能效应可以与宿主进化密切相关,即使在广泛的时间尺度和受控条件下饲养的不同动物系统中也是如此。对宿主-微生物群共生体的组装和功能的研究本质上因饮食、年龄、性别、宿主遗传学和内共生体的不同影响而变得复杂。阐明一种影响与另一种影响的核心是减少混杂因素的实验框架。这项研究利用四个动物群体(鹿、小鼠、苍蝇、蚊子和黄蜂)的共同饲养条件,跨越最近的宿主物种形成事件到更远亲的宿主属,测试微生物群落的组装在宿主相关性或“系统共生”方面是否总体上是随机的,其中宿主群体的系统发育与其微生物群落的生态关系一致。在所有四个动物群体和一个类人猿外部数据集中,我们应用了多种统计数据来分析一致性,并在每个群体中不同程度地证明了系统共生。此外,与驱动系统共生的宿主-微生物群相互作用的选择一致,在小鼠体内移植种间微生物群落显着降低了它们消化食物的能力。同样,接受来自不同黄蜂物种的微生物群落移植的黄蜂的存活率低于那些接受自身微生物群移植的黄蜂。总体而言,这个实验和统计框架显示了相关物种的微生物群落组装和功能如何与动物进化、健康和生存联系起来。
Phylosymbiosis was recently proposed to describe the eco-evolutionary pattern, whereby the ecological relatedness of host-associated microbial communities parallels the phylogeny of related host species. Here, we test the prevalence of phylosymbiosis and its functional significance under highly controlled conditions by characterizing the microbiota of 24 animal species from four different groups (Peromyscus deer mice, Drosophila flies, mosquitoes, and Nasonia wasps), and we reevaluate the phylosymbiotic relationships of seven species of wild hominids. We demonstrate three key findings. First, intraspecific microbiota variation is consistently less than interspecific microbiota variation, and microbiota-based models predict host species origin with high accuracy across the dataset. Interestingly, the age of host clade divergence positively associates with the degree of microbial community distinguishability between species within the host clades, spanning recent host speciation events (~1 million y ago) to more distantly related host genera (~108 million y ago). Second, topological congruence analyses of each group's complete phylogeny and microbiota dendrogram reveal significant degrees of phylosymbiosis, irrespective of host clade age or taxonomy. Third, consistent with selection on host–microbiota interactions driving phylosymbiosis, there are survival and performance reductions when interspecific microbiota transplants are conducted between closely related and divergent host species pairs. Overall, these findings indicate that the composition and functional effects of an animal's microbial community can be closely allied with host evolution, even across wide-ranging timescales and diverse animal systems reared under controlled conditions. Studies on the assembly and function of host-microbiota symbioses are inherently complicated by the diverse effects of diet, age, sex, host genetics, and endosymbionts. Central to unraveling one effect from the other is an experimental framework that reduces confounders. Using common rearing conditions across four animal groups (deer mice, flies, mosquitoes, and wasps) that span recent host speciation events to more distantly related host genera, this study tests whether microbial community assembly is generally random with respect to host relatedness or "phylosymbiotic," in which the phylogeny of the host group is congruent with ecological relationships of their microbial communities. Across all four animal groups and one external dataset of great apes, we apply several statistics for analyzing congruencies and demonstrate phylosymbiosis to varying degrees in each group. Moreover, consistent with selection on host–microbiota interactions driving phylosymbiosis, transplanting interspecific microbial communities in mice significantly decreased their ability to digest food. Similarly, wasps that received transplants of microbial communities from different wasp species had lower survival than those given their own microbiota. Overall, this experimental and statistical framework shows how microbial community assembly and functionality across related species can be linked to animal evolution, health, and survival.
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