Coral-mucus-associated <i>Vibrio</i> integrons in the Great Barrier Reef: genomic hotspots for environmental adaptation

Koenig, Jeremy E.; Bourne, David G.; Curtis, Bruce A.; Dlutek, Marlena; Stokes, H. W.; Doolittle, W. Ford; Boucher, Yan

doi:10.1038/ismej.2010.193

Cited by 38 publications

(42 citation statements)

References 73 publications

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“…VcP1, in contrast, contains 12 unique prophage, transposon and integron regions, as well as a unique flagellar operon. This is consistent with a recent report that closely related Vibrio strains harbor unique integrons as a result of lateral gene transfer (Koenig et al, 2011). Further, genomic comparison at the nucleotide level shows a substantial level of divergence, ANIb (average nucleotide identity via BLAST) ¼ 96.6, between the two strains (Goris et al 2007).…”

Section: Resultssupporting

confidence: 79%

Temperature regulation of virulence factors in the pathogen Vibrio coralliilyticus

Kimes

Grim

Johnson³

et al. 2011

The ISME Journal

230

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Sea surface temperatures (SST) are rising because of global climate change. As a result, pathogenic Vibrio species that infect humans and marine organisms during warmer summer months are of growing concern. Coral reefs, in particular, are already experiencing unprecedented degradation worldwide due in part to infectious disease outbreaks and bleaching episodes that are exacerbated by increasing SST. For example, Vibrio coralliilyticus, a globally distributed bacterium associated with multiple coral diseases, infects corals at temperatures above 27 1C. The mechanisms underlying this temperature-dependent pathogenicity, however, are unknown. In this study, we identify potential virulence mechanisms using whole genome sequencing of V. coralliilyticus ATCC (American Type Culture Collection) BAA-450. Furthermore, we demonstrate direct temperature regulation of numerous virulence factors using proteomic analysis and bioassays. Virulence factors involved in motility, host degradation, secretion, antimicrobial resistance and transcriptional regulation are upregulated at the higher virulent temperature of 27 1C, concurrent with phenotypic changes in motility, antibiotic resistance, hemolysis, cytotoxicity and bioluminescence. These results provide evidence that temperature regulates multiple virulence mechanisms in V. coralliilyticus, independent of abundance. The ecological and biological significance of this temperature-dependent virulence response is reinforced by climate change models that predict tropical SST to consistently exceed 27 1C during the spring, summer and fall seasons. We propose V. coralliilyticus as a model Gram-negative bacterium to study temperature-dependent pathogenicity in Vibrio-related diseases.

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Section: Resultssupporting

confidence: 79%

Temperature regulation of virulence factors in the pathogen Vibrio coralliilyticus

Kimes

Grim

Johnson³

et al. 2011

The ISME Journal

230

200

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“…Interestingly, however, in cases where the function can be inferred it appears that the gene products produced from the cassettes are often involved in interactions with the environment that may be subject to rapid change (for example, functions associated with host interactions and virulence, interaction with phages and biofilm formation). This suggests that our results are relevant beyond shorter mobile integrons of classes 1-3, and that the extraordinary gene-cassette diversity in chromosomal integrons in environmental bacteria (for example, Gillings et al, 2009;Boucher et al, 2011;Koenig et al, 2011) can be explained by positive selection for an active integron integrase.…”

Section: Evolutionary Dynamics Of Integronsmentioning

confidence: 85%

The evolutionary dynamics of integrons in changing environments

2016

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Integrons are genetic elements that are common in bacteria and are hotspots for genome evolution. They facilitate the acquisition and reassembly of gene cassettes encoding a variety of functions, including drug resistance. Despite their importance in clinical settings, the selective forces responsible for the evolution and maintenance of integrons are poorly understood. We present a mathematical model of integron evolution within bacterial populations subject to fluctuating antibiotic exposures. Bacteria carrying a functional integrase that mediates reshuffling of cassette genes and thereby modulates gene expression patterns compete with bacteria without a functional integrase. Our results indicate that for a wide range of parameters, the functional integrase can be stably maintained in the population despite substantial fitness costs. This selective advantage arises because gene-cassette shuffling generates genetic diversity, thus enabling the population to respond rapidly to changing selective pressures. We also show that horizontal gene transfer promotes stable maintenance of the integrase and can also lead to de novo assembly of integrons. Our model generates testable predictions for integron evolution, including loss of functional integrases in stable environments and selection for intermediate gene-shuffling rates in changing environments. Our results highlight the need for experimental studies of integron population biology.

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“…in the same samples as those in which orf C-LIM1 , orf C-LIM27 and orf C-LIM37 gene cassettes were found. This link between the gene cassette pools of CIs and RIs has previously been described (Mazel, 2006;LeRoux et al, 2009;Koenig et al, 2011).…”

mentioning

confidence: 76%

Quantitative and qualitative impact of hospital effluent on dissemination of the integron pool

et al. 2013

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There is increasing evidence that human activity, and especially the resulting effluent, has a major role in the dissemination of bacterial antibiotic-resistance determinants in the environment. Hospitals are the major antibiotic consumers and thus facilitate the spread of antibiotic resistance. Questions are increasingly being raised about the management of hospital effluents, but their involvement in antibiotic-resistance dissemination has never been assessed. Integrons are a paradigm of genetic transfer between the environmental resistome and both commensal and pathogenic bacteria. In order to assess the impact of hospital activities on antibiotic-resistance dissemination in the environment, we monitored integrons and their gene cassettes in hospital effluents, and their release in the environment. We found that bacterial communities present in a hospital effluent contained a high proportion of integrons. In terms of both their gene cassette diversity and gene cassette arrays, the urban effluent and municipal wastewater treatment plant (WWTP) influent were most similar, whereas the hospital effluent and recirculation sludge exhibited very specific patterns. We found that anthropogenic activities led to the release of abundant integrons and antibiotic-resistance gene cassettes, but we observed no specific impact of hospital activities on the receiving environment. Furthermore, although the WWTP did not reduce the normalized integron copy number, it reduced the diversity of gene cassette arrays contained in the raw wastewater, underlining the effect of the biological treatment on the anthropogenic integron pool arriving at the WWTP.

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Coral-mucus-associated Vibrio integrons in the Great Barrier Reef: genomic hotspots for environmental adaptation

Cited by 38 publications

References 73 publications

Temperature regulation of virulence factors in the pathogen Vibrio coralliilyticus

Temperature regulation of virulence factors in the pathogen Vibrio coralliilyticus

The evolutionary dynamics of integrons in changing environments

Quantitative and qualitative impact of hospital effluent on dissemination of the integron pool

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