Horizontal Gene Transfer Clarifies Taxonomic Confusion and Promotes the Genetic Diversity and Pathogenicity of Plesiomonas shigelloides
Horizontal Gene Transfer Clarifies Taxonomic Confusion and Promotes the Genetic Diversity and Pathogenicity of Plesiomonas shigelloides
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DOI：
10.1128/msystems.00448-20
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发表时间：
2020-09
期刊：
影响因子：
6.4
通讯作者：
Zhiqiu Yin;Si Zhang;Yi Wei;Meng Wang;Shuangshuang Ma;Shuang Yang;Jingting Wang;Chao Yuan;Lingyan Jiang;Yuhui Du
中科院分区：
文献类型：
--
作者：
Zhiqiu Yin;Si Zhang;Yi Wei;Meng Wang;Shuangshuang Ma;Shuang Yang;Jingting Wang;Chao Yuan;Lingyan Jiang;Yuhui Du
志贺氏菌的分类地位一直是人们争论的话题，到目前为止，志贺氏菌的进化动态和致病机制尚不清楚。在这项研究中，泛基因组分析表明，广泛的遗传多样性和大的和可变的基因库的存在。我们的结果表明，水平基因转移是志贺氏菌全基因组遗传多样性的主要驱动力，可能是导致新特性出现的原因之一。弧菌科和气单胞菌科是水平基因的主要供体类群，这可能是历史上造成分类混乱的原因。比较基因组分析揭示了志贺氏菌引起肠道和侵袭性疾病的可能性。我们的研究结果有助于加深对志贺氏菌进化和致病机制的理解，特别是在阐明水平基因转移的作用和研究毒力相关因素方面。摘要志贺样拟单胞菌是一种新发现的致病菌，已被证实与人类胃肠道疾病和肠外感染有关。然而，志贺氏菌的分类地位、进化动态和致病机制仍不清楚。我们报道了代表不同血清群的12株志贺氏菌的基因组草图。我们能够通过核心基因组系统发育、邻居网络和平均基因组同一性分析来确定志贺氏菌和肠杆菌属其他成员之间的明显区别。全基因组分析揭示了志贺氏菌广泛的遗传多样性，并呈现出大量灵活的基因谱系，而核心基因组系统发育表现出较低的克隆性。核心基因组系统发育和泛基因组系统发育的不一致表明，灵活的辅助基因组在志贺氏菌的进化中占有重要的比例，随后确定了数百个水平转移基因(水平基因)，大规模的基因扩张和收缩，以及多样化的可移动遗传元件(MGES)。志贺氏假单胞菌的水平基因转移(HGT)水平明显较高，来源于其他类群(主要是弧菌科和气单胞菌科)具有新特性的细菌，这造成了历史上的分类混乱，并形成了毒力基因库。此外，志贺氏杆菌基因组中含有许多大分子分泌系统基因、毒力因子基因和耐药基因，表明其具有引起肠道和侵袭性感染的潜力。综上所述，我们的工作在基因组水平上对志贺氏菌的系统发育地位、进化动态和致病机理提供了深入的见解，有助于对这种重要病原体的观察和研究。重要意义志贺氏菌的分类地位长期以来一直是争论的主题，到目前为止，志贺氏菌的进化动力学和致病机理尚不清楚。在这项研究中，泛基因组分析表明，广泛的遗传多样性和大的和可变的基因库的存在。我们的结果表明，水平基因转移是志贺氏菌全基因组遗传多样性的主要驱动力，可能是导致新特性出现的原因之一。弧菌科和气单胞菌科是水平基因的主要供体类群，这可能是历史上造成分类混乱的原因。比较基因组分析揭示了志贺氏菌引起肠道和侵袭性疾病的可能性。我们的研究结果有助于加深对志贺氏菌进化和致病机制的理解，特别是在阐明水平基因转移的作用和研究毒力相关因素方面。
The taxonomic position of P. shigelloides has been the subject of debate for a long time, and until now, the evolutionary dynamics and pathogenesis of P. shigelloides were unclear. In this study, pan-genome analysis indicated extensive genetic diversity and the presence of large and variable gene repertoires. Our results revealed that horizontal gene transfer was the focal driving force for the genetic diversity of the P. shigelloides pan-genome and might have contributed to the emergence of novel properties. Vibrionaceae and Aeromonadaceae were found to be the predominant donor taxa for horizontal genes, which might have caused the taxonomic confusion historically. Comparative genomic analysis revealed the potential of P. shigelloides to cause intestinal and invasive diseases. Our results could advance the understanding of the evolution and pathogenesis of P. shigelloides, particularly in elucidating the role of horizontal gene transfer and investigating virulence-related elements. ABSTRACT Plesiomonas shigelloides is an emerging pathogen that has been shown to be involved in gastrointestinal diseases and extraintestinal infections in humans. However, the taxonomic position, evolutionary dynamics, and pathogenesis of P. shigelloides remain unclear. We reported the draft genome sequences of 12 P. shigelloides strains representing different serogroups. We were able to determine a clear distinction between P. shigelloides and other members of Enterobacterales via core genome phylogeny, Neighbor-Net network, and average genome identity analysis. The pan-genome analysis of P. shigelloides revealed extensive genetic diversity and presented large flexible gene repertoires, while the core genome phylogeny exhibited a low level of clonality. The discordance between the core genome phylogeny and the pan-genome phylogeny indicated that flexible accessory genomes account for an important proportion of the evolution of P. shigelloides, which was subsequently characterized by determinations of hundreds of horizontally transferred genes (horizontal genes), massive gene expansions and contractions, and diverse mobile genetic elements (MGEs). The apparently high levels of horizontal gene transfer (HGT) in P. shigelloides were conferred from bacteria with novel properties from other taxa (mainly Vibrionaceae and Aeromonadaceae), which caused the historical taxonomic confusion and shaped the virulence gene pools. Furthermore, P. shigelloides genomes contain many macromolecular secretion system genes, virulence factor genes, and resistance genes, indicating its potential to cause intestinal and invasive infections. Collectively, our work provides insights into the phylogenetic position, evolutionary dynamic, and pathogenesis of P. shigelloides at the genomic level, which could facilitate the observation and research of this important pathogen. IMPORTANCE The taxonomic position of P. shigelloides has been the subject of debate for a long time, and until now, the evolutionary dynamics and pathogenesis of P. shigelloides were unclear. In this study, pan-genome analysis indicated extensive genetic diversity and the presence of large and variable gene repertoires. Our results revealed that horizontal gene transfer was the focal driving force for the genetic diversity of the P. shigelloides pan-genome and might have contributed to the emergence of novel properties. Vibrionaceae and Aeromonadaceae were found to be the predominant donor taxa for horizontal genes, which might have caused the taxonomic confusion historically. Comparative genomic analysis revealed the potential of P. shigelloides to cause intestinal and invasive diseases. Our results could advance the understanding of the evolution and pathogenesis of P. shigelloides, particularly in elucidating the role of horizontal gene transfer and investigating virulence-related elements.