Major distinctions between the two oligopeptide permease systems of Bacillus subtilis with respect to signaling, development and evolutionary divergence

Abstract

Oligopeptide-permeases (Opps) are used by bacteria to import short peptides. In addition to their metabolic benefit, imported short peptides are used in many Gram-positive bacteria as signalling molecules of the RRNPP super-family of quorum-sensing systems, making Opps an integral part of cell–cell communication. In some Gram-positive bacteria there exist multiple Opps and the relative importance of those to RRNPP quorum sensing are not fully clear. Specifically, in Bacillus subtilis , the Gram-positive model species, there exist two homologous oligopeptide permeases named Opp and App. Previous work showed that the App system is mutated in lab strain 168 and its recovery partially complements an Opp mutation for several developmental processes. Yet, the nature of the impact of App on signalling and development in wild-type strains, where both permeases are active was not studied. Here we re-examine the impact of the two permease systems. We find that App has a minor contribution to biofilm formation, surfactin production and phage infection compared to the effect of Opp. This reduced effect is also reflected in its lower ability to import the signals of four different Rap-Phr RRNPP systems. Further analysis of the App system revealed that, unlike Opp, some App genes have undergone horizontal transfer, resulting in two distinct divergent alleles of this system in B. subtilis strains. We found that both alleles were substantially better adapted than the Opp system to import an exogenous RRNPP signal of the Bacillus cereus group PlcR-PapR system. In summary, we find that the App system has only a minor role in signalling but may still be crucial for the import of other peptides.