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Multiple evolutionary origins reflect the importance of sialic acid transporters in the colonization potential of bacterial pathogens and commensals

Lookup NU author(s): Dr Emmanuele SeveriORCiD, Professor Tracy Palmer FRS FRSE FMedSciORCiD

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This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License (CC BY-NC 4.0).


Abstract

Located at the tip of cell surface glycoconjugates, sialic acids are at the forefront of host-microbe interactions and, being easily liberated by sialidase enzymes, are used as metabolites by numerous bacteria, particularly by pathogens and commensals living on or near diverse mucosal surfaces. These bacteria rely on specific transporters for the acquisition of host-derived sialic acids. Here, we present the first comprehensive genomic and phylogenetic analysis of bacterial sialic acid transporters, leading to the identification of multiple new families and subfamilies. Our phylogenetic analysis suggests that sialic acid-specific transport has evolved independently at least 8 times during the evolution of bacteria, from within 4 of the major families/superfamilies of bacterial transporters, and we propose a robust classification scheme to bring together a myriad of different nomenclatures that exist to date. The new transporters discovered occur in diverse bacteria including Spirochaetes, Bacteroidetes, Planctomycetes, and Verrucomicrobia, many of which are species that have not been previously recognised to have sialometabolic capacities. Two subfamilies of transporters stand out in being fused to the sialic acid mutarotase enzyme, NanM, and these transporter fusions are enriched in bacteria present in gut microbial communities. Our analysis supports the increasing experimental evidence that competition for host-derived sialic acid is a key phenotype for successful colonisation of complex mucosal microbiomes, such that a strong evolutionary selection has occurred for the emergence of sialic acid specificity within existing transporter architectures.


Publication metadata

Author(s): Severi E, Rudden M, Bell A, Palmer T, Juge N, Thomas GH

Publication type: Article

Publication status: Published

Journal: Microbial Genomics

Year: 2021

Volume: 7

Issue: 6

Online publication date: 29/06/2021

Acceptance date: 20/05/2021

Date deposited: 21/05/2021

ISSN (electronic): 2057-5858

Publisher: The Microbiology Society

URL: https://doi.org/10.1099/mgen.0.000614

DOI: 10.1099/mgen.0.000614

PubMed id: 34184979


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Funding

Funder referenceFunder name
BB/P008895/1
BBSRC
BB/R012490/1

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