Antimicrobial and stress responses to increased temperature and bacterial pathogen challenge in the holobiont of a reef-building coral

Jeroen A.J.M. van de Water, Maryam Chaib De Mares, Groves B. Dixon, Jean Baptiste Raina, Bette L. Willis, David G. Bourne, Madeleine J.H. van Oppen

Research output: Contribution to journalArticleResearchpeer-review

9 Citations (Scopus)

Abstract

Global increases in coral disease prevalence have been linked to ocean warming through changes in coral-associated bacterial communities, pathogen virulence and immune system function. However, the interactive effects of temperature and pathogens on the coral holobiont are poorly understood. Here, we assessed three compartments of the holobiont (host, Symbiodinium and bacterial community) of the coral Montipora aequituberculata challenged with the pathogen Vibrio coralliilyticus and the commensal bacterium Oceanospirillales sp. under ambient (27°C) and elevated (29.5 and 32°C) seawater temperatures. Few visual signs of bleaching and disease development were apparent in any of the treatments, but responses were detected in the holobiont compartments. V. coralliilyticus acted synergistically and negatively impacted the photochemical efficiency of Symbiodinium at 32°C, while Oceanospirillales had no significant effect on photosynthetic efficiency. The coral, however, exhibited a minor response to the bacterial challenges, with the response towards V. coralliilyticus being significantly more pronounced, and involving the prophenoloxidase-activating system and multiple immune system-related genes. Elevated seawater temperatures did not induce shifts in the coral-associated bacterial community, but caused significant gene expression modulation in both Symbiodinium and the coral host. While Symbiodinium exhibited an antiviral response and upregulated stress response genes, M. aequituberculata showed regulation of genes involved in stress and innate immune response processes, including immune and cytokine receptor signalling, the complement system, immune cell activation and phagocytosis, as well as molecular chaperones. These observations show that M. aequituberculata is capable of maintaining a stable bacterial community under elevated seawater temperatures and thereby contributes to preventing disease development.

Original languageEnglish
Pages (from-to)1065-1080
Number of pages16
JournalMolecular Ecology
Volume27
Issue number4
DOIs
Publication statusPublished - 1 Feb 2018
Externally publishedYes

Keywords

  • bacteria
  • climate change
  • coral
  • disease
  • holobiont
  • immune response
  • Oceanospirillales
  • Symbiodinium
  • symbiosis
  • Vibrio coralliilyticus

Cite this

van de Water, J. A. J. M., Chaib De Mares, M., Dixon, G. B., Raina, J. B., Willis, B. L., Bourne, D. G., & van Oppen, M. J. H. (2018). Antimicrobial and stress responses to increased temperature and bacterial pathogen challenge in the holobiont of a reef-building coral. Molecular Ecology, 27(4), 1065-1080. https://doi.org/10.1111/mec.14489
van de Water, Jeroen A.J.M. ; Chaib De Mares, Maryam ; Dixon, Groves B. ; Raina, Jean Baptiste ; Willis, Bette L. ; Bourne, David G. ; van Oppen, Madeleine J.H. / Antimicrobial and stress responses to increased temperature and bacterial pathogen challenge in the holobiont of a reef-building coral. In: Molecular Ecology. 2018 ; Vol. 27, No. 4. pp. 1065-1080.
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abstract = "Global increases in coral disease prevalence have been linked to ocean warming through changes in coral-associated bacterial communities, pathogen virulence and immune system function. However, the interactive effects of temperature and pathogens on the coral holobiont are poorly understood. Here, we assessed three compartments of the holobiont (host, Symbiodinium and bacterial community) of the coral Montipora aequituberculata challenged with the pathogen Vibrio coralliilyticus and the commensal bacterium Oceanospirillales sp. under ambient (27°C) and elevated (29.5 and 32°C) seawater temperatures. Few visual signs of bleaching and disease development were apparent in any of the treatments, but responses were detected in the holobiont compartments. V. coralliilyticus acted synergistically and negatively impacted the photochemical efficiency of Symbiodinium at 32°C, while Oceanospirillales had no significant effect on photosynthetic efficiency. The coral, however, exhibited a minor response to the bacterial challenges, with the response towards V. coralliilyticus being significantly more pronounced, and involving the prophenoloxidase-activating system and multiple immune system-related genes. Elevated seawater temperatures did not induce shifts in the coral-associated bacterial community, but caused significant gene expression modulation in both Symbiodinium and the coral host. While Symbiodinium exhibited an antiviral response and upregulated stress response genes, M. aequituberculata showed regulation of genes involved in stress and innate immune response processes, including immune and cytokine receptor signalling, the complement system, immune cell activation and phagocytosis, as well as molecular chaperones. These observations show that M. aequituberculata is capable of maintaining a stable bacterial community under elevated seawater temperatures and thereby contributes to preventing disease development.",
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van de Water, JAJM, Chaib De Mares, M, Dixon, GB, Raina, JB, Willis, BL, Bourne, DG & van Oppen, MJH 2018, 'Antimicrobial and stress responses to increased temperature and bacterial pathogen challenge in the holobiont of a reef-building coral', Molecular Ecology, vol. 27, no. 4, pp. 1065-1080. https://doi.org/10.1111/mec.14489

