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Spp. (Alphaproteobacteria) Insights into the Transposable Mobilome of Paracoccus spp. (Alphaproteobacteria) Lukasz Dziewit, Jadwiga Baj, Magdalena Szuplewska, Anna Maj, Mateusz Tabin, Anna Czyzkowska, Grazyna Skrzypczyk, Marcin Adamczuk, Tomasz Sitarek, Piotr Stawinski, Agnieszka Tudek, Katarzyna Wanasz, Ewa Wardal, Ewa Piechucka, Dariusz Bartosik* Department of Bacterial Genetics, Faculty of Biology, Institute of Microbiology, University of Warsaw, Warsaw, Poland Abstract Several trap plasmids (enabling positive selection of transposition events) were used to identify a pool of functional transposable elements (TEs) residing in bacteria of the genus Paracoccus (Alphaproteobacteria). Complex analysis of 25 strains representing 20 species of this genus led to the capture and characterization of (i) 37 insertion sequences (ISs) representing 9 IS families (IS3,IS5,IS6,IS21,IS66,IS256,IS1182,IS1380 and IS1634), (ii) a composite transposon Tn6097 generated by two copies of the ISPfe2 (IS1634 family) containing two predicted genetic modules, involved in the arginine deiminase pathway and daunorubicin/doxorubicin resistance, (iii) 3 non-composite transposons of the Tn3 family, including Tn5393 carrying streptomycin resistance and (iv) a transposable genomic island TnPpa1 (45 kb). Some of the elements (e.g. Tn5393,Tn6097 and ISs of the IS903 group of the IS5 family) were shown to contain strong promoters able to drive transcription of genes placed downstream of the target site of transposition. Through the application of trap plasmid pCM132TC, containing a promoterless tetracycline resistance reporter gene, we identified five ways in which transposition can supply promoters to transcriptionally silent genes. Besides highlighting the diversity and specific features of several TEs, the analyses performed in this study have provided novel and interesting information on (i) the dynamics of the process of transposition (e.g. the unusually high frequency of transposition of TnPpa1) and (ii) structural changes in DNA mediated by transposition (e.g. the generation of large deletions in the recipient molecule upon transposition of ISPve1 of the IS21 family). We also demonstrated the great potential of TEs and transposition in the generation of diverse phenotypes as well as in the natural amplification and dissemination of genetic information (of adaptative value) by horizontal gene transfer, which is considered the driving force of bacterial evolution. Citation: Dziewit L, Baj J, Szuplewska M, Maj A, Tabin M, et al. (2012) Insights into the Transposable Mobilome of Paracoccus spp. (Alphaproteobacteria). PLoS ONE 7(2): e32277. doi:10.1371/journal.pone.0032277 Editor: Laurence Van Melderen, Universite Libre de Bruxelles, Belgium Received October 7, 2011; Accepted January 24, 2012; Published February 16, 2012 Copyright: ß 2012 Dziewit 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 (grant PBZ-MNiSW-04/I/2007). 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 frequently occur on mobile plasmids and bacteriophages, which enhances the propagation of TEs by horizontal gene transfer Transposable elements (TEs) are components of nearly all (HGT) between various bacteria. This results in significant prokaryotic genomes. They are mobilized to change their location enrichment of the bacterial mobilome, i.e. a pool of mobile in DNA by the action of a transposase (TPase), an enzyme which DNA involved in HGT, which is considered to be the driving force catalyses transposition, i.e. recombination that does not require of bacterial evolution. sequence homology between the TE and the target site. The The simplest TEs are insertion sequences (ISs), which are highly presence and activity of TEs may lead to structural changes in abundant in bacteria. They carry only genetic information that is both the size and composition of a genome. TEs can generate (i) necessary and sufficient for transposition and its regulation. The various mutations, such as insertions, deletions, duplications, majority of ISs are composed of a single open reading frame inversions and translocations of even large DNA fragments, and (ii) (ORF), encoding a transposase, flanked by two inverted repeat replicon fusions [1]. Some elements are able to activate silent, sequences (IRs) that are recognized by the TPase during promoterless genes, when they are located in close proximity to the transposition. In most cases, the transposition of ISs causes target site of transposition [2,3]. Moreover, TEs can mobilize duplication of the target site, so