Department of Ecology and Evolutionary Biology, University of California, Irvine, California, USA.
Department of Integrative Biology, University of Texas at Austin, Austin, Texas, USA.
Mol Ecol. 2023 Feb;32(3):724-740. doi: 10.1111/mec.16769. Epub 2022 Nov 22.
How a host's microbiome changes over its lifespan can influence development and ageing. As these temporal patterns have only been described in detail for a handful of hosts, an important next step is to compare microbiome succession more broadly and investigate why it varies. Here we characterize the temporal dynamics and stability of the bumble bee worker gut microbiome. Bumble bees have simple and host-specific gut microbiomes, and their microbial dynamics may influence health and pollination services. We used 16S rRNA gene sequencing, quantitative PCR and metagenomics to characterize gut microbiomes over the lifespan of Bombus impatiens workers. We also sequenced gut transcriptomes to examine host factors that may control the microbiome. At the community level, microbiome assembly is highly predictable and similar to patterns of primary succession observed in the human gut. However, at the strain level, partitioning of bacterial variants among colonies suggests stochastic colonization events similar to those observed in flies and nematodes. We also find strong differences in temporal dynamics among symbiont species, suggesting ecological differences among microbiome members in colonization and persistence. Finally, we show that both the gut microbiome and host transcriptome-including expression of key immunity genes-stabilize, as opposed to senesce, with age. We suggest that in highly social groups such as bumble bees, maintenance of both microbiomes and immunity contribute to inclusive fitness, and thus remain under selection even in old age. Our findings provide a foundation for exploring the mechanisms and functional outcomes of bee microbiome succession.
宿主微生物组在其生命周期中的变化如何影响其发育和衰老。由于这些时间模式仅在少数宿主中详细描述过,因此下一步的重要步骤是更广泛地比较微生物组的演替,并研究为什么会发生变化。在这里,我们描述了熊蜂工蜂肠道微生物组的时间动态和稳定性。熊蜂具有简单且宿主特异性的肠道微生物组,其微生物动态可能会影响其健康和传粉服务。我们使用 16S rRNA 基因测序、定量 PCR 和宏基因组学来描述 Bombus impatiens 工蜂在其生命周期中的肠道微生物组。我们还测序了肠道转录组,以研究可能控制微生物组的宿主因素。在群落水平上,微生物组的组装是高度可预测的,与在人类肠道中观察到的初生演替模式相似。然而,在菌株水平上,细菌变体在菌落之间的分区表明存在类似于在苍蝇和线虫中观察到的随机定植事件。我们还发现共生体物种之间的时间动态存在强烈差异,这表明微生物组成员在定植和持久性方面存在生态差异。最后,我们表明,肠道微生物组和宿主转录组(包括关键免疫基因的表达)都随着年龄的增长而稳定,而不是衰老。我们认为,在像熊蜂这样高度社会化的群体中,对两个微生物组和免疫力的维持有助于包容性适合度,因此即使在老年时也仍然受到选择。我们的研究结果为探索蜜蜂微生物组演替的机制和功能结果提供了基础。