Bioinformatics Advance Access originally published online on November 22, 2005
Bioinformatics 2006 22(9):1072-1079; doi:10.1093/bioinformatics/bti793
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Describing ancient horizontal gene transfers at the nucleotide and gene levels by comparative pathogenicity island genometrics
1 Inserm E0364—Université de Lille II, Faculté de Médecine Henri Warembourg, Institut Pasteur de Lille 1 rue du Pr Calmette, F-59021 Lille, France
2 Département de Microbiologie Fondamentale, Bâtiment de Biologie, Faculté de Biologie et de Médecine, Université de Lausanne CH-1015 Dorigny, Switzerland
*To whom correspondence should be addressed.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Motivation: Lateral gene transfer is a major mechanism contributing to bacterial genome dynamics and pathovar emergence via pathogenicity island (PAI) spreading. However, since few of these genomic exchanges are experimentally reproducible, it is difficult to establish evolutionary scenarios for the successive PAI transmissions between bacterial genera. Methods initially developed at the gene and/or nucleotide level for genomics, i.e. comparisons of concatenated sequences, ortholog frequency, gene order or dinucleotide usage, were combined and applied here to homologous PAIs: we call this approach comparative PAI genometrics.
Results: YAPI, a Yersinia PAI, and related islands were compared with measure evolutionary relationships between related modules. Through use of our genometric approach designed for tracking codon usage adaptation and gene phylogeny, an ancient inter-genus PAI transfer was oriented for the first time by characterizing the genomic environment in which the ancestral island emerged and its subsequent transfers to other bacterial genera.
Contact: claude-alain.roten{at}unil.ch
Supplementary information: http://www.unil.ch/comparativegenometrics/collyn_et_al_2005/collyn.htm
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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In pathogenic bacteria, virulence genes are often clustered into pathogenicity islands (PAIs) (Hacker and Kaper, 2000). These laterally acquired genetic elements (GEs) are present on the chromosomes of bacterial pathogens but not on their counterparts in related but harmless bacteria. The foreign origin of PAIs is evidenced by the presence of various mobility genes, as well as by G + C content and codon usage that generally differ from those of the core genome. Since gene acquisition is an important evolutionary process by which microorganisms obtain novel phenotypes (Dobrindt and Hacker, 2001), PAIs play an essential role in virulence gene spreading and contribute to the emergence of new pathogens (Hacker and Kaper, 2000; Ochman et al., 2000). However, even though homologous PAIs have already been described in distant bacterial species, no clear scenario describing ancient inter-genus transmission of these mobile units has yet been demonstrated—partly because attempts to experimentally observe PAI transfer have rarely been successful. Thus, bioinformatics appears to be the method of choice for establishing accurate descriptions of lateral genetic exchanges in prokaryotes.
Bioinformatics tools have already been developed for comparative genomics. Two different strategies have been used successfully: the first, based on comparisons of homologous DNA sequences or gene units, measures either (1) gene concatenate similarities (Wolf et al., 2001), (2) ortholog frequencies (Snel et al., 1999) or (3) gene order conservation (Blanchette et al., 1999). In contrast to the first-listed technique, the latter two, which use genes as basic units, are insensitive to homing, i.e. the tendency of the codon usage of mobile elements to become similar to that of the cell counterpart. Both techniques were efficiently developed for viral or mitochondrial DNA sequences affected by high mutation rates (Wolfe et al., 1987; Blanchette et al., 1999; Montague and Hutchison, 2000; Herniou et al., 2003) and have subsequently been applied to bacterial genome phylogeny (Fitz-Gibbon and House, 1999; Snel et al., 1999; Tekaia et al., 1999; Snel et al., 2002). Since homing of transmissible GEs affects phylogenetic analyses based on the similarity of laterally acquired genes, these methods can also be used for comparative PAI analysis.