that the inserted element is chromosomal genes for transposition, which results in shuffling of bordered by two short (2–15 bp) identical direct repeat sequences genetic information among various replicons present in a bacterial (DRs) [5]. cell [4]. Thus, these highly recombinogenic elements may be ISs are also able to form more complex TEs such as (i) considered as major architects responsible for shaping the composite transposons consisting of random segments of genomic structure of prokaryotic genomes. Their activity significantly DNA (core region) bordered by a pair of ISs, or (ii) transposable enhances genome variability and consequently the adaptative modules (TMos) and ISCR elements composed of one IS copy, and evolutionary capacities of their hosts. In addition, TEs very which can mobilize an adjacent DNA segment for transposition PLoS ONE | www.plosone.org 1 February 2012 | Volume 7 | Issue 2 | e32277 Transposable Elements of Paracoccus spp. [3,6]. ISs are also responsible for the mobility of non-autonomous and distribution of the captured TEs, which allowed us to draw TEs (i.e. not encoding their own transposase), such as (i) mobile more general conclusions concerning their evolutionary impact, as insertion cassettes (MICs), identified in Bacillus cereus [7] and (ii) well as the direction and frequency of horizontal gene transfer in miniature inverted repeat transposable elements (MITEs), which this group of bacteria. may constitute up to 2% of a bacterial genome [8]. There is another widely distributed group of TEs called the non- Materials and Methods composite transposons, which is divided into the Tn3 and Tn7 families. Besides a transposase, the Tn3 elements contain a site- Bacterial Strains and Culture Conditions specific recombination module encoding a resolvase (an enzyme For identification of transposable elements rifampicin-resistant responsible for resolution of cointegrates, which are intermediate (Rifr) derivatives of the wild-type strains of Paracoccus spp. (listed in forms in replicative transposition), while the Tn7 elements are Table 1) were used. Escherichia coli TG1 [21] was used for plasmid known for their complex transposition machinery (they encode five construction. The majority of the strains were grown in lysogeny transposition proteins) [9,10]. These transposons often encode broth (LB) medium (Sigma) at 30uC(Paracoccus spp.) or 37uC(E. beneficial functions such as drug or heavy metal resistance, coli). P. homiensis DSM 17862 was cultivated in Marine Broth pathogenicity or the ability to utilize different carbon sources (Difco). Where necessary, the medium was supplemented with [11,12]. sucrose (10%) and with antibiotics at the following concentrations Large-scale genome sequencing projects have led to an (mg?ml21): kanamycin, 50; rifampicin, 50; tetracycline, 0.3–35 explosion in the number of annotated prokaryotic and eukaryotic (depending on the strain). TEs (for example, more than 3800 IS elements have now been isolated from over 295 prokaryotic species; ISfinder database [13]). However, in most cases their activity has not been experimentally confirmed. In 2009 we initiated a project aimed at identifying functional transposable elements harbored by bacteria belonging to the genus Table 1. Paracoccus spp. strains used in this study. Paracoccus (Alphaproteobacteria). This genus currently comprises 31 species, which have been isolated from many geographical locations and from different environments. Paracoccus spp. are Paracoccus spp. strain References physiologically among the most versatile bacteria, and are able to P. aestuarii DSM 19484 [59] perform a number of different growth modes. Many are aerobic P. alcaliphilus JCM 7364 [60] chemoorganoheterotrophs utilizing a wide variety of organic P. alkenifer DSM 11593 [61] compounds, including potential pollutants like acetone, N,N- dimethylformamide and methylamine [14]. Some strains of P. aminophilus JCM 7686 [62] Paracoccus spp. are facultative chemolithoautotrophs utilizing P. aminovorans JCM 7685 [62] reduced sulfur compounds, molecular hydrogen and Fe(II) as P. bengalensis DSM 17099 [63] energy sources [14,15]. Because of their versatile metabolism, P. denitrificans LMD 22.21 [64] these bacteria can play an important role in the cycling of P. ferrooxidans NCCB 1300066 [15] chemical elements in the environment. In addition, these P. haeundaensis LMG P-21903 [65] physiological properties raise the possibility of employing para- cocci in bioremediation systems, particularly since many species P. halophilus
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