Department of Biological Sciences, University at Albany, State University of New York, Albany, NY, USA.
Department of Molecular, Cellular and Biomedical Sciences, University of New Hampshire, Durham, NH, USA.
BMC Microbiol. 2023 Aug 25;23(1):235. doi: 10.1186/s12866-023-02985-9.
Staphylococcus aureus can infect and adapt to multiple host species. However, our understanding of the genetic and evolutionary drivers of its generalist lifestyle remains inadequate. This is particularly important when considering local populations of S. aureus, where close physical proximity between bacterial lineages and between host species may facilitate frequent and repeated interactions between them. Here, we aim to elucidate the genomic differences between human- and animal-derived S. aureus from 437 isolates sampled from disease cases in the northeast region of the United States.
Multi-locus sequence typing revealed the existence of 75 previously recognized sequence types (ST). Our population genomic analyses revealed heterogeneity in the accessory genome content of three dominant S. aureus lineages (ST5, ST8, ST30). Genes related to antimicrobial resistance, virulence, and plasmid types were differentially distributed among isolates according to host (human versus non-human) and among the three major STs. Across the entire population, we identified a total of 1,912 recombination events that occurred in 765 genes. The frequency and impact of homologous recombination were comparable between human- and animal-derived isolates. Low-frequency STs were major donors of recombined DNA, regardless of the identity of their host. The most frequently recombined genes (clfB, aroA, sraP) function in host infection and virulence, which were also frequently shared between the rare lineages.
Taken together, these results show that frequent but variable patterns of recombination among co-circulating S. aureus lineages, including the low-frequency lineages, that traverse host barriers shape the structure of local gene pool and the reservoir of host-associated genetic variants. Our study provides important insights to the genetic and evolutionary factors that contribute to the ability of S. aureus to colonize and cause disease in multiple host species. Our study highlights the importance of continuous surveillance of S. aureus circulating in different ecological host niches and the need to systematically sample from them. These findings will inform development of effective measures to control S. aureus colonization, infection, and transmission across the One Health continuum.
金黄色葡萄球菌可以感染和适应多种宿主物种。然而，我们对其普遍生活方式的遗传和进化驱动因素的理解仍然不足。当考虑到金黄色葡萄球菌的局部种群时，这一点尤其重要，因为细菌谱系之间以及宿主物种之间的近距离身体接近可能会促进它们之间频繁和反复的相互作用。在这里，我们旨在阐明从美国东北部疾病病例中采集的 437 株人源和动物源金黄色葡萄球菌之间的基因组差异。
多位点序列分型显示存在 75 种先前确定的序列类型（ST）。我们的群体基因组分析揭示了三个主要金黄色葡萄球菌谱系（ST5、ST8、ST30）的辅助基因组内容存在异质性。根据宿主（人类与非人类）和三个主要 ST 之间的不同，与抗生素耐药性、毒力和质粒类型相关的基因在分离株中分布不均。在整个种群中，我们总共鉴定出了 1912 次发生在 765 个基因中的重组事件。同源重组的频率和影响在人源和动物源分离株之间是可比的。无论其宿主身份如何，低频率 ST 都是重组 DNA 的主要供体。最频繁重组的基因（clfB、aroA、sraP）在宿主感染和毒力中发挥作用，这些基因也经常在稀有谱系之间共享。
综上所述，这些结果表明，包括低频谱系在内的循环金黄色葡萄球菌谱系之间频繁但可变的重组模式，跨越宿主屏障，塑造了局部基因库的结构和与宿主相关的遗传变异库。我们的研究为金黄色葡萄球菌在多种宿主物种中定植和引起疾病的遗传和进化因素提供了重要的见解。我们的研究强调了对不同生态宿主小生境中循环金黄色葡萄球菌进行连续监测的重要性，以及从这些小生境中系统采样的必要性。这些发现将为制定有效的措施以控制金黄色葡萄球菌在整个同一健康连续体中的定植、感染和传播提供信息。
