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Alphaproteobacteria) - Structure, Diversity and Evolution Plasmids of Carotenoid-Producing Paracoccus spp. (Alphaproteobacteria) - Structure, Diversity and Evolution Anna Maj, Lukasz Dziewit, Jakub Czarnecki, Miroslawa Wlodarczyk, Jadwiga Baj, Grazyna Skrzypczyk, Dorota Giersz, Dariusz Bartosik* Department of Bacterial Genetics, Institute of Microbiology, Faculty of Biology, University of Warsaw, Warsaw, Poland Abstract Plasmids are components of many bacterial genomes. They enable the spread of a large pool of genetic information via lateral gene transfer. Many bacterial strains contain mega-sized replicons and these are particularly common in Alphaproteobacteria. Considerably less is known about smaller alphaproteobacterial plasmids. We analyzed the genomes of 14 such plasmids residing in 4 multireplicon carotenoid-producing strains of the genus Paracoccus (Alphaproteobacteria): P. aestuarii DSM 19484, P. haeundaensis LG P-21903, P. marcusii DSM 11574 and P. marcusii OS22. Comparative analyses revealed mosaic structures of the plasmids and recombinational shuffling of diverse genetic modules involved in (i) plasmid replication, (ii) stabilization (including toxin-antitoxin systems of the relBE/parDE, tad-ata, higBA, mazEF and toxBA families) and (iii) mobilization for conjugal transfer (encoding relaxases of the MobQ, MobP or MobV families). A common feature of the majority of the plasmids is the presence of AT-rich sequence islets (located downstream of exc1-like genes) containing genes, whose homologs are conserved in the chromosomes of many bacteria (encoding e.g. RelA/SpoT, SMC-like proteins and a retron-type reverse transcriptase). The results of this study have provided insight into the diversity and plasticity of plasmids of Paracoccus spp., and of the entire Alphaproteobacteria. Some of the identified plasmids contain replication systems not described previously in this class of bacteria. The composition of the plasmid genomes revealed frequent transfer of chromosomal genes into plasmids, which significantly enriches the pool of mobile DNA that can participate in lateral transfer. Many strains of Paracoccus spp. have great biotechnological potential, and the plasmid vectors constructed in this study will facilitate genetic studies of these bacteria. Citation: Maj A, Dziewit L, Czarnecki J, Wlodarczyk M, Baj J, et al. (2013) Plasmids of Carotenoid-Producing Paracoccus spp. (Alphaproteobacteria) - Structure, Diversity and Evolution. PLoS ONE 8(11): e80258. doi:10.1371/journal.pone.0080258 Editor: Axel Cloeckaert, Institut National de la Recherche Agronomique, France Received August 9, 2013; Accepted October 11, 2013; Published November 8, 2013 Copyright: © 2013 Maj et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Funding: This work was supported by the Ministry of Science and Higher Education, Poland – grants 2 P04A 028 29 (characterization of pMARC plasmids), PBZ-MNiSW-04/I/2007 (characterization of pAES, pHAE, and pMOS plasmids) and N N302 224638 (construction of vector cassettes and shuttle vectors). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing interests: The authors have declared that no competing interests exist. * E-mail: [email protected] Introduction and sometimes several smaller plasmids (e.g. [1,2]). Analysis of the genomic data collected by The National Center for Bacterial plasmids have a modular structure: their genomes Biotechnology Information (NCBI) revealed that the sequenced can be separated into several DNA cassettes encoding specific genomes of 240 alphaproteobacterial strains include a total of functions. Besides the conserved backbone, composed of 315 plasmids. Twenty six of these strains are multi-plasmid genetic modules encoding replication (REP), stabilization and containing, with at least five extrachromosomal replicons. transfer functions, plasmids can contain an additional “genetic For many years, knowledge of plasmids of the load”, which may significantly influence the metabolic Alphaproteobacteria was mainly limited to the repABC and properties of any recipient strain. Many plasmids are giant repC families of replicons, which are specific for megaplasmids molecules that can even exceed the size of some bacterial of this group of bacteria (repA and repB of repABC replicons chromosomes. Such mega-sized replicons (megaplasmids) are encode partitioning proteins, while repC encodes replication particularly common in Alphaproteobacteria. initiator) (e.g. [3,4]). Recent studies have revealed the Alphaproteobacteria constitute interesting models for presence of plasmids classified into the repA and repB families studying the complexity and diversity of bacterial