Antimicrobial and stress responses to increased temperature and bacterial pathogen challenge in the holobiont of a reef-building coral. / van de Water, Jeroen A.J.M.; Chaib De Mares, Maryam; Dixon, Groves B.; Raina, Jean Baptiste; Willis, Bette L.; Bourne, David G.; van Oppen, Madeleine J.H.

In: Molecular Ecology, Vol. 27, No. 4, 01.02.2018, p. 1065-1080.

Research output: Contribution to journalArticleResearchpeer-review

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AU - van de Water, Jeroen A.J.M.

AU - Chaib De Mares, Maryam

AU - Dixon, Groves B.

AU - Raina, Jean Baptiste

AU - Willis, Bette L.

AU - Bourne, David G.

AU - van Oppen, Madeleine J.H.

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AB - Global increases in coral disease prevalence have been linked to ocean warming through changes in coral-associated bacterial communities, pathogen virulence and immune system function. However, the interactive effects of temperature and pathogens on the coral holobiont are poorly understood. Here, we assessed three compartments of the holobiont (host, Symbiodinium and bacterial community) of the coral Montipora aequituberculata challenged with the pathogen Vibrio coralliilyticus and the commensal bacterium Oceanospirillales sp. under ambient (27°C) and elevated (29.5 and 32°C) seawater temperatures. Few visual signs of bleaching and disease development were apparent in any of the treatments, but responses were detected in the holobiont compartments. V. coralliilyticus acted synergistically and negatively impacted the photochemical efficiency of Symbiodinium at 32°C, while Oceanospirillales had no significant effect on photosynthetic efficiency. The coral, however, exhibited a minor response to the bacterial challenges, with the response towards V. coralliilyticus being significantly more pronounced, and involving the prophenoloxidase-activating system and multiple immune system-related genes. Elevated seawater temperatures did not induce shifts in the coral-associated bacterial community, but caused significant gene expression modulation in both Symbiodinium and the coral host. While Symbiodinium exhibited an antiviral response and upregulated stress response genes, M. aequituberculata showed regulation of genes involved in stress and innate immune response processes, including immune and cytokine receptor signalling, the complement system, immune cell activation and phagocytosis, as well as molecular chaperones. These observations show that M. aequituberculata is capable of maintaining a stable bacterial community under elevated seawater temperatures and thereby contributes to preventing disease development.

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KW - climate change

KW - coral

KW - disease

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KW - immune response

KW - Oceanospirillales

KW - Symbiodinium

KW - symbiosis

KW - Vibrio coralliilyticus

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