Extensive variation in surface lipoprotein gene content and genomic changes associated with virulence during evolution of a novel North American house finch epizootic strain of Mycoplasma gallisepticum. Microbiology

Department of Pathobiology and Veterinary Science and Center of Excellence for Vaccine Research, University of Connecticut, Storrs, CT, USA.
Microbiology (Impact Factor: 2.56). 05/2012; 158(Pt 8):2073-88. DOI: 10.1099/mic.0.058560-0
Source: PubMed


Mycoplasma gallisepticum, a significant respiratory and reproductive pathogen of domestic poultry, has since 1994 been recognized as an emergent pathogen of the American house finch (Carpodacus mexicanus). Epizootic spread and pathognomonic characteristics of house finch-associated Mycoplasma gallisepticum (HFMG) have been studied as a model of an emergent to endemic pathogen in a novel host. Here we present comparative analysis of eight HFMG genomes, including one from an index isolate and seven isolates separated spatially and temporally (1994-2008) across the epizootic, and notably having differences in virulence. HFMG represented a monophyletic clade relative to sequenced poultry isolates, with genomic changes indicating a novel M. gallisepticum lineage and including unique deletions of coding sequence. Though most of the HFMG genome was highly conserved among isolates, genetic distances correlated with temporal-spatial distance from the index. The most dramatic genomic differences among HFMG involved phase-variable and immunodominant VlhA lipoprotein genes, including those variable in presence and genomic location. Other genomic differences included tandem copy number variation of a 5 kbp repeat, changes in and adjacent to the clustered regularly interspaced short palindromic repeats, and small-scale changes affecting coding potential and association of genes with virulence. Divergence of monophyletic isolates from similar time/space in the epizootic indicated local diversification of distinct HFMG sublineages. Overall, these data identify candidate virulence genes and reveal the importance of phase-variable lipoproteins during the evolution of M. gallisepticum during its emergence and dissemination in a novel host in nature, likely mediating an important role at the interface between pathogen virulence and host immunity.