genomes. as well as a dnaA-like family, encoding replication proteins with Many strains within the genera Rhizobium, Agrobacterium and similarity to the DnaA proteins involved in the initiation of Paracoccus contain chromosomes, chromids, megaplasmids replication of bacterial chromosomes [1]. Detailed analysis of PLOS ONE | www.plosone.org 1 November 2013 | Volume 8 | Issue 11 | e80258 Plasmids of Carotenoid-Producing Paracoccus spp. the REP regions allowed the following incompatibility (inc) Table 1. Basic characterization of the Paracoccus spp. groups to be distinguished: (i) 9 groups of repABC replicons, plasmid genomes. (ii) 5 groups of repA-family replicons and (iii) 4 groups of repB- family replicons [1]. Most of the analyzed REPs are harbored by megaplasmids and much less is known about smaller GC content (%) alphaproteobacterial plasmids. Plasmid Host Number Genetic Several years ago we initiated a project aimed at identifying Plasmid Host Size (bp)DNA DNA of ORFs modules and characterizing the pool of mobile DNA in bacteria P. aestuarii DSM 62 belonging to the genus Paracoccus (Alphaproteobacteria). This pAES1 2925 64.4 2 REP, MOB 19484 [43] genus currently comprises 42 species and hundreds of strains pAES2 4502 57.9 5 REP, R-M (not identified at species level), which are known for their pAES3 5434 51.7 7 REP, TA versatile physiological properties and ability to perform a REP, MOB, number of different growth modes. We focused our interest on pAES4 5850 58.6 9 TA mobile genetic elements (MGE) of Paracoccus spp., especially REP, MOB, plasmids and transposable elements (TE) (e.g. [5]). As a result pAES7 13,005 60.1 15 TA(2) of this approach we have identified and analyzed (i) four P. haeundaensis 66.9 pHAE1 5301 58.8 4 REP related repABC as well as several pTAV3-type megaplasmids LG P-21903 [44] – both groups residing in P. versutus UW1 and four strains of pHAE2 5777 53.6 5 REP, TA Paracoccus pantotrophus [6,7], (ii) plasmid pALC1 of P. marcusii DSM 66 pMARC1 5122 49.0 6 REP, TA Paracoccus alcaliphilus JCM 7364, with an iteron-containing 11574 [45] replication system [8], (iii) plasmid pMTH1 of Paracoccus pMARC2 5789 51.6 6 REP, MOB methylutens DM12, whose genome is predominantly (80%) REP, PAR, pMARC3 10,672 59.0 10 composed of transposable modules (TMos) [9], (iv) three MOB, TA plasmids of Paracoccus aminophilus JCM 7686, whose REP REP, MOB, pMARC4 15,289 53.4 15 modules were used for the construction of versatile DIY TA cassettes [10,11], as well as (v) plasmid pWKS1 of P. P. marcusii 66 pMOS2 6410 54.0 5 REP, MOB pantotrophus DSM 11072 – the smallest replicon identified so OS22 [45] far in Paracoccus spp. [12]. REP, MOB, pMOS6 7672 63.1 12 In this study we identified four plasmid-rich strains of TA Paracoccus spp. Genomic analysis of their plasmids revealed pMOS7 5979 50.0 7 REP, TA that the genetic organization and structure of many of them doi: 10.1371/journal.pone.0080258.t001 differ significantly from that previously described in Alphaproteobacteria. Comparative bioinformatic analysis was used to distinguish the plasmid backbones, composed of different combinations of Results and Discussion genetic modules responsible for plasmid replication (REP), stabilization (toxin-antitoxin – TA; partitioning – PAR) and Plasmids of carotenoid-producing strains of mobilization for conjugal transfer (MOB), and accessory Paracoccus spp. genetic information, which may potentially influence the At the initial stage of this study we analyzed the plasmid phenotype of the host (Figure 1). Detailed characterization of content of 22 strains representing 20 Paracoccus spp. (listed in the predicted modules is presented below. Methods section). Plasmid screening revealed that the majority of the tested strains contained megaplasmids (above 100 kb) Replication modules (data not shown). Only four of the strains (P. aestuarii DSM 19484, P. haeundaensis LG P-21903, P. marcusii DSM 11574 Replication systems of the vast majority of plasmids residing and P. marcusii OS22 – all able to produce beta-carotenoid in gram-negative bacteria consist of two elements: (i) a gene pigments) contained numerous smaller replicons ranging in encoding a Rep protein, which initiates DNA replication, and (ii) size from approx. 2.5 kb to 85 kb. the cis-required origin (oriV; equivalent to chromosomal oriC) To analyze plasmid diversity in these strains we obtained the where replication begins. Most Rep proteins are highly nucleotide sequences of 14 randomly selected replicons (listed conserved and they can be grouped into several families on the in Table 1): (i) 5 pAES plasmids of P. aestuarii DSM 19484, (ii) basis of amino acid (aa) sequence
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