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Transcriptome Analyses of Immune System Behaviors in Primary Polyp of Coral Acropora digitifera Exposed to the Bacterial Pathogen Vibrio coralliilyticus under Thermal Loading

Abstract

Elevated sea surface temperature associated with global warming is a serious threat to coral reefs. Elevated temperatures directly or indirectly alter the distribution of coral-pathogen interactions and thereby exacerbate infectious coral diseases. The pathogenic bacterium Vibrio coralliilyticus is well-known as a causative agent of infectious coral disease. Rising sea surface temperature promotes the infection of corals by this bacterium, which causes several coral pathologies, such as bacterial bleaching, tissue lysis, and white syndrome. However, the effects of thermal stress on coral immune responses to the pathogen are poorly understood. To delineate the effects of thermal stress on coral immunity, we performed transcriptome analysis of aposymbiotic primary polyps of the reef-building coral Acropora digitifera exposed to V. coralliilyticus under thermal stress conditions. V. coralliilyticus infection of coral that was under thermal stress had negative effects on various molecular processes, including suppression of gene expression related to the innate immune response. In response to the pathogen, the coral mounted various responses including changes in protein metabolism, exosome release delivering signal molecules, extracellular matrix remodeling, and mitochondrial metabolism changes. Based on these results, we provide new insights into innate immunity of A. digitifera against pathogen infection under thermal stress conditions.

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Acknowledgments

For technical assistance with experiments and sequencing, we would like to thank Shinichi Yamasaki (DNA Sequencing Section, Okinawa Institute of Science and Technology Graduate University). We thank Prof. E. Stabb (Franklin College, University of Georgia) for generously providing conjugation protocols and materials.

Funding

This study was supported by JSPS Research Fellowship for Postdoctoral Researchers (TT, 17 J05024), Grant-in-Aid for Young Scientists (KAKENHI) (TT, 18 K14479), and a research grant from the Yamaguchi Educational and Scholarship Foundation (TT). This study was also partially supported by the Collaborative Research of Tropical Biosphere Research Center, University of the Ryukyus.

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Supplementary Fig. S1

Volcano plots showing coral genes that are differentially expressed at (a) 5 mpi (b) and 180 mpi after V. coralliilyticus infection compared to uninfected control. The red plots show a q-value ≤0.05 and a log2 fold change in transcript of >1 (up-regulated genes). The blue plots showed a q-value ≤0.05 and a log2 fold change in transcript of < −1 (down-regulated genes). (PPTX 4214 kb)

Table S1

Summary of quality trimming and mapping rates Table S2 Up-regulated DEGs at 30 mpi Table S3 Down-regulated DEGs at 30 mpi Table S4 Up-regulated DEGs at 60 mpi Table S5 Down-regulated DEGs at 60 mpi Table S6 Down-regulated GO categories enriched at 30 min post infection (with corrected P value ≤0.05; fold Enrichment >1.5; and number of genes ≥5) Table S7 Down-regulated GO categories enriched at 60 min post infection (with corrected P value ≤0.05; fold Enrichment >1.5; and number of genes ≥5) Table S8 Genes listed in “extracellular exosome” (GO:0070062) enriched at 30 mpi Table S9 Genes listed in “extracellular exosome” (GO:0070062) enriched at 60 mpi Table S10 Genes listed in “extracellular matrix” (GO:0031012) enriched at 30 mpi Table S11 Genes listed in “extracellular matrix” (GO:0031012) enriched at 60 mpi Table S12 Genes listed in “innate immune response” (GO:0045087) enriched at 60 mpi Table S13 Genes listed in “oxidation-reduction process” (GO:0055114) enriched at 60 mpi Table S14 Genes listed in “mitochondrion” (GO:0005739) enriched at 60 mpi Table S15 Genes listed in “mitochondrial respiratory chain complex I” (GO:0005747) enriched at 60 mpi Table S16 Genes listed in “mitochondrial inner membrane” (GO:0005743) enriched at 60 mpi (XLSX 131 kb)

Supplemental movie 1

Visualization of V. coralliilyticus infection using microscopic imaging. (MOV 4291 kb)

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Takagi, T., Yoshioka, Y., Zayasu, Y. et al. Transcriptome Analyses of Immune System Behaviors in Primary Polyp of Coral Acropora digitifera Exposed to the Bacterial Pathogen Vibrio coralliilyticus under Thermal Loading. Mar Biotechnol 22, 748–759 (2020). https://doi.org/10.1007/s10126-020-09984-1

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Keywords

  • Coral
  • Vibrio coralliilyticus
  • Thermal stress
  • Innate immunity
  • Transcriptome analysis
  • Immunosuppression