Horizontal transfer of the immunoglobulin A1 protease gene (iga) from Streptococcus to Gemella haemolysans

Abstract

Bacterial IgA1 proteases share the ability to cleave human IgA1 at the hinge region. Nature has developed this trait along at least five independent evolutionary lineages. To obtain further insight into the phylogeny and function of IgA1 proteases, the nucleotide sequence of the iga gene that encodes the IgA1 protease was determined from two Streptococcus mitis strains and one Gemella haemolysans strain. Heterologous expression in Escherichia coli confirmed that the genes encode human IgA1-cleaving activity. IgA1 proteases from Streptococcus and G. haemolysans shared structural features, including a motif typical for zinc-dependent metalloproteases of clan MA(E) family M26 and an N-terminal signal sequence followed by an LPXTG cell-wall-anchor motif and two putative membrane-spanning domains. In addition, they all harboured a repeat region preceding the active site of the protease. In the streptococcal IgA1 proteases, a G5 domain, which has been suggested to bind N-acetylglucosamine, was identified. Conservation of these structures in otherwise diverse proteases suggests that they are essential to the biological function of the enzyme. The phylogenetic distribution of homologous iga genes and conservation of gene order in the iga gene region in different Streptococcus species, combined with the sequence homologies, strongly suggest that the iga gene is more ancient in Streptococcus than in G. haemolysans, and therefore that the IgA1 protease gene was transferred from Streptococcus to G. haemolysans.

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

“…There have been changes in the taxonomic assignment of several mitis group Streptococcus species subsequent to the availability of comparative phylogenetic analyses of core genomes, multilocus sequence analysis (MLSA), and 16S rRNA gene sequence data [23]. In the current study, revised streptococcal taxonomy showed changes in species nomenclature of 25 strains used in phylogenetic analyses.…”

“…(+) ABP, (-) ABP on bacterial cells (Methods) c S. milleri reclassified as S. anginosis in Ruoff et al [48] d Sabharwal et al [22]; strains sequenced for this study e Brown et al [3] f Strain labeled NCTC 10712 ( S. mitis ) in our collection is now corrected to S. gordonii , UB10712 upon whole genome sequencing g Vorrasi et al [16] h The strain from our collection named S. mitis in Brown et al [3] Submitted to GenBank as S. mitis ; updated to S. oralis in 2015 as per reclassification Takenouchi-Ohkubo et al [28] and Kilian et al [49] i Updated taxonomic classifications for Mitis group, Jensen et al [23] j Reference strains used for genome post-assembly: S. cristatus ATCC 51100 for S. cristatus CC5A and CR3; S. gordonii Challis substrain CH1 for S. gordonii G9B; S. mitis B6 for S. mitis OT25, SK145, SK137; S. parasanguinis ATCC 15912 for S. parasanguinis MGH413; S. salivarius CCHSS3 for S. salivarius KB005…”

“…In the current study, revised streptococcal taxonomy showed changes in species nomenclature of 25 strains used in phylogenetic analyses. Briefly, several members of mitis , oligofermentans , pseudopneumoniae , and sanguinis species that represent ABS were revised to other Streptococcus species based on MLSA and whole genome core phylogeny [23]. Taxonomic reassignments are summarized in Additional file 1: Table S1, and updates have also been made to our draft genome submissions [22].…”

“…AbpA subgroups generally correlate with species, although there is evidence of interspecies divergence. For example, within the mitis group of Streptococcus species, the S. oralis clade is more distantly related to the S. parasanguinis clade [23], and both contain strains that carry AbpA-like proteins from a variety of subgroups. This apparent random distribution of the co-transcribed abpA-srtB genes in more distantly related Streptococcus species, the lack of synteny conservation in closely related species, and the presence of an AbpA ortholog in a different genus ( Gemella ) suggests that these genes are part of a genomic island acquired by horizontal gene transfer.…”

Bacterial Modulation of Fc Effector Functions

“…In addition, several bacteria genetically related to these important pathogens produce IgA 1 proteases, reflecting either shared ancestry or, in some cases, horizontal gene transfer. 37,38 The biological significance of IgA 1 proteases is indirectly supported by the fact that they are a striking result of convergent evolution along at least five independent lineages. In spite of virtually identical enzymatic function, IgA 1 proteases of different bacteria belong to all major protease families (i.e., serine proteases, metalloproteases, and thiol proteases).…”