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The twin-arginine translocation (Tat) pathway exports fully folded proteins out of the cytoplasm of Gram-negative and Gram-positive bacteria. Although much progress has been made in unraveling the molecular mechanism and biochemical characterization of the Tat system, little is known concerning its functionality and biological role to confer adaptive skills, symbiosis or pathogenesis in the α-proteobacteria class. A comparative genomic analysis in the α-proteobacteria class confirmed the presence of  tatA ,  tatB , and  tatC  genes in almost all genomes, but significant variations in gene synteny and rearrangements were found in the order Rickettsiales with respect to the typically described operon organization. Transcription of  tat  genes was confirmed for  Anaplasma marginale str. St. Maries  and  Brucella abortus  2308, two α-proteobacteria with full and partial intracellular lifestyles, respectively. The tat genes of  A. marginale  are scattered throughout the genome, in contrast to the more generalized operon organization. Particularly,  tatA  showed an approximately 20-fold increase in mRNA levels relative to  tatB  and  tatC . We showed Tat functionality in  B. abortus  2308 for the first time, and confirmed conservation of functionality in  A. marginale . We present the first experimental description of the Tat system in the  Anaplasmataceae  and  Brucellaceae  families. In particular, in  A. marginale  Tat functionality is conserved despite operon splitting as a consequence of genome rearrangements. Further studies will be required to understand how the proper stoichiometry of the Tat protein complex and its biological role are achieved. In addition, the predicted substrates might be the evidence of role of the Tat translocation system in the transition process from a free-living to a parasitic lifestyle in these α-proteobacteria.

The Twin-Arginine Translocation Pathway in α-Proteobacteria Is Functionally Preserved Irrespective of Genomic and Regulatory Divergence