The second strategy is based on nucleotide signatures and enables comparison of non-homologous DNA sequences. The genome signature reflects codon usage by measuring dinucleotide biases (Karlin and Cardon, 1994; Karlin et al., 1998) and is able to (1) specify evolutionary relationships (Karlin et al., 1994), (2) measure taxonomical distances between bacteria, plasmids and eukaryotic organelles (Campbell et al., 1999) and (3) detect bacterial, chromosomal PAIs (Karlin, 2001). However, the genome signature must be carefully interpreted, since horizontally acquired genes gradually adapt their codon usage and thus their nucleotide composition to those of the core genome: the more ancient the genetic acquisition, the less conserved the PAI signature.
When applied to whole PAIs or some of their gene subsets, a combination of these comparative methods referred to here as comparative pathogenicity island genometrics appears capable of documenting lateral transfer at the gene and nucleotide levels. Homologous PAIs shared by non-closely-related species constitute suitable models for testing this strategy.
We recently identified a 11 kb type IV pilus gene cluster (pil) on the chromosome of the enteropathogenic bacteria Yersinia pseudotuberculosis (Collyn et al., 2002). This virulence factor is encoded by a 98 kb PAI called YAPI (Collyn et al., 2004a). A DNA segment homologous to Y.pseudotuberculosis YAPI (YAPIpst) was found in the chromosome of Yersinia enterocolitica (Collyn et al., 2004b), the other enteropathogenic species in the Yersinia genus. Designated as YAPIent, this 66 kb PAI comprises 61 ORFs, of which 41 are homologous to YAPIpst genes. Furthermore, 37 of the latter (including the pil genes) have counterparts on the 134 kb SPI-7 PAI from Salmonella enterica serovar Typhi (SPI-7ty) (Fig. 1), an Enterobacteriaceae found in the host digestive tract along with enteropathogenic Yersiniae. Of the 37 orthologs, 32 shared by YAPIs and SPI-7 were also detected in 1 W14, a 297 kb PAI from the entomopathogenic bacterium Photorhabdus luminescens (Duchaud et al., 2003). Furthermore, sequence analyses of SPI-7, YAPIs and 1 W14 showed that all contain coding sequences (CDS) related to type IV pilus-encoding genes and other transfer genes harbored on the Salmonella conjugative plasmids from the same family, R64 and ColIbP9. All these data suggest a common origin for R64-like plasmids, SPI-7, 1 W14 and YAPIs (Pickard et al., 2003; Collyn et al., 2004a). Since YAPIs, SPI-7 and 1 W14 are (1) fully sequenced and well documented, (2) harbored by distinct bacterial genera and (3) related to a conjugative plasmid likely to have contributed to their emergence (Pickard et al., 2003), they constitute a paradigmatic system for challenging PAI-scale phylogenetic scenarios.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Sequence sources
The database accession numbers of PAI and plasmid sequences are, respectively, SPI-7ty, NC_003198 [GenBank] ; 1W14, NC_005126 [GenBank] , YAPIpst, AJ627388 [GenBank] ; pSLT, NC_003277 [GenBank] ; R721, NC_002525 [GenBank] ; R64, NC_005014 [GenBank] ; ColIb-P9, NC_002122 [GenBank] ; pCD1, NC_003131 [GenBank] ; pCP1, NC_003132 [GenBank] ; pMT1, NC_003134 [GenBank] and pYV, NC_005017 [GenBank] . The YAPIent sequence was downloaded from the Sanger website (www.sanger.ac.uk/Projects/Y_enterocolitica/).
Ortholog identification
Amino acid sequences of all CDSs from the four PAIs and two plasmids were compared with those of related GEs using BLASTP 2.2.10 (Altschul et al., 1997) with the BLOSUM62 matrix and gap penalties of 11 and 1. The threshold of E-values was 0.01 and non-reciprocal matches were removed. When a protein sequence presented several orthologs, only the best E-value comparison was considered.
Similarity analysis of concatenated pil genes
All the pil gene products housed by the YAPIs, SPI-7, 1 W14, R64 and ColIbP9 were concatenated as previously described (McGeoch et al., 2000; Wolf et al., 2001; Ling et al., 2002; Sharp et al., 2005) and compared using ClustalW (Thompson et al., 1994). The Neighbor-Joining (NJ) tree was drawn with Treeview v.1.1.6 (Page, 1996).
