Yang Wentao, Petersen Carola, Pees Barbara, Zimmermann Johannes, Waschina Silvio, Dirksen Philipp, Rosenstiel Philip, Tholey Andreas, Leippe Matthias, Dierking Katja, Kaleta Christoph, Schulenburg Hinrich
Research Group Evolutionary Ecology and Genetics, Zoological Institute, Christian-Albrechts-Universität zu Kiel, Kiel, Germany.
Research Group Comparative Immunobiology, Zoological Institute, Christian-Albrechts-Universität zu Kiel, Kiel, Germany.
Front Microbiol. 2019 Aug 7;10:1793. doi: 10.3389/fmicb.2019.01793. eCollection 2019.
The biology of all organisms is influenced by the associated community of microorganisms. In spite of its importance, it is usually not well understood how exactly this microbiota affects host functions and what are the underlying molecular processes. To rectify this knowledge gap, we took advantage of the nematode as a tractable, experimental model system and assessed the inducible transcriptome response after colonization with members of its native microbiota. For this study, we focused on two isolates of the genus . These bacteria are known to be abundant in the nematode's microbiota and are capable of colonizing and persisting in the nematode gut, even under stressful conditions. The transcriptome response was assessed across development and three time points of adult life, using general and -specific enrichment analyses to identify affected functions. Our assessment revealed an influence of the microbiota members on the nematode's dietary response, development, fertility, immunity, and energy metabolism. This response is mainly regulated by a GATA transcription factor, most likely ELT-2, as indicated by the enrichment of (i) the GATA motif in the promoter regions of inducible genes and (ii) of ELT-2 targets among the differentially expressed genes. We compared our transcriptome results with a corresponding previously characterized proteome data set, highlighting a significant overlap in the differentially expressed genes, the affected functions, and ELT-2 target genes. Our analysis further identified a core set of 86 genes that consistently responded to the microbiota members across development and adult life, including several C-type lectin-like genes and genes known to be involved in energy metabolism or fertility. We additionally assessed the consequences of induced gene expression with the help of metabolic network model analysis, using a previously established metabolic network for . This analysis complemented the enrichment analyses by revealing an influence of the isolates on energy metabolism and furthermore metabolism of specific amino acids, fatty acids, and also folate biosynthesis. Our findings highlight the multifaceted impact of naturally colonizing microbiota isolates on life history and thereby provide a framework for further analysis of microbiota-mediated host functions.
所有生物体的生物学特性都受到相关微生物群落的影响。尽管其重要性,但通常人们并不十分清楚这种微生物群究竟如何影响宿主功能以及潜在的分子过程是什么。为了弥补这一知识空白,我们利用线虫作为一个易于处理的实验模型系统,并评估了用其天然微生物群成员定殖后的诱导转录组反应。在本研究中,我们聚焦于该属的两个分离株。已知这些细菌在线虫的微生物群中含量丰富,并且即使在压力条件下也能够在线虫肠道中定殖并持续存在。我们使用通用和特定富集分析来确定受影响的功能,从而在发育过程和成年生活的三个时间点评估转录组反应。我们的评估揭示了微生物群成员对线虫的饮食反应、发育、繁殖力、免疫力和能量代谢的影响。这种反应主要由一种GATA转录因子调控,很可能是ELT-2,这一点通过以下方面得到体现:(i)诱导基因启动子区域中GATA基序的富集,以及(ii)差异表达基因中ELT-2靶标的富集。我们将转录组结果与先前表征的相应蛋白质组数据集进行了比较,突出了差异表达基因、受影响的功能以及ELT-2靶基因之间的显著重叠。我们的分析进一步确定了一组86个核心基因,这些基因在发育过程和成年生活中始终对微生物群成员产生反应,包括几个C型凝集素样基因以及已知参与能量代谢或繁殖力的基因。我们还借助代谢网络模型分析评估了诱导基因表达的后果,使用了先前建立的针对该线虫的代谢网络。该分析通过揭示该分离株对线虫能量代谢以及特定氨基酸、脂肪酸代谢以及叶酸生物合成的影响,对富集分析进行了补充。我们的研究结果突出了自然定殖的微生物群分离株对线虫生活史的多方面影响,从而为进一步分析微生物群介导的宿主功能提供了一个框架。