Evidence of extensive DNA transfer between bacteroidales species within the human gut.

Evidence of extensive DNA transfer between bacteroidales species within the human gut.
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DOI:
10.1128/mbio.01305-14
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发表时间:
2014-06-17
期刊:
影响因子:
6.4
通讯作者:
Comstock LE
Comstock LE
中科院分区:
生物学1区
文献类型:
--
作者:
Coyne MJ;Zitomersky NL;McGuire AM;Earl AM;Comstock LE

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肠道拟杆菌属菌株的基因组序列揭示了广泛的水平基因转移的证据。拟杆菌和其他细菌的体外研究已经解决了接合转移的机制和这些DNA获得在受体中的一些表型结果,例如获得抗生素抗性。然而,很少有研究涉及的水平转移的细菌物种共存的自然微生物群落,特别是人类的微生物生态系统中的遗传元件。在这里,我们研究了两个成年人的拟杆菌属物种的基因组,以确定这些拟杆菌之间可能转移的遗传因子,而它们在肠道中共存。使用7个共存拟杆菌属物种从一个人和8个从另一个,我们确定了5个大的染色体区域,每个存在于至少三个共存菌株在近100%的DNA同一性。这五个区域在任何其他测序的拟杆菌属基因组中都没有发现,可能都是整合接合元件(ICE)。这种高度相似和独特的区域仅出现在0.4%的具有遗传学代表性的模拟群落中,这提供了强有力的证据,表明这五个区域在这些受试者的共存菌株之间转移。除了转移所必需的必需蛋白质之外,这些元件编码预测增加适应性的蛋白质,包括可能改变基因表达的孤儿DNA甲基化酶、可能促进附着和利用新底物的菌毛合成蛋白、推定的分泌型抗微生物分子和预测的VI型分泌系统(T6SS),这可以赋予这些菌株在其复杂的微生物生态系统中的竞争性生态优势。通过分析两个成年人肠道微生物群中共存的拟杆菌属菌株,我们为人类个体肠道微生物群中整合接合元件的广泛种间和家族间转移提供了强有力的证据。在受体菌株中,我们表明,接合元件本身可以通过插入序列和受体基因组的逆转录元件的转座进行修饰,随后将这些修饰的元件转移到微生物群的其他成员中。这些数据表明,我们肠道细菌的基因组被生态系统中的其他共存成员大幅修改,导致高度个性化的拟杆菌菌株可能是该个体所独有的。这些ICE的遗传内容表明,它们从成功适应的生态系统成员转移给受体,增加其适应性,使其能够在特定的个性化肠道微生物生态系统中更好地竞争。
The genome sequences of intestinal Bacteroidales strains reveal evidence of extensive horizontal gene transfer. In vitro studies of Bacteroides and other bacteria have addressed mechanisms of conjugative transfer and some phenotypic outcomes of these DNA acquisitions in the recipient, such as the acquisition of antibiotic resistance. However, few studies have addressed the horizontal transfer of genetic elements between bacterial species coresident in natural microbial communities, especially microbial ecosystems of humans. Here, we examine the genomes of Bacteroidales species from two human adults to identify genetic elements that were likely transferred among these Bacteroidales while they were coresident in the intestine. Using seven coresident Bacteroidales species from one individual and eight from another, we identified five large chromosomal regions, each present in a minimum of three of the coresident strains at near 100% DNA identity. These five regions are not found in any other sequenced Bacteroidetes genome at this level of identity and are likely all integrative conjugative elements (ICEs). Such highly similar and unique regions occur in only 0.4% of phylogenetically representative mock communities, providing strong evidence that these five regions were transferred between coresident strains in these subjects. In addition to the requisite proteins necessary for transfer, these elements encode proteins predicted to increase fitness, including orphan DNA methylases that may alter gene expression, fimbriae synthesis proteins that may facilitate attachment and the utilization of new substrates, putative secreted antimicrobial molecules, and a predicted type VI secretion system (T6SS), which may confer a competitive ecological advantage to these strains in their complex microbial ecosystem. By analyzing Bacteroidales strains coresident in the gut microbiota of two human adults, we provide strong evidence for extensive interspecies and interfamily transfer of integrative conjugative elements within the intestinal microbiota of individual humans. In the recipient strain, we show that the conjugative elements themselves can be modified by the transposition of insertion sequences and retroelements from the recipient’s genome, with subsequent transfer of these modified elements to other members of the microbiota. These data suggest that the genomes of our gut bacteria are substantially modified by other, coresident members of the ecosystem, resulting in highly personalized Bacteroidales strains likely unique to that individual. The genetic content of these ICEs suggests that their transfer from successful adapted members of an ecosystem confers beneficial properties to the recipient, increasing its fitness and allowing it to better compete within its particular personalized gut microbial ecosystem.