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Recombination in the genome of Chlamydia trachomatis involving the polymorphic membrane protein C gene relative to ompA and evidence for horizontal gene transfer.

ABSTRACT: Genome sequencing of Chlamydia trachomatis serovar D has identified polymorphic membrane proteins (Pmp) that are a newly recognized protein family unique to the Chlamydiaceae family. Cumulative data suggest that these diverse proteins are expressed on the cell surface and might be immunologically important. We performed phylogenetic analyses and statistical modeling with 18 reference serovars and 1 genovariant of C. trachomatis to examine the evolutionary characteristics and comparative genetics of PmpC and pmpC, the gene that encodes this protein. We also examined 12 recently isolated ocular and urogenital clinical samples, since reference serovars are laboratory adapted and may not represent strains that are presently responsible for human disease. Phylogenetic reconstructions revealed a clear distinction for disease groups, corresponding to levels of tissue specificity and virulence of the organism. Further, the most prevalent serovars, E, F, and Da, formed a distinct clade. According to the results of comparative genetic analyses, these three genital serovars contained two putative insertion sequence (IS)-like elements with 10- and 15-bp direct repeats, respectively, while all other genital serovars contained one IS-like element. Ocular trachoma serovars also contained both insertions. Previously, no IS-like elements have been identified for Chlamydiaceae. Surprisingly, 7 (58%) of 12 clinical isolates revealed pmpC sequences that were identical to the sequences of other serovars, providing clear evidence for a high rate of whole-gene recombination. Recombination and the differential presence of IS-like elements among distinct disease and prevalence groups may contribute to genome plasticity, which may lead to adaptive changes in tissue tropism and pathogenesis over the course of the organism's evolution.

SUBMITTER: Gomes JP

PROVIDER: S-EPMC421610 | biostudies-literature | 2004 Jul

REPOSITORIES: biostudies-literature

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Recombination in the genome of Chlamydia trachomatis involving the polymorphic membrane protein C gene relative to ompA and evidence for horizontal gene transfer.

Gomes João P JP Bruno William J WJ Borrego Maria J MJ Dean Deborah D

Journal of bacteriology 20040701 13

Genome sequencing of Chlamydia trachomatis serovar D has identified polymorphic membrane proteins (Pmp) that are a newly recognized protein family unique to the Chlamydiaceae family. Cumulative data suggest that these diverse proteins are expressed on the cell surface and might be immunologically important. We performed phylogenetic analyses and statistical modeling with 18 reference serovars and 1 genovariant of C. trachomatis to examine the evolutionary characteristics and comparative genetics ...[more]

PMID: 15205432

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Project description:BackgroundSerovars of the human pathogen Chlamydia trachomatis occupy one of three specific tissue niches. Genomic analyses indicate that the serovars have a phylogeny congruent with their pathobiology and have an average substitution rate of less than one nucleotide per kilobase. In contrast, the gene that determines serovar specificity, ompA, has a phylogenetic association that is not congruent with tissue tropism and has a degree of nucleotide variability much higher than other genomic loci. The ompA gene encodes the major surface-exposed antigenic determinant, and the observed nucleotide diversity at the ompA locus is thought to be due to recombination and host immune selection pressure. The possible contribution of a localized increase in mutation rate, however, has not been investigated.ResultsNucleotide diversity and phylogenetic relationships of the five constant and four variable domains of the ompA gene, as well as several loci surrounding ompA, were examined for each serovar. The loci flanking the ompA gene demonstrated that nucleotide diversity increased monotonically as ompA is approached and that their gene trees are not congruent with either ompA or tissue tropism. The variable domains of the ompA gene had a very high level of non-synonymous change, which is expected as these regions encode the surface-exposed epitopes and are under positive selection. However, the synonymous changes are clustered in the variable regions compared to the constant domains; if hitchhiking were to account for the increase in synonymous changes, these substitutions should be more evenly distributed across the gene. Recombination also cannot entirely account for this increase as the phylogenetic relationships of the constant and variable domains are congruent with each other.ConclusionsThe high number of synonymous substitutions observed within the variable domains of ompA appears to be due to an increased mutation rate within this region of the genome, whereas the increase in nucleotide substitution rate and the lack of phylogenetic congruence in the regions flanking ompA are characteristic motifs of gene conversion. Together, the increased mutation rate in the ompA gene, in conjunction with gene conversion and positive selection, results in a high degree of variability that promotes host immune evasion.