Evolutionary distance estimated by ortholog frequencies
Evolutionary relationships between PAIs and plasmids were measured by the proportion of orthologous genes shared by pairs of GEs. The method differs slightly from that previously reported (Snel et al., 1999). For instance, when selecting GEa as reference, the distance between GEa and GEb corresponds to the proportion of GEb genes having a GEa homolog. The resulting distance matrix was analyzed using the Phylip package (Felsenstein, 2004) via the Unweighted Pair Group Method with Arithmetic Means (UPGMA), Neighbor-Joining (NJ) and Fitch Margoliash methods. Resulting dendrograms were drawn with Treeview v.1.1.6. Calculated for the UPGMA tree, the root of these ultrametric dendrograms is posted on the figures at the midpoint of the longest pathway between taxa.
Gene order comparison
In order to quantify the inversion and transposition events leading to the current organization of PAIs and plasmids, we measured the proportion of conserved ortholog pairs in these GEs, as previously described (Blanchette et al., 1999; Greub et al., 2004). Dendrograms and related roots were calculated as for the comparison of ortholog frequencies.
Dinucleotide signature analysis
Dinucleotide signature analysis was performed according to the method of Campbell and co-workers (Karlin and Cardon, 1994; Karlin et al., 1998; Campbell et al., 1999). The distance between pairs of GEs was estimated by summing up all the absolute differences in dinucleotide bias (Manhattan distances). Resulting matrices were represented as UPGMA, NJ and Fitch Margoliash dendrograms. A dissimilarity matrix of Euclidean distances generated for all PAIs and plasmids was also represented by a principal coordinates (PCO) analysis (Gower, 1966).
Dendrogram robustness
The robustness of the analyses shown in Figures 2 and 4 was evaluated by performing an omit test on the UPGMA, NJ and Fitch Margoliash dendrograms: for each final tree of n GEs, n subtrees are produced with n – 1 GEs, where each GE is omitted in turn. The conservation of subtree topologies indicates the robustness of the final dendrogram.
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In NJ and Fitch Margoliash distance analysis, the dinucleotide usage distance biases were bootstrapped: 1000 distance matrices were built by random resampling with R 2.0.1 (Ihaka and Gentleman, 1996) and Fitch Margoliash trees were calculated using the Phylip package. A consensus dendrogram obtained with the extended Majority Rule method was used to obtain a bootstrapped evaluation of the original analysis.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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YAPI, SPI-7 and 1 W14 were generated by horizontal transfer of an ancestral pathogenicity island
Since the pil operon was the only identified functional unit shared by the four PAIs and the two R64-related plasmids, we first measured sequence similarity between Pil proteins encoded by these GEs using ClustalW (Supplementary Fig. 1). Very similar trees were drawn when comparing individual genes (data not shown). Unfortunately, this investigation failed to shed light on PAI emergence: no unambiguous conclusion about PAI transfer could be drawn from the dendrogram, which was characterized by poor resolution of major branches. The divergence of type IV pilus function in the different GEs (plasmids, bacterial conjugation; PAIs, bacterial adhesion, respectively) might also be responsible for pil operon sequence variations.
To bypass this difficulty, the frequency of orthologs present on PAIs and plasmids was used to identify those GEs exhibiting the most similar organization (Snel et al., 1999). The UPGMA representation of the resulting dissimilarity matrix provided more information than ClustalW analyses: R64-like plasmids were clearly discriminated from YAPIs, SPI-7 and 1 W14 (Fig. 2A), suggesting that a unique, ancestral PAI emerged in a bacterium after chromosomal integration of a R64-like plasmid and was then transferred to other bacterial genera. NJ representations of this distance matrix provided tree topologies similar to those generated by UPGMA (Supplementary Fig. 2). To confirm this scenario, PAIs and plasmids were compared by using gene order breakpoint analysis (Blanchette et al., 1999) measuring local gene order and rearrangement events (insertion, deletion, transposition or inversion) in conserved gene sets: we obtained similar results to those obtained by ortholog frequency analysis (Fig. 2B).
