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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

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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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References

  • Arboleda M, Reichardt W (2009) Epizoic communities of prokaryotes on healthy and diseased scleractinian corals in Lingayen gulf, Philippines. Microb Ecol 57:117–128

    PubMed  Google Scholar 

  • Arnoult D, Soares F, Tattoli I, Girardin SE (2011) Mitochondria in innate immunity. EMBO Rep 12:901–910

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bachère E (2003) Anti-infectious immune effectors in marine invertebrates: potential tools for disease control in larviculture. Aquaculture 227:427–438

    Google Scholar 

  • Bai Y, Onuma H, Bai X, Medvedev AV, Misukonis M, Weinberg JB, Cao W, Robidoux J, Floering LM, Daniel KW, Collins S (2005) Persistent nuclear factor-κB activation in Ucp2−/− mice leads to enhanced nitric oxide and inflammatory cytokine production. J Biol Chem 280:19062–19069

    CAS  PubMed  Google Scholar 

  • Baird AH, Guest JR, Willis BL (2009) Systematic and biogeographical patterns in the reproductive biology of scleractinian corals. Annu Rev Ecol Evol Syst 40:551–571

    Google Scholar 

  • Ben-Haim Y, Zicherman-Keren M, Rosenberg E (2003) Temperature-regulated bleaching and lysis of the coral Pocillopora damicornis by the novel pathogen Vibrio coralliilyticus. Appl Environ Microbiol 69:4236–4242

    CAS  PubMed  PubMed Central  Google Scholar 

  • Berkelmans R, Van Oppen MJ (2006) The role of zooxanthellae in the thermal tolerance of corals: a ‘nugget of hope’ for coral reefs in an era of climate change. Proc R Soc B 273:2305–2312

    PubMed  PubMed Central  Google Scholar 

  • Bourne DG, Garren M, Work TM, Rosenberg E, Smith GW, Harvell CD (2009) Microbial disease and the coral holobiont. Trends Microbiol 17:554–562

    CAS  PubMed  Google Scholar 

  • Bray NL, Pimentel H, Melsted P, Pachter L (2016) Near-optimal probabilistic RNA-seq quantification. Nat Biotechnol 34:525–527

    CAS  PubMed  Google Scholar 

  • Brennan JJ, Messerschmidt JL, Williams LM, Matthews BJ, Reynoso M, Gilmore TD (2017) Sea anemone model has a single toll-like receptor that can function in pathogen detection, NF-κB signal transduction, and development. Proc Natl Acad Sci U S A 114:E10122–E10131

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bruno JF, Selig ER, Casey KS, Page CA, Willis BL, Harvell CD, Sweatman H, Melendy AM (2007) Thermal stress and coral cover as drivers of coral disease outbreaks. PLoS Biol 5:e124

    PubMed  PubMed Central  Google Scholar 

  • Burge CA, Mouchka ME, Harvell CD, Roberts S (2013) Immune response of the Caribbean Sea fan, Gorgonia ventalina, exposed to an Aplanochytrium parasite as revealed by transcriptome sequencing. Front Physiol 4:180

    PubMed  PubMed Central  Google Scholar 

  • Clayton A, Turkes A, Dewitt S, Steadman R, Mason MD, Hallett MB (2004) Adhesion and signaling by B cell-derived exosomes: the role of integrins. FASEB J 18:977–979

    CAS  PubMed  Google Scholar 

  • Cooper EL (2010) Evolution of immune systems from self/not self to danger to artificial immune systems (AIS). Phys Life Rev 7:55–78

    PubMed  Google Scholar 

  • Dalle-Donne I, Rossi R, Colombo R, Giustarini D, Milzani A (2006) Biomarkers of oxidative damage in human disease. Clin Chem 52:601–623

    CAS  PubMed  Google Scholar 

  • DeSalvo MK, Voolstra CR, Sunagawa S, Schwarz JA, Stillman JH, Coffroth MA, Szmant AM, Medina M (2008) Differential gene expression during thermal stress and bleaching in the Caribbean coral Montastraea faveolata. Mol Ecol 17:3952–3971

