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Exploring the Evolutionary Dynamics of Plasmids: the Acinetobacter Pan

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Exploring the Evolutionary Dynamics of Plasmids: the Acinetobacter Pan Fondi et al. BMC Evolutionary Biology 2010, 10:59 http://www.biomedcentral.com/1471-2148/10/59 RESEARCH ARTICLE Open Access Exploring the evolutionary dynamics of plasmids: the Acinetobacter pan-plasmidome Marco Fondi1, Giovanni Bacci1, Matteo Brilli2, Maria Cristiana Papaleo1, Alessio Mengoni1, Mario Vaneechoutte3, Lenie Dijkshoorn4, Renato Fani1* Abstract Background: Prokaryotic plasmids have a dual importance in the microbial world: first they have a great impact on the metabolic functions of the host cell, providing additional traits that can be accumulated in the cell without altering the gene content of the bacterial chromosome. Additionally and/or alternatively, from a genome perspective, plasmids can provide a basis for genomic rearrangements via homologous recombination and so they can facilitate the loss or acquisition of genes during these events, which eventually may lead to horizontal gene transfer (HGT). Given their importance for conferring adaptive traits to the host organisms, the interest in plasmid sequencing is growing and now many complete plasmid sequences are available online. Results: By using the newly developed Blast2Network bioinformatic tool, a comparative analysis was performed on the plasmid and chromosome sequence data available for bacteria belonging to the genus Acinetobacter,an ubiquitous and clinically important group of g-proteobacteria. Data obtained showed that, although most of the plasmids lack mobilization and transfer functions, they have probably a long history of rearrangements with other plasmids and with chromosomes. Indeed, traces of transfers between different species can be disclosed. Conclusions: We show that, by combining plasmid and chromosome similarity, identity based, network analysis, an evolutionary scenario can be described even for highly mobile genetic elements that lack extensively shared genes. In particular we found that transposases and selective pressure for mercury resistance seem to have played a pivotal role in plasmid evolution in Acinetobacter genomes sequenced so far. Background bacterial genus. Plasmids genes are in fact under differ- Plasmids are among the most important players in the ential selection while moving through the prokaryotic evolution of prokaryotes and in their adaptation to fluc- community [3], and consequently, they frequently gain tuating environmental conditions [1-3]. They are actu- and lose genes, revealing a very dynamic organization ally involved in many accessory functions and [2,7,8]. This flexibility is mostly due to the abundance of constitute, together with “not essential” chromosomal transposable elements they harbor and that facilitate regions, what is referred to as the “dispensable genome” intra- and intermolecular recombination by creating in the microbial pan-genome concept [4]. Typically, a homology regions. Moreover, plasmids can be both ver- plasmid includes one or more essential genes encoding tically and horizontally inherited in a prokaryotic com- replicative functions. In addition, it may harbor one or munity, giving rise to the possibility that the very same more genes coding for a variable panoply of accessory plasmid molecule can be hosted in different genomic metabolic processes and functions that are, in general, contexts, boosting the rearrangement of their functions different from those encoded by chromosome(s) [2,5,6]. and of gene organization [9-11]. Actually, plasmid architecture is more flexible than the Despite the key-role of plasmids in the prokaryotic chromosomal one, concerning both gene content and world, the evolutionary dynamics of plasmids have been gene organization, even within members of the same poorly explored, mainly because of the lack of extensive similarities between them, except for genes involved in * Correspondence: [email protected] replication and transfer functions [12,13], which ham- 1 Laboratory of Microbial and Molecular Evolution, Dept. of Evolutionary pers classical phylogenetic analyses based on gene Biology, Via Romana 17-19, University of Florence, I-50125 Florence, Italy © 2010 Fondi et al; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Fondi et al. BMC Evolutionary Biology 2010, 10:59 Page 2 of 15 http://www.biomedcentral.com/1471-2148/10/59 genealogy and synteny [14]. However, a computational the sequences of 7 genomes and 29 plasmids were avail- biology approach (Blast2Network) based on similarity able (Table 1). The Acinetobacter “pan-plasmidome”, networks reconstruction and phylogenetic profiling has that is the complete set of