Abstract

BackgroundSialic acids comprise a family of nine-carbon amino sugars that are prevalent in mucus rich environments. Sialic acids from the human host are used by a number of pathogens as an energy source. Here we explore the evolution of the genes involved in the catabolism of sialic acid.ResultsThe cluster of genes encoding the enzymes N-acetylneuraminate lyase (NanA), epimerase (NanE), and kinase (NanK), necessary for the catabolism of sialic acid (the Nan cluster), are confined 46 bacterial species, 42 of which colonize mammals, 33 as pathogens and 9 as gut commensals. We found a putative sialic acid transporter associated with the Nan cluster in most species. We reconstructed the phylogenetic history of the NanA, NanE, and NanK proteins from the 46 species and compared them to the species tree based on 16S rRNA. Within the NanA phylogeny, Gram-negative and Gram-positive bacteria do not form distinct clades. NanA from Yersinia and Vibrio species was most closely related to the NanA clade from eukaryotes. To examine this further, we reconstructed the phylogeny of all NanA homologues in the databases. In this analysis of 83 NanA sequences, Bacteroidetes, a human commensal group formed a distinct clade with Verrucomicrobia, and branched with the Eukaryotes and the Yersinia/Vibrio clades. We speculate that pathogens such as V. cholerae may have acquired NanA from a commensal aiding their colonization of the human gut. Both the NanE and NanK phylogenies more closely represented the species tree but numerous incidences of incongruence are noted. We confirmed the predicted function of the sialic acid catabolism cluster in members the major intestinal pathogens Salmonella enterica, Vibrio cholerae, V. vulnificus, Yersinia enterocolitica and Y. pestis.ConclusionThe Nan cluster among bacteria is confined to human pathogens and commensals conferring them the ability to utilize a ubiquitous carbon source in mucus rich surfaces of the human body. The Nan region shows a mosaic evolution with NanA from Bacteroidetes, Vibrio and Yersinia branching closely together with NanA from eukaryotes.

Highlights

  • Sialic acids comprise a family of nine-carbon amino sugars that are prevalent in mucus rich environments

  • We considered three genes to form a Nan cluster if: 1) they were the best matches in BLAST for N-acetylneuraminic lyase (NanA), NanK since the epimerase (NanE), and N-acetylmannosamine kinase (NanK) from V. cholerae N16961; 2) reciprocal BLAST searches of the three genes against the V. cholerae N16961 genome hit on V. cholerae N16961 NanA, NanE, and NanK; 3) the same applied when performing BLAST search using NanA, NanK, and NanE from S. aureus N315; 4) the three genes were encoded and within 10 ORFs of each other

  • Clostridium botulinum is the causative agent of botulism, Haemophilus influenzae is a major cause of lower respiratory infections and meningitis in children, Streptococcus pneumoniae causes pneumonia, and Yersinia pestis is the agent of plague

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Summary

Introduction

Sialic acids comprise a family of nine-carbon amino sugars that are prevalent in mucus rich environments. Sialic acids from the human host are used by a number of pathogens as an energy source. Sialic acid or neuraminic acid, is the designation of a family that encompasses over 50 naturally occurring and structurally distinct nine-carbon amino sugars found both in the Eukaryotes and Prokaryotes, being the only ninecarbon sugar known to date in the latter [1]. Both names, sialic acid and neuraminic acid, indicate the source of the molecules from which they were first discovered: sialic,. Sialic acids are found in Fungi and some protozoa, the latter likely can only scavenge them from the host [11,12,13]

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