Abstract
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 °C. 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 °C, 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 °C 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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Acknowledgements
This work was supported by NSF Biodiversity Surveys and Inventories (DEB 0516347, DEB 0964997) to PJM, a NSF Foundation Graduate Research Fellowship to NEK, the NOAA OHHI Distinguished Scholars program to RCC, and NOAA (SO660009) and NIH (1R01A139129-01) to RRC. Sequencing support was received from the Office of the Chief Scientist (USA), University of Maryland Vibrio Genome Sequencing Project and the Los Alamos National Laboratory. The Fellowship for Interpretation of Genomes (FIG, Argonne National Laboratory) and the National Institute of Allergy and Infectious Diseases (NIH) were instrumental in supporting the RAST and the SEED data analysis environments. We thank Veronika Vonstein and Ross Overbeek for their assistance with the RAST system, Lisa Kilpatrick (NIST) and Kevin Schey/Jennifer Bethard (MUSC Mass Spectrometry Facility) for the use of their facilities to perform the two-dimensional liquid chromatography coupled with tandem mass spectrometry experiments, and Jana Lee (Proteome Software) for assistance in using the Scaffold software.
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Kimes, N., Grim, C., Johnson, W. et al. Temperature regulation of virulence factors in the pathogen Vibrio coralliilyticus. ISME J 6, 835–846 (2012). https://doi.org/10.1038/ismej.2011.154
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DOI: https://doi.org/10.1038/ismej.2011.154
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