plasmids harbored by mem- been recently proposed and applied in a study-case to bers of this genus (comprising plasmids isolated from depict the similarities among plasmids from Enterobac- both pathogenic and environmental strains), is then par- teriaceae [15]. The bioinformatic package Blast2Network ticularly attractive to study its evolutionary dynamics (hereafter designated B2N) provides an immediate visua- because of the eclectic lifestyle of their host strains and lization of the similarities, existing among aminoacidic the possible frequent genetic exchanges between its or nucleic sequences [15]. This, in turn, opens the possi- members. bility to trace the evolutionary dynamics and history of Therefore, in this work, a detailed comparative analy- entire plasmids and not only of single genes and/or sis of the completely sequenced Acinetobacter plasmids, operons harbored by them. In this context, bacteria available in public databases, was performed with the belonging to the genus Acinetobacter may represent an aim to i) reconstruct their evolutionary dynamics and ii) excellent study-case, because strains of this genus are investigate the evolutionary cross-talk between them commonly found in soil, water and in association with and the chromosomes of Acinetobacter strains. animals [16,17]. Besides, some of them are well-known human pathogens, often responsible for opportunistic Results infections in hospitalized patients [16,18,19]. A striking Plasmid networks recent manifestation of A. baumannii is the occurrence The first aim of the work was the identification and the in severely wounded soldiers coming back from Iraq analysis of the possible evolutionary relationships exist- [20].Currently,thegenusAcinetobacter comprises 19 ing among the 29 Acinetobacter plasmids. To this pur- species with valid names and at least 13 putative species pose, all the 493 retrieved sequences of Acinetobacter [21]. More than 975 strains have been recorded in the plasmid-encoded proteins were used as input for the Taxonomy Browser of NCBI at July, 2 2009, but the B2N software (see Material and Methods), generating a precise taxonomy of these strains is not always clear set of networks showing all the sequence identities exist- since many have not been identified by unambiguous ing among these proteins. In these networks nodes genotypic identification methods [21,22]. Acinetobacter represent proteins, whereas links indicate the existence strains are of special interest for the huge variety of of sequence identity among them (Figure 1 and [Addi- environments they can colonize and the diverse meta- tional file 1]). The degree of sequence identity threshold bolic abilities they display, as inferred from the occur- is a priori selected. In principle, the higher the threshold rence of, e.g., hydrocarbon degrading strains in oil spills, used, the lower the number of links existing between human pathogens resistant to a plethora of antibiotics, proteins encoded by different plasmids. In addition, it rhizospheric bacteria and strains inhabiting bioreactors can be assumed that the higher the degree of aminoacid or insect guts [6,23-29]. Moreover, a special interest for identity between two proteins, the more recent would members of this genus also relies on the ability of some be the event (recombination/transposition/duplication/ strains, i.e. those belonging to the species A. baylyi,to vertical transmission) responsible for the presence of the undergo natural transformation [9,30]. This attribute two orthologous/paralogous coding genes in different has made the A. baylyi strain ADP1 (also named plasmids. We selected a minimum of 50% identity BD413) an exceptional tool for genetic analysis and threshold since this degree of sequence identity is suffi- engineering [31]. ciently high to guarantee that in most cases the inter- It has been reported that several Acinetobacter strains, connected proteins perform the same function (i.e., they especially those sharing particular ecological niches that are encoded for by orthologous genes) [37,38]. The require specific adaptations, like polluted environments three networks shown in Figure 1 (at 100%, 90%, and and bioreactors, harbor plasmid molecules of different 50% identity thresholds) and the other three reported in sizes undergoing frequent molecular rearrangements [Additional file 1]. (at 60%, 70%, and 80% identity [32-34]. Particularly interesting among Acinetobacter thresholds) were obtained by reiterating the analysis plasmids is the pKLH2 family [35], a group of evolution- using different identity thresholds. ary related plasmids harboring mercury resistance genes Analysis of links (mer) embedded in a single compact operon that, in The analysis of the networks
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