Vertical Inheritance Facilitates Interspecies Diversification in Biosynthetic Gene Clusters and Specialized Metabolites.
Vertical Inheritance Facilitates Interspecies Diversification in Biosynthetic Gene Clusters and Specialized Metabolites.
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DOI：
10.1128/mbio.02700-21
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发表时间：
2021-12-21
期刊：
影响因子：
6.4
通讯作者：
Jensen PR
中科院分区：
文献类型：
--
作者：
Chase AB;Sweeney D;Muskat MN;Guillén-Matus DG;Jensen PR
虽然特殊代谢物被认为介导生态相互作用，但驱动化学多样化的进化过程，尤其是在密切相关的谱系之间，仍然知之甚少。在此，我们研究了控制天然产物生物合成基因簇（BGCs）在代表海洋放线菌属盐孢菌属目前所有九个已命名物种的118个菌株中的分布的进化动态。虽然水平基因转移（HGT）在构建BGC分布中的作用已受到大量关注，但我们发现垂直遗传在进化时间尺度上促进了种间BGC多样化。此外，我们在BGC和代谢物水平上在盐孢菌属物种中都发现了明显的系统发育信号，这表明特殊代谢是一种保守的系统发育特征。通过结合基因组分析以及针对九个经过实验表征的BGC及其小分子产物的液相色谱 - 高分辨率串联质谱（LC - MS/MS），我们确定了基因获得/缺失事件、受限的种间重组以及与垂直遗传相关的其他进化过程是BGC多样化的主要贡献因素。这些进化动态对所产生的化合物有直接影响，例如盐孢酰胺生产中的物种水平差异。总之，我们的结果支持这样的概念：特殊代谢物及其相关的BGC可以代表系统发育上保守的功能特征，并且化学多样化在进化时间框架内以物种特异性模式进行。
While specialized metabolites are thought to mediate ecological interactions, the evolutionary processes driving chemical diversification, particularly among closely related lineages, remain poorly understood. Here, we examine the evolutionary dynamics governing the distribution of natural product biosynthetic gene clusters (BGCs) among 118 strains representing all nine currently named species of the marine actinobacterial genus Salinispora. While much attention has been given to the role of horizontal gene transfer (HGT) in structuring BGC distributions, we find that vertical descent facilitates interspecies BGC diversification over evolutionary timescales. Moreover, we identified a distinct phylogenetic signal among Salinispora species at both the BGC and metabolite level, indicating that specialized metabolism represents a conserved phylogenetic trait. Using a combination of genomic analyses and liquid chromatography–high-resolution tandem mass spectrometry (LC-MS/MS) targeting nine experimentally characterized BGCs and their small molecule products, we identified gene gain/loss events, constrained interspecies recombination, and other evolutionary processes associated with vertical inheritance as major contributors to BGC diversification. These evolutionary dynamics had direct consequences for the compounds produced, as exemplified by species-level differences in salinosporamide production. Together, our results support the concept that specialized metabolites, and their cognate BGCs, can represent phylogenetically conserved functional traits with chemical diversification proceeding in species-specific patterns over evolutionary time frames.