The ancestral YAPI emerged from a Salmonella GE
The next step was to specify the bacterial environment in which the ancestral PAI emerged. Dinucleotide usage biases, constant along 
50 kb sequences, are efficient tools for comparing small GEs such as plasmids or mitochondria (Campbell et al., 1999) and detecting PAIs along prokaryotic chromosomes (Karlin, 2001). Hence, this genometric method appears to be appropriate for PAI comparison but, until now, had never been used for this purpose—most probably because PAIs often display chimeric genetic structures and thus exhibit heterogeneous nucleotide patterns. However, determination of dinucleotide frequencies on related modules (i.e. gene subsets from a common source and no smaller than animal mitochondrial genomes) might be useful for PAI comparison.
Before measuring inter-species/genus relationships, we first challenged the signal constancy of genome signatures of sets of PAI orthologs. Dinucleotide analyses of (1) pil operons, (2) genes located upstream or (3) downstream of the pil operon and (4) the entire set of orthologs for all PAIs indicated that this gene module constitutes an homogeneous core of an ancestral PAI, since the four dendrogram topologies were conserved (Fig. 3). Figure 3 also shows that pil operon dinucleotide usage was similar to those for the orthologs common to the four PAIs: we therefore compared the genome signatures of (1) PAI- and plasmid-borne pil operons and (2) all PAI orthologs and the R64-like plasmid sequences, regardless of whether they included pil genes or not. All the resulting trees were very similar (Fig. 4). As a control, our analysis also included the R721 self-transmissible plasmid—distantly related to R64 but also bearing pil CDSs (Kim and Komano, 1992): its dinucleotide usage diverged strongly from those of the R64-related plasmids, demonstrating that the genome signature method can indeed be used for phylogenetic analysis. NJ and Fitch Margoliash representations provided topologies similar to those generated by UPGMA (Supplementary Figs 3 and 4). All the results presented in Figures 3 and 4 clearly reveal that dinucleotide signatures have been conserved along the sequences of PAIs subsets and plasmids and demonstrate that PAI gene subsets can be reliably compared with whole plasmid sequences, including non-homologous genes.
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Finally, in order to identify the bacterial environment in which the ancestral PAI emerged, our study also included plasmids not harboring the pil operon: (1) pSLT1, isolated from Salmonella and not involved in YAPIs and SPI-7 emergence (McClelland et al., 2001); (2) virulence-associated plasmids from Yersinia pestis (pCD) and Y.enterocolitica (pYV) and (3) Y.pestis plasmids encoding a murine toxin (pMT) and a plasminogen activator (pPCP). Unfortunately, no Photorhabdus plasmid sequences were available in databases for comparative purposes. Figure 5A shows that the dinucleotide frequencies of two R64-family plasmids (R64 and ColIb-P9) were similar and resembled that of Salmonella plasmid pLST1, thus validating the specificity of the Salmonella plasmid signature. Since R721 houses tra and pil genes, it could theoretically be the source of the ancestral island formed by plasmid integration into a bacterial chromosome. Nevertheless, dinucleotide frequency comparisons clearly showed that the R721 plasmid did not contribute to the emergence of YAPIs, 1 W14 or SPI-7, since its dinucleotide signature diverged strongly from those of all PAIs. Our conclusion is also supported by the lower degree of sequence conservation between R721-encoded Pil proteins and their counterparts on PAIs and the R64-related plasmids. In contrast, the genome signatures of the R64-plasmid family and SPI-7 were found to be very similar, indicating that a plasmid from the R64 family was the source of the Salmonella PAI. Since representations of phylogenetic trees introduce some bias in relative distances and imply that all sequences have a common ancestor, we also performed a PCO analysis (Fig. 5B) providing no dendrogram, but calculating distance estimations of GE relationships more accurately. The close clustering of SPI-7 and the R64-related and pSLT1 plasmids demonstrates that the SPI-7 module presents a Salmonella-plasmid signature. In conclusion, our dinucleotide analyses revealed that a R64-related plasmid was the source of an ancestral PAI in a Salmonella environment. These results consequently enabled us to orient an ancient PAI transfer for the first time: a pristine island referred as PISYP (i.e. PAI module shared by Salmonella, Yersinia and Photorhabdus) first emerged in a Salmonella environment and then spread into the Yersinia and Photorhabdus genera.
