Comparative genomics and evolution of the amylase-binding proteins of oral streptococci

Abstract

BackgroundSuccessful commensal bacteria have evolved to maintain colonization in challenging environments. The oral viridans streptococci are pioneer colonizers of dental plaque biofilm. Some of these bacteria have adapted to life in the oral cavity by binding salivary α-amylase, which hydrolyzes dietary starch, thus providing a source of nutrition. Oral streptococcal species bind α-amylase by expressing a variety of amylase-binding proteins (ABPs). Here we determine the genotypic basis of amylase binding where proteins of diverse size and function share a common phenotype.ResultsABPs were detected in culture supernatants of 27 of 59 strains representing 13 oral Streptococcus species screened using the amylase-ligand binding assay. N-terminal sequences from ABPs of diverse size were obtained from 18 strains representing six oral streptococcal species. Genome sequencing and BLAST searches using N-terminal sequences, protein size, and key words identified the gene associated with each ABP. Among the sequenced ABPs, 14 matched amylase-binding protein A (AbpA), 6 matched amylase-binding protein B (AbpB), and 11 unique ABPs were identified as peptidoglycan-binding, glutamine ABC-type transporter, hypothetical, or choline-binding proteins. Alignment and phylogenetic analyses performed to ascertain evolutionary relationships revealed that ABPs cluster into at least six distinct, unrelated families (AbpA, AbpB, and four novel ABPs) with no phylogenetic evidence that one group evolved from another, and no single ancestral gene found within each group. AbpA-like sequences can be divided into five subgroups based on the N-terminal sequences. Comparative genomics focusing on the abpA gene locus provides evidence of horizontal gene transfer.ConclusionThe acquisition of an ABP by oral streptococci provides an interesting example of adaptive evolution.Electronic supplementary materialThe online version of this article (doi:10.1186/s12866-017-1005-7) contains supplementary material, which is available to authorized users.

Polymicrobial communities in periodontal disease: Their quasi‐organismal nature and dialogue with the host

“…12,13 Streptococcal adhesins can be fimbrial components (eg, cell-surface hydrophobicity protein A in Streptococcus gordonii and fimbria-associated protein-1 in Streptococcus parasanguinis) and surface structural proteins, such as the conserved antigen I/II family or the amylase-binding proteins A and B. [14][15][16] The latter example highlights a recurring theme in oral bacterial ecology, namely, an association between binding and nutrition. Starch degradation by amylase will produce glucose and maltodextrins in close proximity to bacterial cells, which can then be transported into the bacteria as a source of energy.…”

“…Indeed, successful oral colonizers often possess a multiplicity of adhesins with a variety of specificities, a configuration which both increases the range of available substrates and the affinity of binding 12,13 . Streptococcal adhesins can be fimbrial components (eg, cell‐surface hydrophobicity protein A in Streptococcus gordonii and fimbria‐associated protein‐1 in Streptococcus parasanguinis ) and surface structural proteins, such as the conserved antigen I/II family or the amylase‐binding proteins A and B 14‐16 . The latter example highlights a recurring theme in oral bacterial ecology, namely, an association between binding and nutrition.…”

Amylases: Biofilm Inducer or Biofilm Inhibitor?

“…Amylase-binding Streptococci (ABS) express different proteins ranging from 20-87 kDa which bind salivary a-amylase in vitro ( Gwynn and Douglas, 1994 ; Brown et al., 1999 ; Haase et al., 2017 ). The heterogeneity of these proteins varies from species to species with some expressing more than one ABP.…”

“…The functional significance of amylase binding proteins in oral colonization by Streptococci is important for understanding how salivary components influence oral biofilm formation by these important dental-plaque species. Therefore, the question is raised of whether amylase assists in the formation of dental biofilm or, paradoxically, it can be used as a biofilm inhibitor ( Haase et al., 2017 ; Wu et al., 2020 ). Amylase seems to be useful for removing biofilm by disintegrating the carbohydrate moiety of the biofilm matrices, but at the same time it can also induce biofilm formation.…”

Erratum to: comparative genomics and evolution of the amylase-binding proteins of oral streptococci

“…Upon publication of the original article [ 1 ] discrepancies were highlighted in the references of this manuscript. On page 11, the references in the following sentence should be amended “Homologs are now found in many oral streptococcal species of humans and animals whose saliva contains amylase activity [32, 33].” Citation 33 should read 34 and was incorrectly amended during the proofing process.…”