Identification of a novel pentatricopeptide repeat subfamily with a C-terminal domain of bacterial origin acquired via ancient horizontal gene transfer

BACKGROUND: Pentatricopeptide repeat (PPR) proteins are a large family of sequence-specific RNA binding proteins involved in organelle RNA metabolism. Very little is known about the origin and evolution of these proteins, particularly outside of plants. Here, we report the identification of a novel subfamily of PPR proteins not found in plants and explore their evolution. RESULTS: We identified a novel subfamily of PPR proteins, which all contain a C-terminal tRNA guanine methyltransferase (TGM) domain, suggesting a predicted function not previously associated with PPR proteins. This group of proteins, which we have named the PPR-TGM subfamily, is found in distantly related eukaryotic lineages including cellular slime moulds, entamoebae, algae and diatoms, but appears to be the first PPR subfamily absent from plants. Each PPR-TGM protein identified is predicted to have different subcellular locations, thus we propose that these proteins have roles in tRNA metabolism in all subcellular locations, not just organelles. We demonstrate that the TGM domain is not only similar to bacterial TGM proteins, but that it is most similar to chlamydial TGMs in particular, despite the absence of PPR proteins in bacteria. Based on our data, we postulate that this subfamily of PPR proteins evolved from a TGM-encoding gene of a member of the Chlamydiae, which was obtained via ancient prokaryote-to-eukaryote horizontal gene transfer. Following its acquisition, the N-terminus of the encoded TGM protein must have been extended to include PPR motifs, possibly to confer additional functions to the protein, giving rise to the PPR-TGM subfamily. CONCLUSIONS: The identification of a unique PPR subfamily which originated from the Chlamydiae group of bacteria offers novel insight into the origin and evolution of PPR proteins not previously considered. It also provides further understanding into their roles in non-organellar RNA metabolism.