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The Composite 259-Kb Plasmid of Martelella Mediterranea DSM 17316T–A Natural Replicon with Functional Repabc Modules from Rhodobacteraceae and Rhizobiaceae

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The Composite 259-Kb Plasmid of Martelella Mediterranea DSM 17316T–A Natural Replicon with Functional Repabc Modules from Rhodobacteraceae and Rhizobiaceae ORIGINAL RESEARCH published: 21 September 2017 doi: 10.3389/fmicb.2017.01787 The Composite 259-kb Plasmid of Martelella mediterranea DSM 17316T–A Natural Replicon with Functional RepABC Modules from Rhodobacteraceae and Rhizobiaceae Pascal Bartling, Henner Brinkmann, Boyke Bunk, Jörg Overmann, Markus Göker and Jörn Petersen* Leibniz-Institute DSMZ–German Collection of Microorganisms and Cell Cultures, Braunschweig, Germany Edited by: A multipartite genome organization with a chromosome and many extrachromosomal Bernd Wemheuer, University of New South Wales, replicons (ECRs) is characteristic for Alphaproteobacteria. The best investigated ECRs Australia of terrestrial rhizobia are the symbiotic plasmids for legume root nodulation and the Reviewed by: tumor-inducing (Ti) plasmid of Agrobacterium tumefaciens. RepABC plasmids represent William Martin, University of Dusseldorf Medical the most abundant alphaproteobacterial replicon type. The currently known homologous School, Germany replication modules of rhizobia and Rhodobacteraceae are phylogenetically distinct. Andrew W. B. Johnston, In this study, we surveyed type-strain genomes from the One Thousand Microbial University of East Anglia, United Kingdom Genomes (KMG-I) project and identified a roseobacter-specific RepABC-type operon T *Correspondence: in the draft genome of the marine rhizobium Martelella mediterranea DSM 17316 . Jörn Petersen PacBio genome sequencing demonstrated the presence of three circular ECRs with [email protected] sizes of 593, 259, and 170-kb. The rhodobacteral RepABC module is located together Specialty section: with a rhizobial equivalent on the intermediate sized plasmid pMM259, which likely This article was submitted to originated in the fusion of a pre-existing rhizobial ECR with a conjugated roseobacter Aquatic Microbiology, a section of the journal plasmid. Further evidence for horizontal gene transfer (HGT) is given by the presence Frontiers in Microbiology of a roseobacter-specific type IV secretion system on the 259-kb plasmid and the Received: 22 March 2017 rhodobacteracean origin of 62% of the genes on this plasmid. Functionality tests Accepted: 05 September 2017 documented that the genuine rhizobial RepABC module from the Martelella 259-kb Published: 21 September 2017 plasmid is only maintained in A. tumefaciens C58 (Rhizobiaceae) but not in Phaeobacter Citation: Bartling P, Brinkmann H, Bunk B, inhibens DSM 17395 (Rhodobacteraceae). Unexpectedly, the roseobacter-like replication Overmann J, Göker M and Petersen J system is functional and stably maintained in both host strains, thus providing evidence (2017) The Composite 259-kb for a broader host range than previously proposed. In conclusion, pMM259 is the Plasmid of Martelella mediterranea DSM 17316T–A Natural Replicon with first example of a natural plasmid that likely mediates genetic exchange between Functional RepABC Modules from roseobacters and rhizobia. Rhodobacteraceae and Rhizobiaceae. Front. Microbiol. 8:1787. Keywords: RepABC-type plasmids, compatibility, type IV secretion systems, plasmid fusion, comparative doi: 10.3389/fmicb.2017.01787 genomics, horizontal gene transfer Frontiers in Microbiology | www.frontiersin.org 1 September 2017 | Volume 8 | Article 1787 Bartling et al. The Composite 259-kb Plasmid of Martelella INTRODUCTION genetically engineered and serve as crucial tools for molecular biology (see e.g., Kovach et al., 1995). RepABC-type plasmids play a crucial role for the multipartite Conjugative plasmid transfer is an important factor in genome organization and the lifestyle of rhizobia (Pappas and the evolution of rhizobia (Ding and Hynes, 2009; López- Cevallos, 2011). Long-known examples are the pathogenic Guerrero et al., 2012) and has been proposed as the major tumor-inducing (Ti) plasmid of Agrobacterium tumefaciens driving force for the rapid adaptation of roseobacters to novel and the symbiotic nodulation (pSym) plasmids of the genus ecological niches (Petersen et al., 2013). In nitrogen-fixing Rhizobium. RepABC-type plasmids comprise up to 50% rhizobia, symbiotic plasmids mediate legume root nodulation of the rhizobial genome and represent the by far most and define the particular plant host (Perret et al., 2000; abundant replicon type of these soil bacteria (Pappas and Gibson et al., 2008). The pSym plasmid has been horizontally Cevallos, 2011). Rhizobium etli CFN42 harbors eight RepABC exchanged between different sympatric Rhizobium species, operons that are located on six extrachromosomal replicons thereby transferring the capacity to nodulate the same host (ECRs; González et al., 2006). The relevance of ECRs for the cell, i.e., the common bean Phaseolus vulgaris (Pérez Carrascal marine roseobacter group (Rhodobacterceae) is exemplified et al., 2016). Comparative genome analyses of Rhodobacteraceae by photosynthesis, flagellar and biofilm plasmids (Petersen showed that T4S systems for plasmid mobilization are typically et al., 2012; Michael et al., 2016). Roseobacters contains located on RepABC plasmids, and experimental conjugation of at least four different plasmid types (RepA, RepB, DnaA- natural plasmids has recently become feasible (Patzelt et al., like, RepABC) with more than 20 compatibility groups 2016). The wealth of more than 400 draft genomes allowed (Petersen, 2011). Nine different compatibility groups of tracing natural plasmid transfer among genus barriers in RepABC-type plasmids, which can stably coexist in the same the roseobacter group (Petersen and Wagner-Döbler, 2017). cell, have been identified in this lineage (Petersen et al., However, the recombination rate between bacteria exponentially 2009). drops with increasing sequence divergence (Fraser et al., 2007), RepABC modules are specific for Alphaproteobacteria and which depends, e.g., on the limited host range of mobilizable contain three genes, the repA and repB partitioning genes plasmids. as well as the replication gene repC, which are arranged in One purpose of the current study was the experimental a characteristic operon (Pinto et al., 2012). The structure of validation of our in silico prediction that RepABC-type RepABC type plasmids coincides with the localization of the plasmids can not be transferred stably between Rhizobiaceae origin of replication (ori) within the protein coding part of the and Rhodobacteraceae. They are equivalent in structure and replicase (repC) and the presence of a regulatory antisense RNA function but can clearly be distinguished by phylogenetic between repB and repC (Weaver, 2007). Conserved palindromes analyses (Petersen et al., 2009). Eight RepABC compatibility of RepABC-type plasmids that serve as cis-acting anchors for groups from roseobacters (Rhodobacteraceae) have a common RepB proteins are indispensable for the successful partitioning origin and were once recruited from a rhizobial donor, but of these low copy number replicons. The RepA/RepB system the respective plasmids have not been identified in rhizobia. of RepABC-type plasmids is homologous to the universal The strict phylogenetic separation of these plasmid modules ParA/ParB partitioning system of the bacterial chromosome and allows for a reliable genomic differentiation between both other tripartite plasmids (Petersen et al., 2011). alphaproteobacterial orders, thus providing indirect evidence Horizontal gene transfer (HGT) correlates with major for functional constraints resulting in a narrow-host-range. evolutionary transitions (Nelson-Sathi et al., 2015) and the However, the supposed ecological separation between the process is inter alia mediated by phages and conjugative soil and the ocean, which would limit the physical contact plasmids. Plasmid mobilization is ensured by type IV secretion for conjugation, is less pronounced than a priori assumed. systems (T4SS), representing a conserved export apparatus Several rhizobial lineages, such as the genus Martelella are that is also used by several pathogenic bacteria for DNA adapted to saline habitats (Rivas et al., 2005) and roseobacters and protein secretion (Cascales and Christie, 2003). The represent a paraphyletic group associated with non-marine role of plasmid conjugation for the rapid adaptability of Rhodobacteraceae including the genus Paracoccus (Simon et al., bacteria is exemplified by the emergence of multi-resistant 2017). hospital strains as a consequence of massive antibiotic (mis) In the current study we experimentally document that use in medicine and livestock husbandry (Palmer et al., rhizobial RepABC plasmids do not replicate in Phaeobacter 2010). Many extrachromosomal elements are adapted to inhibens DSM 17395 (Rhodobacteraceae), but we provide their host and do not stably maintain in distantly related the first example of a natural plasmid that can be stably bacteria (narrow-host-range plasmid; Kües and Stahl, 1989). maintained in both rhizobia and roseobacters. This A prominent example is the Ti plasmid from A. tumefaciens composite plasmid from the marine rhizobium Martelella C58 that can be conjugated into Escherichia coli but requires mediterranea DSM 17316T originated from a plasmid an additional replication system for stable maintenance in fusion and still harbors rhizobial and rhodobacteral Enterobacteriaceae (Gammaproteobacteria; Holsters et al., 1978). RepABC cassettes thus overcoming the limits of their host Naturally occurring broad-host-range vectors from E. coli were range. Frontiers in Microbiology | www.frontiersin.org 2 September 2017 | Volume 8 | Article 1787 Bartling et al. The Composite 259-kb
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