Transcriptional start site turnover in the evolution of bacterial paralogous genes – the pelE‐pelD virulence genes in Dickeya

Abstract

After a gene duplication event, the resulting paralogous genes frequently acquire distinct expression profiles, roles, and/or functions but the underlying mechanisms are poorly understood. While transcription start site (TSS) turnover, i.e., the repositioning of the TSS during evolution, is widespread in eukaryotes, it is less documented in bacteria. Using pelD and pelE, two closely related paralogous genes encoding key virulence factors in Dickeya, a gamma proteobacterial genus of phytopathogens, we show that pelE has been selected as an initiator of bacterial aggression, while pelD acts at a later stage, thanks to modifications in the transcriptional regulation of these two genes. This expression change is linked to a few mutations that caused a shift in the position of the pelETSS and the rapid divergence in the regulation of these genes after their duplication. Genomic surveys detected additional examples of putative turnovers in other bacteria. This first report of TSS shifting in bacteria suggests that this mechanism could play a major role in paralogous genes fixation in prokaryotes.

Common and distinctive adaptive traits expressed in Dickeya dianthicola and Dickeya solani pathogens when exploiting potato plant host

“…While the maceration enzyme arsenal is quite similar in Ddi04.9 and Dso3337, most of the encoded genes were equally or even more expressed in Ddi04.9 than in Dso3337, with the exception of pelE . Interestingly, PelE plays a key role in the initiation of maceration by Dickeya (Duprey et al ., ). This noticeable difference in pelE expression levels could contribute to the stronger capacity of Dso3337 to initiate maceration at a low cell density, as we showed in this work.…”

“…Remarkably, pelE is the unique pel gene that is more expressed in Dso3337 than in Ddi04.9 in tuber colonizing condition and it is also about 10‐fold more expressed in rich medium in Dso3337 than in Ddi04.9. Because this gene plays a key role in the initiation of maceration by Dickeya (Duprey et al ., ), we hypothesized that Dso3337 could more efficiently initiate maceration than Ddi04.9. To test this hypothesis, tubers were infected by a low cell number (2 × 10 4 CFU per tuber), and after 5‐days incubation, the measured symptoms were stronger following Dso3337 infection than that of Ddi04.9.…”

The phytopathogenic nature of Dickeya aquatica 174/2 and the dynamic early evolution of Dickeya pathogenicity

“…S2), suggesting that strain ATCC 39006 represents the sisterlineage of Dickeya, and was wrongly affiliated to the Serratia, based on its capacity to synthesize prodigiosin, a red pigment secondary metabolite with antimicrobial, anticancer and immunosuppressant properties, characteristic of Serratia species (Thomson et al, 2000). The sisterrelationship of ATCC 39006 and Dickeya is consistent with the close evolutionary link between the pectinolytic gene clusters (pel, paeY and pemA) shared by these taxa (Duprey et al, 2016b), and with the presence, in Serratia sp. ATCC 39006, of an homologue of the Vfm quorum sensing system previously reported as specific to Dickeya species (Supporting Information Table S4 and Fig.…”

“…According to their taxonomic distribution and phylogeny, most of these proteins could be inferred in the ancestor of Dickeya and in its sister lineage P. confusarubida . Regarding the pelAED cluster, while P. confusarubida has a single gene, the ancestor of Dickeya had two copies, pelA and an undifferentiated pelDE pectate lyase‐coding gene (Duprey et al ., ), suggesting that a duplication event occurred in the stem of Dickeya . This undifferentiated pelDE has undergone a duplication event after the emergence of D. paradisiaca , giving rise to pelD and pelE (Supporting Information Fig.…”

The diguanylate cyclase GcpA inhibits the production of pectate lyases via the H‐NS protein and RsmB regulatory RNA in Dickeya dadantii

“…1D, 1E and 1F). A recent study demonstrated that the transcriptional start site shift after gene duplication might be one of the reasons for the different expression patterns of pelD and pelE (Duprey et al , 2016). However, the upstream regulatory mechanism remains unclear.…”