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Y.pseudotuberculosis and Y.enterocolitica acquired ancestral YAPI prior to speciation
The close relationship between YAPIent and YAPIpst raises the question of how this PAI was acquired by both species and whether this DNA transfer occurred before or after enteropathogenic Yersinia speciation. In all the above analyses, the distances separating either YAPIpst or YAPIent from the other GEs were found to be almost identical (Figs 2–5 and Supplementary Fig. 1). This observation supports a parsimonious scenario proposing a contemporary acquisition of PISYP predating the enteropathogenic Yersiniae speciation. Furthermore, the similar degree of identity between (1) YAPIent and YAPIpst gene products (64–97% identity; average 82%) (Collyn et al., 2004b) and (2) homologous proteins encoded by the chromosomal cores of both Yersinia species (70–97% identity; average 86%) (Supplementary Table 2) reinforce our evolutionary scenario.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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This study is the first to measure evolutionary relationships between PAIs and/or PAI modules using comparative PAI genometrics, i.e. the simultaneous application to mobile GEs of tools developed for prokaryotic chromosome comparisons at nucleotide or gene levels. Since large PAIs usually result from successive additions of heterologous DNA modules, the identification of a common gene set in PAIs was essential for evaluating this overall strategy. We showed that dinucleotide signatures can be used as phylogenetic tools for PAI modules containing genes from the same origin, when applied to sequences not smaller than 30 kb. Consequently, tools have to be developed for highlighting segmentation in PAI modules that lack homology to identified sequences. Moreover, mobile GEs responsible for PAI emergence (including the Salmonella and Yersinia plasmids used here) can display distinct genome signatures when compared with their recipient chromosome. The latter GEs are not directly relevant to the understanding of ancestral PAI emergence, since their horizontal transfer can be accurately oriented by comparative genometrics of PAIs and mobile GEs.
Comparative PAI genometrics enabled us to orient PISYP horizontal transfers. Since conjugative plasmids containing type IV pilus genes have not been isolated from Yersinia or Photorhabdus, PISYP would have most probably emerged in bacteria such as Salmonella harboring conjugative plasmids and PAIs. This proposal is supported by dinucleotide frequency analyses: the YAPI- and Yersinia plasmids signatures diverge significantly, confirming the various origins of these GEs. Moreover, YAPI signatures are more closely related to those of Salmonella plasmids than those of Yersinia plasmids. All these data enable us to propose a parsimonious evolutionary scenario for YAPI emergence (Fig. 6). Since YAPI acquisition by Yersiniae is probably an ancient transfer event, this PAI would have progressively adopted the codon and nucleotide usage of the host (Hacker and Kaper, 2000), explaining the divergence of the YAPI and SPI-7 dinucleotide signatures. This nucleotide adaptation is a strong argument in favor of genome signatures as phylogenetic tools, when they are challenged using several representations of distance matrix comparisons. However, our scenario does not provide a time frame for the ancestral R64 plasmid integration into the Salmonella chromosome.
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In conclusion, this contribution reveals how comparative genometrics enables characterization of GEs responsible for the formation of PAIs or related modules (prophages, plasmids, transposons, etc.). Our multiscale, comparative approach opens up new horizons in the understanding of microbial genome evolution due to horizontal transfer in general and the emergence of pathogenic bacterial species by virulence gene transfer in particular.
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Acknowledgments |
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We warmly thank Philippe Marti and Ruedi Füllemann for providing DinucOne (preliminary dinucleotide analyses) and Philippe Moreillon, Christophe Carnoy and Jean-Claude Sirard for stimulating discussions. F.C. received a doctoral studentship from the French Ministère de l’Enseignement Supérieur, de la Recherche et de la Technologie and the Fondation pour la Recherche Médicale.
Conflict of Interest: none declared.
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FOOTNOTES |
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Associate Editor: Joaquin Dopazo
Received on July 27, 2005; revised on October 18, 2005; accepted on November 15, 2005
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