Gene Acquisition by a Distinct Phyletic Group within Streptococcus pneumoniae Promotes Adhesion to the Ocular Epithelium.
Gene Acquisition by a Distinct Phyletic Group within Streptococcus pneumoniae Promotes Adhesion to the Ocular Epithelium.
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DOI：
10.1128/msphere.00213-17
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发表时间：
2017-09
期刊：
影响因子：
4.8
通讯作者：
Hiller NL
中科院分区：
文献类型：
--
作者：
Antic I;Brothers KM;Stolzer M;Lai H;Powell E;Eutsey R;Cuevas RA;Miao X;Kowalski RP;Shanks RMQ;Durand D;Hiller NL
病原体基因内容的变化可以改变它们在人类宿主不同身体部位定殖和/或生存的能力。在这项研究中，我们研究了基因获取事件及其在肺炎链球菌（肺炎球菌）发病机制中的作用。我们的研究结果表明，编码预测表面蛋白 SspB 的基因已从猪链球菌（一种远缘链球菌物种）转移到一组独特的肺炎球菌菌株中。这组菌株与其余肺炎球菌菌株的区别在于基因组组成的巨大差异以及引起结膜炎的能力。我们发现 sspB 的存在增加了肺炎球菌对眼上皮的粘附。因此，我们的数据支持这样的假设，即肺炎球菌菌株的一个子集从邻近物种获得了基因，增强了它们在眼睛上皮细胞中定殖的能力，从而扩展到一个新的生态位。肺炎链球菌（肺炎球菌）表现出广泛的组织嗜性并感染人类宿主的多个身体部位。然而，结膜感染仅限于具有多位点序列类型 ST448、ST344、ST1186、ST1270 和 ST2315 的不同系统群内的菌株。在这项研究中，我们对从眼部感染中分离出的六种肺炎球菌菌株的基因组进行了测序。结膜炎分离株与鼻咽分离株一起被分为不同的系统群。角膜炎（角膜感染）和眼内炎（玻璃体感染）分离株与其余肺炎球菌菌株归为一组。表型特征与不同系统群相关的形态差异一致。具体而言，来自不同系统群的分离物在浮游培养物中形成聚集体，并在非生物表面生长的生物膜中形成链状结构。为了开始研究基因型和流行病学之间的关联，我们重点研究了由这个独特的系统群专门编码的预测表面暴露粘附素（SspB）。在链球菌物种树的背景下对编码 SspB 的基因进行的系统发育分析表明，sspB 是通过猪链球菌的横向基因转移获得的。此外，与同基因野生型和互补菌株相比，sspB 缺失突变体表现出对眼上皮培养细胞的粘附性降低。这些发现共同表明，从物种外部获取基因通过增强部分菌株感染眼上皮导致结膜炎的能力，从而促进了肺炎球菌的组织向性。重要性 病原体基因内容的变化可以改变它们在人类宿主不同身体部位定殖和/或生存的能力。在这项研究中，我们研究了基因获取事件及其在肺炎链球菌（肺炎球菌）发病机制中的作用。我们的研究结果表明，编码预测表面蛋白 SspB 的基因已从猪链球菌（一种远缘链球菌物种）转移到一组独特的肺炎球菌菌株中。这组菌株与其余肺炎球菌菌株的区别在于基因组组成的巨大差异以及引起结膜炎的能力。我们发现 sspB 的存在增加了肺炎球菌对眼上皮的粘附。因此，我们的数据支持这样的假设，即肺炎球菌菌株的一个子集从邻近物种获得了基因，增强了它们在眼睛上皮细胞中定殖的能力，从而扩展到一个新的生态位。
Changes in the gene content of pathogens can modify their ability to colonize and/or survive in different body sites in the human host. In this study, we investigate a gene acquisition event and its role in the pathogenesis of Streptococccus pneumoniae (pneumococcus). Our findings suggest that the gene encoding the predicted surface protein SspB has been transferred from Streptococcus suis (a distantly related streptococcal species) into a distinct set of pneumococcal strains. This group of strains distinguishes itself from the remainder of pneumococcal strains by extensive differences in genomic composition and by the ability to cause conjunctivitis. We find that the presence of sspB increases adherence of pneumococcus to the ocular epithelium. Thus, our data support the hypothesis that a subset of pneumococcal strains has gained genes from neighboring species that enhance their ability to colonize the epithelium of the eye, thus expanding into a new niche. Streptococcus pneumoniae (pneumococcus) displays broad tissue tropism and infects multiple body sites in the human host. However, infections of the conjunctiva are limited to strains within a distinct phyletic group with multilocus sequence types ST448, ST344, ST1186, ST1270, and ST2315. In this study, we sequenced the genomes of six pneumococcal strains isolated from eye infections. The conjunctivitis isolates are grouped in a distinct phyletic group together with a subset of nasopharyngeal isolates. The keratitis (infection of the cornea) and endophthalmitis (infection of the vitreous body) isolates are grouped with the remainder of pneumococcal strains. Phenotypic characterization is consistent with morphological differences associated with the distinct phyletic group. Specifically, isolates from the distinct phyletic group form aggregates in planktonic cultures and chain-like structures in biofilms grown on abiotic surfaces. To begin to investigate the association between genotype and epidemiology, we focused on a predicted surface-exposed adhesin (SspB) encoded exclusively by this distinct phyletic group. Phylogenetic analysis of the gene encoding SspB in the context of a streptococcal species tree suggests that sspB was acquired by lateral gene transfer from Streptococcus suis. Furthermore, an sspB deletion mutant displays decreased adherence to cultured cells from the ocular epithelium compared to the isogenic wild-type and complemented strains. Together these findings suggest that acquisition of genes from outside the species has contributed to pneumococcal tissue tropism by enhancing the ability of a subset of strains to infect the ocular epithelium causing conjunctivitis. IMPORTANCE Changes in the gene content of pathogens can modify their ability to colonize and/or survive in different body sites in the human host. In this study, we investigate a gene acquisition event and its role in the pathogenesis of Streptococccus pneumoniae (pneumococcus). Our findings suggest that the gene encoding the predicted surface protein SspB has been transferred from Streptococcus suis (a distantly related streptococcal species) into a distinct set of pneumococcal strains. This group of strains distinguishes itself from the remainder of pneumococcal strains by extensive differences in genomic composition and by the ability to cause conjunctivitis. We find that the presence of sspB increases adherence of pneumococcus to the ocular epithelium. Thus, our data support the hypothesis that a subset of pneumococcal strains has gained genes from neighboring species that enhance their ability to colonize the epithelium of the eye, thus expanding into a new niche.