Diversity and Evolution of Bacterial Twin Arginine Translocase Protein, TatC, Reveals a Protein Secretion System That Is Evolving to Fit Its Environmental Niche

Abstract

BackgroundThe twin-arginine translocation (Tat) protein export system enables the transport of fully folded proteins across a membrane. This system is composed of two integral membrane proteins belonging to TatA and TatC protein families and in some systems a third component, TatB, a homolog of TatA. TatC participates in substrate protein recognition through its interaction with a twin arginine leader peptide sequence.Methodology/Principal FindingsThe aim of this study was to explore TatC diversity, evolution and sequence conservation in bacteria to identify how TatC is evolving and diversifying in various bacterial phyla. Surveying bacterial genomes revealed that 77% of all species possess one or more tatC loci and half of these classes possessed only tatC and tatA genes. Phylogenetic analysis of diverse TatC homologues showed that they were primarily inherited but identified a small subset of taxonomically unrelated bacteria that exhibited evidence supporting lateral gene transfer within an ecological niche. Examination of bacilli tatCd/tatCy isoform operons identified a number of known and potentially new Tat substrate genes based on their frequent association to tatC loci. Evolutionary analysis of these Bacilli isoforms determined that TatCy was the progenitor of TatCd. A bacterial TatC consensus sequence was determined and highlighted conserved and variable regions within a three dimensional model of the Escherichia coli TatC protein. Comparative analysis between the TatC consensus sequence and Bacilli TatCd/y isoform consensus sequences revealed unique sites that may contribute to isoform substrate specificity or make TatA specific contacts. Synonymous to non-synonymous nucleotide substitution analyses of bacterial tatC homologues determined that tatC sequence variation differs dramatically between various classes and suggests TatC specialization in these species.Conclusions/SignificanceTatC proteins appear to be diversifying within particular bacterial classes and its specialization may be driven by the substrates it transports and the environment of its host.

Tle distribution and diversity in metagenomic datasets reveal niche specialization

“…Moreover, the differential abundance of Tle families within certain niches as well as the presence of different Tle families within the same genomes suggests that there is specialization of the various Tle families. Indeed, a recent report identified niche specialization of the twin‐arginine translocation system, with different levels of selective pressure on the TatC protein, which were focused on certain positions in the protein, evident in different strains (Simone et al ., ). This suggests that these phenomena may be more widespread generally among bacterial secretion systems.…”

Structural features of the TatC membrane protein that determine docking and insertion of a twin-arginine signal peptide

“…The DCCD-sensitive residue Glu 170 of TatC is highly conserved among bacterial TatCs (42). Mutational replacement of this glutamate residue impairs Tat-specific transport but does not eliminate it (22,41,43).…”

Compartmentalization of the Carbaryl Degradation Pathway: Molecular Characterization of Inducible Periplasmic Carbaryl Hydrolase from Pseudomonas spp

“…Secretory proteins are generally known to be translocated to the periplasm via either TAT (twin arginine translocation) or Sec (secretory) pathway. Proteins translocated via the TAT pathway have a conserved twin-arginine motif, are translocated in their folded forms, and predominantly require a cofactor for their activity (35,36). In the Sec pathway, proteins are transported in their unfolded state (35).…”