An epigenetic switch activates bacterial quorum sensing and horizontal transfer of an integrative and conjugative element

Abstract

Horizontal transfer of the integrative and conjugative element ICEMlSymR7A converts non-symbiotic Mesorhizobium spp. into nitrogen-fixing legume symbionts. Here, we discover subpopulations of Mesorhizobium japonicum R7A become epigenetically primed for quorum-sensing (QS) and QS-activated horizontal transfer. Isolated populations in this state termed R7A* maintained these phenotypes in laboratory culture but did not transfer the R7A* state to recipients of ICEMlSymR7A following conjugation. We previously demonstrated ICEMlSymR7A transfer and QS are repressed by the antiactivator QseM in R7A populations and that the adjacently-coded DNA-binding protein QseC represses qseM transcription. Here RNA-sequencing revealed qseM expression was repressed in R7A* cells and that RNA antisense to qseC was abundant in R7A but not R7A*. Deletion of the antisense-qseC promoter converted cells into an R7A*-like state. An adjacently coded QseC2 protein bound two operator sites and repressed antisense-qseC transcription. Plasmid overexpression of QseC2 stimulated the R7A* state, which persisted following curing of this plasmid. The epigenetic maintenance of the R7A* state required ICEMlSymR7A-encoded copies of both qseC and qseC2. Therefore, QseC and QseC2, together with their DNA-binding sites and overlapping promoters, form a stable epigenetic switch that establishes binary control over qseM transcription and primes a subpopulation of R7A cells for QS and horizontal transfer.

Population genomics of Australian indigenous Mesorhizobium reveals diverse nonsymbiotic genospecies capable of nitrogen-fixing symbioses following horizontal gene transfer

“…Genome extractions for Oxford Nanopore Technologies MinION and PacBio RSII sequencing were performed as previously described [ 47 ]. For assembly of complete genomes with MiniION or PacBio reads, long-reads alone were first assembled with Flye 2.7.1 [ 48 ] and then assemblies were polished with Illumina reads as previously described [ 49 ]. Genome extractions for Illumina NextSeq sequencing were performed with FavorPrep Tissue Genomic DNA Extraction Mini Kit (Favorgen).…”

“…ICE Ml Sym R7A was conjugated from strain R7A* as in [ 49 ]. Briefly, donor and recipient strains were mixed and spotted on a TY agar plate and incubated at 28 °C for 24 h. Exconjugants were selected on G/RDM containing tetracycline (50 µg ml −1 ) or neomycin (200 µg ml −1 ), without supplemented nicotinate, biotin or thiamine.…”

Construction of microbial consortia for microbial degradation of complex compounds

“…QS primarily regulates collective features that involve energetically costly “public goods” and are most effective or even only functional if performed by a microbial consortium. Bacterial traits controlled by QS include genetic phenotypes, biofilm formation, promoting or inhibiting function, and virulence ( Mashruwala et al, 2022 ; Pütz et al, 2022 ; Ramsay et al, 2022 ). QS even can be a driver and target of other functions ( Striednig and Hilbi, 2022 ).…”

Gold mining nature for natural products

“…Quorum sensing (QS) is the communication mechanism among bacteria communities to control environmental aspects across a community, such as formation and maintenance of biofilms, expression of virulence factors, and production of secondary metabolites. Finally, epigenetic modification of gene expression plays a key role in responding to environmental cues by suppressing or turning on relevant genes, and as such is another potential target for seeking secondary metabolites (Ramsay et al , 2022).…”