Yang Linghuan, Samut Hilal, Kemmerling Leonie, Orsi Renato Hohl, Wiedmann Martin, Chen Ruixi, Resendiz-Moctezuma Cristina
Department of Food Science, Cornell University, Ithaca, NY, United States.
Front Microbiol. 2025 Jun 13;16:1547190. doi: 10.3389/fmicb.2025.1547190. eCollection 2025.
Despite the emergence of whole genome sequencing (WGS) for characterization, serotype assignment remains important as it allows identification of subgroups that differ in distribution, virulence, and ecology. However, it has been shown that multiple divergent lineages of the same serovar may have evolved independently multiple times and may present distinct epidemiological characteristics. Previous studies that aimed to identify the phylogeny of certain serovars often used isolates from specific geographical locations or outbreaks and a small number of isolates to infer the phylogeny. To address these limitations and to advance the understanding of 's evolutionary patterns, we (i) identified the phylogenetic grouping (i.e., mono-, para-, or polyphyly) of the 100 most common serovars analyzing 63,204 genomes available in the NCBI Pathogen Detection database, (ii) identified, for each polyphyletic serovar, the lineages that contain the majority of genomes, and (iii) inferred the antigen divergence between the five most common serovars (i.e., Enteritidis, Typhimurium, Newport, I 4,[5],12:i:-, and Infantis) and their respective closely-related serovars. Among the 100 most common serovars analyzed, 19 serovars are monophyletic, nine are paraphyletic, and 72 are polyphyletic. In 47 of the 72 polyphyletic serovars, one lineage contains more than 90% of the serovar's confirmed genomes. Antigen divergence results suggest that serovars Typhimurium and I 4,[5],12:i:- (often referred to as monophasic Typhimurium) have emerged independently of each other multiple times, except for the major I 4,[5],12:i:- lineage, which emerged from the major Typhimurium lineage. Furthermore, divergence in serovars appears to primarily occur through modifications in the H1 antigen. Hence, this study shows that (i) a much larger number of serovars than previously known are polyphyletic; (ii) serovars previously known to be polyphyletic contain more lineages than previously known; and (iii) many serovars include lineages that only have a few isolates with a given serovar. Our data suggests that, in the age of genomics, molecular serotyping should be combined with other phylogenetically informative approaches to not just assign a serovar but to also indicate the serovar lineage for polyphyletic and paraphyletic serovars.
尽管全基因组测序（WGS）已出现用于特征描述，但血清型分型仍然很重要，因为它能够识别在分布、毒力和生态方面存在差异的亚群。然而，研究表明，同一血清型的多个不同谱系可能已多次独立进化，并且可能呈现出不同的流行病学特征。以往旨在确定某些血清型系统发育的研究通常使用来自特定地理位置或疫情的分离株以及少量分离株来推断系统发育。为了解决这些局限性并增进对[血清型]进化模式的理解，我们：（i）通过分析NCBI病原体检测数据库中可用的63204个基因组，确定了100种最常见血清型的系统发育分组（即单系、并系或多系）；（ii）对于每种多系血清型，确定了包含大多数基因组的谱系；（iii）推断了五种最常见血清型（即肠炎沙门氏菌、鼠伤寒沙门氏菌、纽波特沙门氏菌、I 4,[5],12:i:-和婴儿沙门氏菌）与其各自密切相关血清型之间的抗原差异。在分析的100种最常见血清型中，19种血清型是单系的，9种是并系的，72种是多系的。在72种多系血清型中的47种中，一个谱系包含该血清型90%以上的已确认基因组。抗原差异结果表明，除了主要的I 4,[5],12:i:-谱系源自主要的鼠伤寒沙门氏菌谱系外，鼠伤寒沙门氏菌和I 4,[5],12:i:-（通常称为单相鼠伤寒沙门氏菌）已多次彼此独立出现。此外，血清型的差异似乎主要通过H1抗原的修饰发生。因此，本研究表明：（i）多系血清型的数量比以前已知的要多得多；（ii）以前已知为多系的血清型包含比以前已知更多的谱系；（iii）许多血清型包括仅含有少数给定血清型分离株的谱系。我们的数据表明，在基因组学时代，分子血清型分型应与其他系统发育信息丰富的方法相结合，不仅要确定血清型，还要为多系和并系血清型指明血清型谱系。
