Distribution and Evolutionary History of Sialic Acid Catabolism in the Phylum Actinobacteria

Microbiol Spectr. 2022 Jan 12;e0238021. doi: 10.1128/spectrum.02380-21. Online ahead of print.

Abstract

Sialic acids are present in humans and other metazoans, playing essential roles in physiological and pathological processes. Commensal and pathogenic bacteria have evolved the capacity to utilize sialic acids as nutrient and energy sources. However, in some actinobacteria, sialic acid catabolism (SAC) is associated with free-living populations. To unravel the distribution and evolutionary history of SAC in the phylum Actinobacteria, we analyzed the presence and diversity of the putative SAC gene cluster (nan) in 7,180 high-quality, nonredundant actinobacterial genomes that covered 1,969 species. The results showed that ∼13% of actinobacterial species had the potential to utilize sialic acids, with 45 species capable of anhydro-SAC, all except two of them through the canonical pathway. These species belonged to 20 orders and 81 genera, with ∼36% of them from four genera, Actinomyces, Bifidobacterium, Corynebacterium, and Streptomyces. Moreover, ∼40% of the nan-positive species are free living. Phylogenetic analysis of the key nan genes, nanA, nanK, and nanE, revealed a strong signal of horizontal gene transfer (HGT), accompanied with vertical inheritance and gene loss. This evolutionary pattern led to high diversity and differential distribution of nan among actinobacterial taxa and might cause the cluster to spread to some free-living species while losing in some host-associated species. The evolution of SAC in actinobacteria probably represents the evolution of certain kinds of noncore bacterial functions for environmental adaptation and lifestyle switch, in which HGT plays a dominant role. IMPORTANCE Sialic acids play essential roles in the physiology of humans and other metazoan animals, and microbial sialic acid catabolism (SAC) is one of the processes critical for pathogenesis. To date, microbial SAC is studied mainly in commensals and pathogens, while its distribution in free-living microbes and evolutionary pathway remain largely unexplored. Here, by examining all actinobacterial genomes available, we demonstrate that putative SAC is present in a small proportion of actinobacterial species, of which, however, ∼40% are free-living species. We also reveal remarkable difference in the distribution of SAC among actinobacterial taxa and high diversity of the putative SAC gene clusters. HGT plays a significant role in the evolution of SAC, accompanied with vertical inheritance and gene loss. Our results provide a comprehensive and systematic picture of the distribution and evolutionary history of SAC in actinobacteria, expanding the current knowledge on bacterial adaptation and diversification.

Keywords: Actinobacteria; distribution; environmental adaptation; evolution; free-living species; horizontal gene transfer; sialic acid catabolism.