Abstract
A multipartite genome organization with a chromosome and many extrachromosomal replicons (ECRs) is characteristic for Alphaproteobacteria. The best investigated ECRs of terrestrial rhizobia are the symbiotic plasmids for legume root nodulation and the tumor-inducing (Ti) plasmid of Agrobacterium tumefaciens. RepABC plasmids represent the most abundant alphaproteobacterial replicon type. The currently known homologous replication modules of rhizobia and Rhodobacteraceae are phylogenetically distinct. In this study, we surveyed type-strain genomes from the One Thousand Microbial Genomes (KMG-I) project and identified a roseobacter-specific RepABC-type operon in the draft genome of the marine rhizobium Martelella mediterranea DSM 17316T. PacBio genome sequencing demonstrated the presence of three circular ECRs with sizes of 593, 259, and 170-kb. The rhodobacteral RepABC module is located together with a rhizobial equivalent on the intermediate sized plasmid pMM259, which likely originated in the fusion of a pre-existing rhizobial ECR with a conjugated roseobacter plasmid. Further evidence for horizontal gene transfer (HGT) is given by the presence of a roseobacter-specific type IV secretion system on the 259-kb plasmid and the rhodobacteracean origin of 62% of the genes on this plasmid. Functionality tests documented that the genuine rhizobial RepABC module from the Martelella 259-kb plasmid is only maintained in A. tumefaciens C58 (Rhizobiaceae) but not in Phaeobacter inhibens DSM 17395 (Rhodobacteraceae). Unexpectedly, the roseobacter-like replication system is functional and stably maintained in both host strains, thus providing evidence for a broader host range than previously proposed. In conclusion, pMM259 is the first example of a natural plasmid that likely mediates genetic exchange between roseobacters and rhizobia.
Highlights
RepABC-type plasmids play a crucial role for the multipartite genome organization and the lifestyle of rhizobia (Pappas and Cevallos, 2011)
The discoveries of the current study benefit from the Genomic Encyclopedia of Bacteria and Archaea (GEBA) genome sequencing project, which was aimed to fill phylogenetic gaps in the tree of life (Wu et al, 2009; Mukherjee et al, 2017), and the follow-up study of one thousand microbial genomes (KMG-I) that was focused on type strains (Kyrpides et al, 2014)
BLASTP searches with the RepC-2 replicase of the 126-kb RepABC plasmid from Dinoroseobacter shibae DFL12T allowed us to identify typical rhizobial homologs with a moderate protein identity of up to 40%, which is exemplified by the Tiplasmid of A. tumefaciens C58 (36% identity)
Summary
RepABC-type plasmids play a crucial role for the multipartite genome organization and the lifestyle of rhizobia (Pappas and Cevallos, 2011). The supposed ecological separation between the soil and the ocean, which would limit the physical contact for conjugation, is less pronounced than a priori assumed Several rhizobial lineages, such as the genus Martelella are adapted to saline habitats (Rivas et al, 2005) and roseobacters represent a paraphyletic group associated with non-marine Rhodobacteraceae including the genus Paracoccus (Simon et al, 2017). In the current study we experimentally document that rhizobial RepABC plasmids do not replicate in Phaeobacter inhibens DSM 17395 (Rhodobacteraceae), but we provide the first example of a natural plasmid that can be stably maintained in both rhizobia and roseobacters This composite plasmid from the marine rhizobium Martelella mediterranea DSM 17316T originated from a plasmid fusion and still harbors rhizobial and rhodobacteral RepABC cassettes overcoming the limits of their host range
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