Full-text preview

Available from:
  • Source
    • "Although a well-documented bacterial pathogen of poultry world-wide, this marked the first epidemic of M. gallisepticum in wild birds [9]. Phylogenetic evidence shows a single origin for the epidemic and rapid evolutionary changes of the pathogen as it expanded geographically [7], [10]–[13] and in host range over time[10], [12], [14], [15]. The ongoing continent-wide epidemic in house finches and a local epidemic in Quebec in pine grosbeak Pinicola enucleator and evening grosbeak Coccothraustes vespertinus in 1998-99 was the result of a single successful host jump [11], [16]. "
    [Show abstract] [Hide abstract]
    ABSTRACT: Emerging infectious diseases often result from pathogens jumping to novel hosts. Identifying possibilities and constraints on host transfer is therefore an important facet of research in disease ecology. Host transfers can be studied for the bacterium Mycoplasma gallisepticum, predominantly a pathogen of poultry until its 1994 appearance and subsequent epidemic spread in a wild songbird, the house finch Haemorhous mexicanus and some other wild birds. We screened a broad range of potential host species for evidence of infection by M. gallisepticum in order to answer 3 questions: (1) is there a host phylogenetic constraint on the likelihood of host infection (house finches compared to other bird species); (2) does opportunity for close proximity (visiting bird feeders) increase the likelihood of a potential host being infected; and (3) is there seasonal variation in opportunity for host jumping (winter resident versus summer resident species). We tested for pathogen exposure both by using PCR to test for the presence of M. gallisepticum DNA and by rapid plate agglutination to test for the presence of antibodies. We examined 1,941 individual birds of 53 species from 19 avian families. In 27 species (15 families) there was evidence for exposure with M. gallisepticum although conjunctivitis was very rare in non-finches. There was no difference in detection rate between summer and winter residents, nor between feeder birds and species that do not come to feeders. Evidence of M. gallisepticum infection was found in all species for which at least 20 individuals had been sampled. Combining the present results with those of previous studies shows that a diverse range of wild bird species may carry or have been exposed to M. gallisepticum in the USA as well as in Europe and Asia.
    Full-text · Article · Jul 2014 · PLoS ONE
  • Source
    • "Owing to its relatively small genome (1 Mb) and its importance as a pathogen of poultry, the MG genome was sequenced over a decade ago (Papazisi et al 2003). More recently, the genomes of multiple isolates cultured from wildcaught , infected house finches at various times, and from various populations have been sequenced (Delaney et al. 2012; Tulman et al. 2012). Adding to its utility, this pathogen is easily stored longterm in frozen culture. "
    [Show abstract] [Hide abstract]
    ABSTRACT: Hamilton and Zuk proposed a good-genes model of sexual selection in which genetic variation can be maintained when females prefer ornaments that indicate resistance to parasites. When trait expression depends on a male's resistance, the co-adaptive cycles between host resistance and parasite virulence provide a mechanism in which genetic variation for fitness is continually renewed. The model made predictions at both the intraspecific and interspecific levels. In the three decades since its publication, these predictions have been theoretically examined in models of varying complexity, and empirically tested across many vertebrate and invertebrate taxa. Despite such prolonged interest, however, it has turned out to be extremely difficult to empirically demonstrate the process described, in part because we have not been able to test the underlying mechanisms that would unequivocally identify how parasites act as mediators of sexual selection. Here, we discuss how the use of high-throughput sequencing datasets available from modern genomic approaches might improve our ability to test this model. We expect that important contributions will come through the ability to identify and quantify the suite of parasites likely to influence the evolution of hosts' resistance, to confidently reconstruct phylogenies of both host and parasite taxa, and, perhaps most exciting, to detect generational cycles of heritable variants in populations of hosts and parasites. Integrative approaches, building on systems undergoing parasite-mediated selection with genomic resources already available, will be particularly useful in moving toward robust tests of this hypothesis. We finish by presenting case studies of well-studied host-parasite relationships that represent promising avenues for future research.
    Full-text · Article · May 2014 · Integrative and Comparative Biology
  • Source
    • "Finished NC95 13295-2-2P MGA1 Mycoplasma gallisepticum NC 018407 [63] "
    [Show abstract] [Hide abstract]
    ABSTRACT: The phytoplasmas are currently named using the Candidatus category, as the inability to grow them in vitro prevented (i) the performance of tests, such as DNA-DNA hybridization, that are regarded as necessary to establish species boundaries, and (ii) the deposition of type strains in culture collections. The recent accession to complete or nearly complete genome sequence information disclosed the opportunity to apply to the uncultivable phytoplasmas the same taxonomic approaches used for other bacteria. In this work, the genomes of 14 strains, belonging to the 16SrI, 16SrIII, 16SrV and 16SrX groups, including the species "Ca. P. asteris", "Ca. P. mali", "Ca. P. pyri", "Ca. P. pruni", and "Ca. P. australiense" were analyzed along with Acholeplasma laidlawi, to determine their taxonomic relatedness. Average nucleotide index (ANIm), tetranucleotide signature frequency correlation index (Tetra), and multilocus sequence analysis of 107 shared genes using both phylogenetic inference of concatenated (DNA and amino acid) sequences and consensus networks, were carried out. The results were in large agreement with the previously established 16S rDNA based classification schemes. Moreover, the taxonomic relationships within the 16SrI, 16SrIII and 16SrX groups, that represent clusters of strains whose relatedness could not be determined by 16SrDNA analysis, could be comparatively evaluated with non-subjective criteria. "Ca. P. mali" and "Ca. P. pyri" were found to meet the genome characteristics for the retention into two different, yet strictly related species; representatives of subgroups 16SrI-A and 16SrI-B were also found to meet the standards used in other bacteria to distinguish separate species; the genomes of the strains belonging to 16SrIII were found more closely related, suggesting that their subdivision into Candidatus species should be approached with caution.
    Full-text · Article · Sep 2013 · Systematic and Applied Microbiology
Show more