The influence of the accessory genome on bacterial pathogen evolution

Jackson, Robert W.; Vinatzer, Boris A.; Arnold, Dawn L.; Dorus, Steve; Murillo, Jesús

doi:10.4161/mge.1.1.16432

Cited by 112 publications

(96 citation statements)

References 121 publications

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“…These genomic regions can include phage genes and plasmid elements and may represent genomic islands acquired through horizontal gene transfer (26). Their loss or gain can be attributed to environmental adaptations that can influence antibiotic resistance, virulence, or host range restrictions (26,27). A recent study of M. abscessus subsp.…”

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confidence: 99%

Genome Sequencing of Mycobacterium abscessus Isolates from Patients in the United States and Comparisons to Globally Diverse Clinical Strains

et al. 2014

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f Nontuberculous mycobacterial infections caused by Mycobacterium abscessus are responsible for a range of disease manifestations from pulmonary to skin infections and are notoriously difficult to treat, due to innate resistance to many antibiotics. Previous population studies of clinical M. abscessus isolates utilized multilocus sequence typing or pulsed-field gel electrophoresis, but high-resolution examinations of genetic diversity at the whole-genome level have not been well characterized, particularly among clinical isolates derived in the United States. We performed whole-genome sequencing of 11 clinical M. abscessus isolates derived from eight U.S. patients with pulmonary nontuberculous mycobacterial infections, compared them to 30 globally diverse clinical isolates, and investigated intrapatient genomic diversity and evolution. Phylogenomic analyses revealed a cluster of closely related U.S. and Western European M. abscessus subsp. abscessus isolates that are genetically distinct from other European isolates and all Asian isolates. Large-scale variation analyses suggested genome content differences of 0.3 to 8.3%, relative to the reference strain ATCC 19977 T . Longitudinally sampled isolates showed very few single-nucleotide polymorphisms and correlated genomic deletion patterns, suggesting homogeneous infection populations. Our study explores the genomic diversity of clinical M. abscessus strains from multiple continents and provides insight into the genome plasticity of an opportunistic pathogen. N ontuberculous mycobacteria (NTM) represent a diverse group of environmental and pathogenic bacteria that are increasing in clinical prevalence in the United States (1) and other countries (2, 3). NTM are thought to be acquired primarily through environmental exposure (4), as they reside in water, biofilms, and soil environments (5, 6), although a few recent studies provide evidence of possible person-to person transmission among individuals with cystic fibrosis (CF) (7,8). Mycobacterium abscessus is the second most clinically prevalent NTM species in pulmonary NTM infections (1, 9, 10), with Mycobacterium avium complex (MAC) being the most prevalent. M. abscessus infections are challenging to treat because they are innately resistant to many antimicrobials, including some that are effective against Mycobacterium tuberculosis and other mycobacteria (11-13). Acquired antibiotic resistance has been observed in some M. abscessus strains, with mechanisms of resistance ranging from mutational resistance to aminoglycosides (14) to mutational (15) and inducible (16) resistance to macrolides.The current taxonomy of M. abscessus recognizes two subspecies, M. abscessus subsp. abscessus and M. abscessus subsp. bolletii (17), although recent population and comparative genomic studies support the three previously recognized subspecies, i.e., M. abscessus subsp. abscessus, M. abscessus subsp. massiliense, and M. abscessus subsp. bolletii (18)(19)(20)(21). This delineation is important because clinical studies suggest diff...

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confidence: 99%

Genome Sequencing of Mycobacterium abscessus Isolates from Patients in the United States and Comparisons to Globally Diverse Clinical Strains

et al. 2014

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“…Many of the horizontally acquired elements are virulence factors, including the (85). If acquisition of the regA locus preceded the acquisition of the LEE PAI, promiscuous derepression of H-NS and acquisition of the adcAand kfc-encoded adhesins may have been sufficient to induce asymptomatic colonization of the mouse intestinal lumen, placing C. rodentium in a "prepathogenic" state (8). Promiscuous H-NS derepression by RegA CR may also have played a role in the activation of the LEE PAI once it had been acquired, leading to the development of the RegA CR -LEE PAI interactions that are necessary for the full virulence of C. rodentium.…”

Section: Resultsmentioning

confidence: 99%

“…In particular, these data have revealed the frequency and ubiquity of horizontal gene transfer and how these events may have contributed to the development of bacterial pathogens (1)(2)(3)(4)(5)(6)(7)(8)(9)(10)(11). For example, the acquisition of the pPla and pMT1 plasmids catalyzed speciation of Yersinia pestis from Yersinia pseudotuberculosis (10), and the recent emergence of a new pathogenic strain of Escherichia coli, which caused a dramatic foodborne disease outbreak in Germany in 2011, is attributed to the horizontal transfer of a number of virulence determinants, including Shiga toxin, various adhesins and autotransporters, and the pESBL C227-11 plasmid (12)(13)(14).…”

