Parallel evolution of a type IV secretion system in radiating lineages of the host-restricted bacterial pathogen Bartonella.

Parallel evolution of a type IV secretion system in radiating lineages of the host-restricted bacterial pathogen Bartonella.
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DOI:
10.1371/journal.pgen.1001296
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发表时间:
2011-02-10
期刊:
影响因子:
4.5
通讯作者:
Dehio C
Dehio C
中科院分区:
生物学2区
文献类型:
--
作者:
Engel P;Salzburger W;Liesch M;Chang CC;Maruyama S;Lanz C;Calteau A;Lajus A;Médigue C;Schuster SC;Dehio C

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适应性辐射是多个物种从一个单一的祖先快速起源的结果,同时适应不同的环境。这一基本的进化过程被认为是大部分生命多样性起源的原因。细菌通过利用一系列特殊的环境进化出了巨大的生物多样性,但通过适应性辐射的细菌多样性仅在少数情况下被记录在案,并且基本的分子机制在很大程度上是未知的。在这里,我们展示了病原菌适应性辐射的一个令人信服的例子,并揭示了它们的遗传基础。我们对巴尔通体属α-变形菌的进化基因组分析揭示了这些宿主限制性哺乳动物病原体中的两种平行适应性辐射。我们确定了一个水平获得的蛋白质分泌系统,该系统已经进化到将特定的细菌效应蛋白靶向宿主细胞,作为触发这些并行适应性辐射的进化关键创新。我们发现,VirB IV型分泌系统(T4 SS)的功能多样性和适应潜力,从而易位巴尔通体效应蛋白(Beps),在两个谱系平行进化之前,他们的辐射。virB操纵子的独立染色体固定和谱系特异性bep基因重复的连续轮,随后由其功能多样化表征这些平行的进化轨迹。虽然大多数Beps保持其祖先的结构域的宪法,引人注目的是,一种新型的效应蛋白出现在两个谱系收敛。这导致在巴尔通体的两个谱系中宿主细胞靶向效应蛋白的类似阵列作为其独立辐射的基础。VirB/Bep系统的平行分子进化展示了独立适应过程和细菌病原体出现的关键创新的一个引人注目的例子。此外,我们的研究强调了T4 SSs及其效应蛋白的显著进化性,解释了它们在细菌与环境相互作用中的广泛应用。适应性辐射是一系列物种通过不同生态位的不同殖民化而快速起源。就致病菌而言,辐射可导致新的人类病原体的出现。巴尔通体属分化适应于一系列不同的哺乳动物宿主,包括作为储库或偶然宿主的人类,代表了研究支撑病原体分化适应的基因组机制的合适模型。在这里,我们表明,巴尔通体的两个不同的谱系平行辐射,导致两个阵列的进化不同的物种适应重叠套哺乳动物宿主。这种平行显示优秀的模型,揭示这些独立的进化过程背后的遗传机制的见解。我们的全基因组分析确定了一个惊人的进化平行的水平获得的蛋白质分泌系统中的两个谱系。该系统在两个谱系中的平行进化轨迹的特征在于致力于哺乳动物宿主内的细胞相互作用的广泛的适应性功能的会聚起源。这两个辐射谱系在生态和分子水平上的平行进化表明,分泌系统的水平获取和功能多样化显示了适应性进化背后的进化关键创新。
Adaptive radiation is the rapid origination of multiple species from a single ancestor as the result of concurrent adaptation to disparate environments. This fundamental evolutionary process is considered to be responsible for the genesis of a great portion of the diversity of life. Bacteria have evolved enormous biological diversity by exploiting an exceptional range of environments, yet diversification of bacteria via adaptive radiation has been documented in a few cases only and the underlying molecular mechanisms are largely unknown. Here we show a compelling example of adaptive radiation in pathogenic bacteria and reveal their genetic basis. Our evolutionary genomic analyses of the α-proteobacterial genus Bartonella uncover two parallel adaptive radiations within these host-restricted mammalian pathogens. We identify a horizontally-acquired protein secretion system, which has evolved to target specific bacterial effector proteins into host cells as the evolutionary key innovation triggering these parallel adaptive radiations. We show that the functional versatility and adaptive potential of the VirB type IV secretion system (T4SS), and thereby translocated Bartonella effector proteins (Beps), evolved in parallel in the two lineages prior to their radiations. Independent chromosomal fixation of the virB operon and consecutive rounds of lineage-specific bep gene duplications followed by their functional diversification characterize these parallel evolutionary trajectories. Whereas most Beps maintained their ancestral domain constitution, strikingly, a novel type of effector protein emerged convergently in both lineages. This resulted in similar arrays of host cell-targeted effector proteins in the two lineages of Bartonella as the basis of their independent radiation. The parallel molecular evolution of the VirB/Bep system displays a striking example of a key innovation involved in independent adaptive processes and the emergence of bacterial pathogens. Furthermore, our study highlights the remarkable evolvability of T4SSs and their effector proteins, explaining their broad application in bacterial interactions with the environment. Adaptive radiation is the rapid origination of an array of species by the divergent colonization of disparate ecological niches. In the case of pathogenic bacteria, radiations can lead to the emergence of novel human pathogens. Being divergently adapted to a range of different mammalian hosts, including humans as reservoir or incidental hosts, the genus Bartonella represents a suitable model to study genomic mechanisms underpinning divergent adaptation of pathogens. Here we show that two distinct lineages of Bartonella have radiated in parallel, resulting in two arrays of evolutionary distinct species adapted to overlapping sets of mammalian hosts. Such parallelisms display excellent models to reveal insights into the genetic mechanisms underlying these independent evolutionary processes. Our genome-wide analysis identifies a striking evolutionary parallelism in a horizontally-acquired protein secretion system in the two lineages. The parallel evolutionary trajectory of this system in the two lineages is characterized by the convergent origination of a wide array of adaptive functions dedicated to the cellular interaction within the mammalian hosts. The parallel evolution of the two radiating lineages on the ecological as well as on the molecular level suggests that the horizontal acquisition and the functional diversification of the secretion system display an evolutionary key innovation underlying adaptive evolution.
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影响因子: 11.8
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DOI: 10.1371/journal.pgen.1000546
发表时间: 2009-07
期刊: PLoS genetics
影响因子: 4.5
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