    CAS  PubMed  Google Scholar 

  • Dunn AK, Millikan DS, Adin DM, Bose JL, Stabb EV (2006) New rfp- and pES213-derived tools for analyzing symbiotic Vibrio fischeri reveal patterns of infection and lux expression in situ. Appl Environ Microbiol 72:802–810

    CAS  PubMed  PubMed Central  Google Scholar 

  • Emre Y, Hurtaud C, Nübel T, Criscuolo F, Ricquier D, Cassard-Doulcier A (2007) Mitochondria contribute to LPS-induced MAPK activation via uncoupling protein UCP2 in macrophages. Biochem J 402:271–278

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fuess LE, Mann WT, Jinks LR, Brinkhuis V, Mydlarz LD (2018) Transcriptional analyses provide new insight into the late-stage immune response of a diseased Caribbean coral. R Soc Open Sci 5:172062

    PubMed  PubMed Central  Google Scholar 

  • Garren M, Son K, Tout J, Seymour JR, Stocker R (2016) Temperature-induced behavioral switches in a bacterial coral pathogen. ISME J 10:1363–1372

    CAS  PubMed  Google Scholar 

  • Gestal C, Costa M, Figueras A, Novoa B (2007) Analysis of differentially expressed genes in response to bacterial stimulation in hemocytes of the carpet-shell clam Ruditapes decussatus: identification of new antimicrobial peptides. Gene 406:134–143

    CAS  PubMed  Google Scholar 

  • Gostner JM, Becker K, Fuchs D, Sucher R (2013) Redox regulation of the immune response. Redox Rep 18:88–94

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hakulinen J, Sankkila L, Sugiyama N, Lehti K, Keski-Oja J (2008) Secretion of active membrane type 1 matrix metalloproteinase (MMP-14) into extracellular space in microvesicular exosomes. J Cell Biochem 105:1211–1218

    CAS  PubMed  Google Scholar 

  • Hall CJ, Boyle RH, Astin JW, Flores MV, Oehlers SH, Sanderson LE, Ellett F, Lieschke GJ, Crosier KE, Crosier PS (2013) Immunoresponsive gene 1 augments bactericidal activity of macrophage-lineage cells by regulating β-oxidation-dependent mitochondrial ROS production. Cell Metab 18:265–278

    CAS  PubMed  Google Scholar 

  • Hamada M, Shoguchi E, Shinzato C, Kawashima T, Miller DJ, Satoh N (2012) The complex NOD-like receptor repertoire of the coral Acropora digitifera includes novel domain combinations. Mol Biol Evol 30:167–176

    PubMed  Google Scholar 

  • Harvell CD, Mitchell CE, Ward JR, Altizer S, Dobson AP, Ostfeld RS, Samuel MD (2002) Climate warming and disease risks for terrestrial and marine biota. Science 296:2158–2162

    CAS  PubMed  Google Scholar 

  • Harvell D, Jordán-Dahlgren E, Merkel S, Rosenberg E, Raymundo L, Smith G, Weil E, Willis B (2007) Coral disease, environmental drivers, and the balance between coral and microbial associates. Oceanography 20:172–195

    Google Scholar 

  • Hayashibara T, Shimoike K, Kimura T, Hosaka S, Heyward A, Harrison P, Kudo K, Omori M (1993) Patterns of coral spawning at Akajima Island, Okinawa, Japan. Mar Ecol Prog Ser 101:253–262

    Google Scholar 

  • Helman Y, Natale F, Sherrell RM, LaVigne M, Starovoytov V, Gorbunov MY, Falkowski PG (2008) Extracellular matrix production and calcium carbonate precipitation by coral cells in vitro. Proc Natl Acad Sci U S A 105:54–58

    CAS  PubMed  Google Scholar 

  • Heron SF, Willis BL, Skirving WJ, Eakin CM, Page CA, Miller IR (2010) Summer hot snaps and winter conditions: modelling white syndrome outbreaks on great barrier reef corals. PLoS One 5:e12210

    PubMed  PubMed Central  Google Scholar 

  • Howells E, Beltran V, Larsen N, Bay L, Willis B, