Evolutionary genomics of a temperate bacteriophage in an obligate intracellular bacteria (Wolbachia).

Evolutionary genomics of a temperate bacteriophage in an obligate intracellular bacteria (Wolbachia).
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DOI:
10.1371/journal.pone.0024984
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发表时间:
2011
期刊:
影响因子:
3.7
通讯作者:
Bordenstein SR
Bordenstein SR
中科院分区:
综合性期刊3区
文献类型:
--
作者:
Kent BN;Funkhouser LJ;Setia S;Bordenstein SR

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细菌的基因组进化通常受到生态的影响,例如,具有自由生活阶段的细菌具有较大的基因组和较高的水平基因转移率,而专性细胞内细菌具有较小的基因组和通常较低的基因交换量。然而,最近的研究表明,宿主转换的专性细胞内物种经常含有水平转移的媒介,例如移动元件。例如,沃尔巴克氏体中的温带双链DNA噬菌体WO在同一宿主的细菌共感染之间持续转移。在这里,我们表明,尽管噬菌体在共感染之间具有猖獗的流动性,但原噬菌体的基因组显示出与其细胞内生态位相关的限制特征。首先,每个沃尔巴克氏体基因组中总是至少有一个完整的前噬菌体 WO,并且通常有几个简并的、独立获得的 WO 前噬菌体。其次,虽然原噬菌体基因组的组成是模块化的,具有相似功能的基因组合在一起,但这些模块通常不能与其他不相关的噬菌体互换,因此不能按照模块化理论进化。第三,有一个不寻常的核心基因组,严格由头部和底板基因组成;其他基因模块经常被删除。第四,原噬菌体重组酶多种多样,没有保守的整合序列。最后,作用于原噬菌体WO的分子进化力是点突变、基因内重组、缺失和纯化选择。总而言之,这些分析表明,虽然噬菌体 WO 的横向转移在沃尔巴克氏体之间普遍存在,偶尔会摄取新基因,但细胞内生态位的限制阻碍了 WO 与全球噬菌体群体之间的广泛混合。尽管模块化理论长期以来被认为是自由生活细菌中温和噬菌体进化的范式,但它似乎与专性细胞内细菌的噬菌体无关。
Genome evolution of bacteria is usually influenced by ecology, such that bacteria with a free-living stage have large genomes and high rates of horizontal gene transfer, while obligate intracellular bacteria have small genomes with typically low amounts of gene exchange. However, recent studies indicate that obligate intracellular species that host-switch frequently harbor agents of horizontal transfer such as mobile elements. For example, the temperate double-stranded DNA bacteriophage WO in Wolbachia persistently transfers between bacterial coinfections in the same host. Here we show that despite the phage's rampant mobility between coinfections, the prophage's genome displays features of constraint related to its intracellular niche. First, there is always at least one intact prophage WO and usually several degenerate, independently-acquired WO prophages in each Wolbachia genome. Second, while the prophage genomes are modular in composition with genes of similar function grouping together, the modules are generally not interchangeable with other unrelated phages and thus do not evolve by the Modular Theory. Third, there is an unusual core genome that strictly consists of head and baseplate genes; other gene modules are frequently deleted. Fourth, the prophage recombinases are diverse and there is no conserved integration sequence. Finally, the molecular evolutionary forces acting on prophage WO are point mutation, intragenic recombination, deletion, and purifying selection. Taken together, these analyses indicate that while lateral transfer of phage WO is pervasive between Wolbachia with occasional new gene uptake, constraints of the intracellular niche obstruct extensive mixture between WO and the global phage population. Although the Modular Theory has long been considered the paradigm of temperate bacteriophage evolution in free-living bacteria, it appears irrelevant in phages of obligate intracellular bacteria.