Project description:BackgroundWe report on the probable horizontal transfer of a mitochondrial gene, cytb, between species of Neotropical bruchid beetles, in a zone where these species are sympatric. The bruchid beetles Acanthoscelides obtectus, A. obvelatus, A. argillaceus and Zabrotes subfasciatus develop on various bean species in Mexico. Whereas A. obtectus and A. obvelatus develop on Phaseolus vulgaris in the Mexican Altiplano, A. argillaceus feeds on P. lunatus in the Pacific coast. The generalist Z. subfasciatus feeds on both bean species, and is sympatric with A. obtectus and A. obvelatus in the Mexican Altiplano, and with A. argillaceus in the Pacific coast. In order to assess the phylogenetic position of these four species, we amplified and sequenced one nuclear (28S rRNA) and two mitochondrial (cytb, COI) genes.ResultsWhereas species were well segregated in topologies obtained for COI and 28S rRNA, an unexpected pattern was obtained in the cytb phylogenetic tree. In this tree, individuals from A. obtectus and A. obvelatus, as well as Z. subfasciatus individuals from the Mexican Altiplano, clustered together in a unique little variable monophyletic unit. In contrast, A. argillaceus and Z. subfasciatus individuals from the Pacific coast clustered in two separated clades, identically to the pattern obtained for COI and 28S rRNA. An additional analysis showed that Z. subfasciatus individuals from the Mexican Altiplano also possessed the cytb gene present in individuals of this species from the Pacific coast. Zabrotes subfasciatus individuals from the Mexican Altiplano thus demonstrated two cytb genes, an "original" one and an "infectious" one, showing 25% of nucleotide divergence. The "infectious" cytb gene seems to be under purifying selection and to be expressed in mitochondria.ConclusionThe high degree of incongruence of the cytb tree with patterns for other genes is discussed in the light of three hypotheses: experimental contamination, hybridization, and pseudogenisation. However, none of these seem able to explain the patterns observed. A fourth hypothesis, involving recent horizontal gene transfer (HGT) between A. obtectus and A. obvelatus, and from one of these species to Z. subfasciatus in the Mexican Altiplano, seems the only plausible explanation. The HGT between our study species seems to have occurred recently, and only in a zone where the three beetles are sympatric and share common host plants. This suggests that transfer could have been effected by some external vector such as a eukaryotic or viral parasite, which might still host the transferred fragment.ReviewersThis article was reviewed by Eric Bapteste, Adam Eyre-Walker and Alexey Kondrashov.

Project description:Lateral gene transfer (LGT) among Chlamydia trachomatis strains is common, in both isolates generated in the laboratory and those examined directly from patients. In contrast, there are very few examples of recent acquisition of DNA by any Chlamydia spp. from any other species. Interspecies LGT in this system was analyzed using crosses of tetracycline (Tc)-resistant C. trachomatis L2/434 and chloramphenicol (Cam)-resistant C. muridarum VR-123. Parental C. muridarum strains were created using a plasmid-based Himar transposition system, which led to integration of the Camr marker randomly across the chromosome. Fragments encompassing 79% of the C. muridarum chromosome were introduced into a C. trachomatis background, with the total coverage contained on 142 independent recombinant clones. Genome sequence analysis of progeny strains identified candidate recombination hot spots, a property not consistent with in vitro C. trachomatis × C. trachomatis (intraspecies) crosses. In both interspecies and intraspecies crosses, there were examples of duplications, mosaic recombination endpoints, and recombined sequences that were not linked to the selection marker. Quantitative analysis of the distribution and constitution of inserted sequences indicated that there are different constraints on interspecies LGT than on intraspecies crosses. These constraints may help explain why there is so little evidence of interspecies genetic exchange in this system, which is in contrast to very widespread intraspecies exchange in C. trachomatis IMPORTANCE Genome sequence analysis has demonstrated that there is widespread lateral gene transfer among strains within the species C. trachomatis and with other closely related Chlamydia species in laboratory experiments. This is in contrast to the complete absence of foreign DNA in the genomes of sequenced clinical C. trachomatis strains. There is no understanding of any mechanisms of genetic transfer in this important group of pathogens. In this report, we demonstrate that interspecies genetic exchange can occur but that the nature of the fragments exchanged is different than those observed in intraspecies crosses. We also generated a large hybrid strain library that can be exploited to examine important aspects of chlamydial disease.

Dataset Information

Recombination in the genome of Chlamydia trachomatis involving the polymorphic membrane protein C gene relative to ompA and evidence for horizontal gene transfer.

Publications

Recombination in the genome of Chlamydia trachomatis involving the polymorphic membrane protein C gene relative to ompA and evidence for horizontal gene transfer.

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