Horizontally acquired quorum sensing regulators recruited by the PhoP regulatory network expand host-adaptation repertoire in the phytopathogen Pectobacterium carotovorum

In this study, we examine the impact of transcriptional network rearrangements driven by horizontal gene acquisition in PhoP and SlyA regulons using as a case study the phytopathosystem comprised of potato tubers and the soft rot pathogen Pectobacterium carotovorum subsp. brasiliense (Pcb1692). By comparing those two networks with that of PecS obtained from the closely related Dickeya dadantii, we found that: (a) 24-31% of the genes regulated at late infection are genus-specific (GS) (based on Pectobacterium and Dickeya genera), and that (b) of these, 28.1-44.4% were predicted with high confidence as horizontal gene transfer (HGT) candidates. Further, genome simulation and statistical analyses corroborated the bias in late infection regulons towards the transcriptional control of candidate GS-HGT genes by PhoP, SlyA, and PecS, highlighting the prominence of network rearrangements in these late infection regulons. The evidence further supports the circumscription of two horizontally acquired quorum sensing regulators (carR and expR1) by the PhoP network. By recruiting carR and expR1, the PhoP network also impacts certain host adaptation- and bacterial competition-related systems, seemingly in a quorum sensing-dependent manner, such as the type VI secretion system, carbapenem biosynthesis, and plant cell walls degrading enzymes (PCWDE) such as cellulases and pectate lyases. Conversely, polygalacturonases and the type III secretion system (T3SS) exhibit a transcriptional pattern that suggests quorum sensing-independent regulation by the PhoP network. This includes a yet uncharacterized novel phage-related gene family within the T3SS gene cluster that has been recently acquired by two Pectobacterium species. The evidence further suggests a PhoP-dependent regulation of carbapenem and PCWDE-encoding genes based on the synthesized products9 optimum pH. The PhoP network also controls slyA expression in planta, which seems to impact the carbohydrate metabolism regulation, especially at early infection when 69.6% of the SlyA-regulated genes from that category also require PhoP to achieve normal expression levels.