Xue Hong, Cordero Otto X, Camas Francisco M, Trimble William, Meyer Folker, Guglielmini Julien, Rocha Eduardo P C, Polz Martin F
Parsons Laboratory for Environmental Science and Engineering, Massachusetts Institute of Technology, Cambridge, Massachusetts, USA.
Department of Environmental Systems Science, ETH Zürich, Zürich, Switzerland.
mBio. 2015 May 5;6(3):e00552-15. doi: 10.1128/mBio.00552-15.
Although plasmids and other episomes are recognized as key players in horizontal gene transfer among microbes, their diversity and dynamics among ecologically structured host populations in the wild remain poorly understood. Here, we show that natural populations of marine Vibrionaceae bacteria host large numbers of families of episomes, consisting of plasmids and a surprisingly high fraction of plasmid-like temperate phages. Episomes are unevenly distributed among host populations, and contrary to the notion that high-density communities in biofilms act as hot spots of gene transfer, we identified a strong bias for episomes to occur in free-living as opposed to particle-attached cells. Mapping of episomal families onto host phylogeny shows that, with the exception of all phage and a few plasmid families, most are of recent evolutionary origin and appear to have spread rapidly by horizontal transfer. Such high eco-evolutionary turnover is particularly surprising for plasmids that are, based on previously suggested categorization, putatively nontransmissible, indicating that this type of plasmid is indeed frequently transferred by currently unknown mechanisms. Finally, analysis of recent gene transfer among plasmids reveals a network of extensive exchange connecting nearly all episomes. Genes functioning in plasmid transfer and maintenance are frequently exchanged, suggesting that plasmids can be rapidly transformed from one category to another. The broad distribution of episomes among distantly related hosts and the observed promiscuous recombination patterns show how episomes can offer their hosts rapid assembly and dissemination of novel functions.
Plasmids and other episomes are an integral part of bacterial biology in all environments, yet their study is heavily biased toward their role as vectors for antibiotic resistance genes. This study presents a comprehensive analysis of all episomes within several coexisting bacterial populations of Vibrionaceae from the coastal ocean and represents the largest-yet genomic survey of episomes from a single bacterial family. The host population framework allows analysis of the eco-evolutionary dynamics at unprecedented resolution, yielding several unexpected results. These include (i) discovery of novel, nonintegrative temperate phages, (ii) revision of a class of episomes, previously termed "nontransmissible," as highly transmissible, and (iii) surprisingly high evolutionary turnover of episomes, manifest as frequent birth, spread, and loss.
尽管质粒和其他附加体被认为是微生物间水平基因转移的关键参与者，但它们在野生生态结构宿主群体中的多样性和动态变化仍知之甚少。在此，我们表明海洋弧菌科细菌的自然种群中存在大量附加体家族，包括质粒和比例惊人的类质粒温和噬菌体。附加体在宿主群体中的分布并不均匀，与生物膜中高密度群落是基因转移热点这一观点相反，我们发现附加体在自由生活的细胞而非附着于颗粒的细胞中出现的强烈偏向性。将附加体家族映射到宿主系统发育树上表明，除了所有噬菌体和少数质粒家族外，大多数是近期进化起源的，并且似乎通过水平转移迅速传播。对于基于先前分类被认为是推定不可传播的质粒而言，这种高生态进化周转率尤其令人惊讶，这表明这类质粒确实经常通过目前未知的机制进行转移。最后，对质粒间近期基因转移的分析揭示了一个连接几乎所有附加体的广泛交换网络。在质粒转移和维持中起作用的基因经常发生交换，这表明质粒可以迅速从一种类型转变为另一种类型。附加体在远缘宿主中的广泛分布以及观察到的混杂重组模式表明附加体如何为其宿主提供新功能的快速组装和传播。
质粒和其他附加体是所有环境中细菌生物学的一个组成部分，然而它们的研究严重偏向于其作为抗生素抗性基因载体的作用。本研究对来自沿海洋域的几个共存弧菌科细菌种群中的所有附加体进行了全面分析，代表了对单个细菌家族附加体进行的最大规模基因组调查。宿主群体框架允许以前所未有的分辨率分析生态进化动态，产生了几个意想不到的结果。这些结果包括：（i）发现新型非整合性温和噬菌体；（ii）将一类先前称为“不可传播”的附加体修订为高度可传播的；（iii）附加体惊人的高进化周转率，表现为频繁的产生、传播和丢失。