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confidence: 99%

Evolutionary Adaptation of an AraC-Like Regulatory Protein in Citrobacter rodentium and Escherichia Species

et al. 2015

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dThe evolution of pathogenic bacteria is a multifaceted and complex process, which is strongly influenced by the horizontal acquisition of genetic elements and their subsequent expression in their new hosts. A well-studied example is the RegA regulon of the enteric pathogen Citrobacter rodentium. The RegA regulatory protein is a member of the AraC/XylS superfamily, which coordinates the expression of a gene repertoire that is necessary for full pathogenicity of this murine pathogen. Upon stimulation by an exogenous, gut-associated signal, namely, bicarbonate ions, RegA activates the expression of a series of genes, including virulence factors, such as autotransporters, fimbriae, a dispersin-like protein, and the grlRA operon on the locus of enterocyte effacement pathogenicity island. Interestingly, the genes encoding RegA homologues are distributed across the genus Escherichia, encompassing pathogenic and nonpathogenic subtypes. In this study, we carried out a series of bioinformatic, transcriptional, and functional analyses of the RegA regulons of these bacteria. Our results demonstrated that regA has been horizontally transferred to Escherichia spp. and C. rodentium. Comparative studies of two RegA homologues, namely, those from C. rodentium and E. coli SMS-3-5, a multiresistant environmental strain of E. coli, showed that the two regulators acted similarly in vitro but differed in terms of their abilities to activate the virulence of C. rodentium in vivo, which evidently was due to their differential activation of grlRA. Our data indicate that RegA from C. rodentium has strain-specific adaptations that facilitate infection of its murine host. These findings shed new light on the development of virulence by C. rodentium and on the evolution of virulence-regulatory genes of bacterial pathogens in general. Increases in the amount and availability of DNA sequence data have provided valuable insights into the ongoing speciation and evolution of bacteria. In particular, these data have revealed the frequency and ubiquity of horizontal gene transfer and how these events may have contributed to the development of bacterial pathogens (1-11). For example, the acquisition of the pPla and pMT1 plasmids catalyzed speciation of Yersinia pestis from Yersinia pseudotuberculosis (10), and the recent emergence of a new pathogenic strain of Escherichia coli, which caused a dramatic foodborne disease outbreak in Germany in 2011, is attributed to the horizontal transfer of a number of virulence determinants, including Shiga toxin, various adhesins and autotransporters, and the pESBL C227-11 plasmid (12-14).However, the acquisition of virulence determinants alone is often not sufficient to make a bacterium pathogenic. For example, the murine pathogen Citrobacter rodentium contains a large pathogenicity island known as the locus of enterocyte effacement (LEE PAI), which is required for colonic hyperplasia and the formation of attaching and effacing (A/E) lesions. Evidence indicates that the island has been horizontally mobilized in...

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“…The acquisition and maintenance of accessory genes on plasmids of bacteriophage via integration, horizontal gene transfer, and conjugation are responsible for genotype differentiation among many bacterial species (Jackson et al, 2011;Soares-Castro and Santos, 2014). The accessory genes often appear to move laterally between strains, thereby forming new trait combinations (Segerman, 2012).…”

Section: Introductionmentioning

confidence: 99%

Genomic variability of Pantoea ananatis in maize white spot lesions assessed by AFLP markers

et al. 2016

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ABSTRACT. Measures to control maize white spot (MWS) caused by Pantoea ananatis are preferentially based on resistant cultivars. A lack of knowledge on the genetic variability of pathogens could interfere with the development and utilization of controlling strategies in this pathosystem. The main goals of this study were to investigate the genetic variability of 90 P. ananatis isolates from three different eco-geographical regions of Brazil by amplified fragment length polymorphism (AFLP), and to determine the presence of a universal P. ananatis plasmid in isolates from tropical Brazil. Analysis of genetic similarity by AFLP allowed us to categorize the 90 isolates into two groups. However, no correlation between the collecting sites and genetic groupings was observed. The polymorphism percentage found in P. ananatis ranged between 24.64 and 92.46%, and genetic diversity was calculated to be 0.07-0.09. The analysis of molecular variance showed that 99.18% of genetic variability was within the populations, providing evidence that evolutionary forces were acting on these populations. All P. ananatis isolates showed the P. ananatis universal plasmid (280 or 352 kb). This is the first report on the presence of a universal P. ananatis plasmid from MWS lesions in the tropical area.

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The influence of the accessory genome on bacterial pathogen evolution

Cited by 112 publications

References 121 publications

Genome Sequencing of Mycobacterium abscessus Isolates from Patients in the United States and Comparisons to Globally Diverse Clinical Strains

Genome Sequencing of Mycobacterium abscessus Isolates from Patients in the United States and Comparisons to Globally Diverse Clinical Strains

Evolutionary Adaptation of an AraC-Like Regulatory Protein in Citrobacter rodentium and Escherichia Species

Genomic variability of Pantoea ananatis in maize white spot lesions assessed by AFLP markers

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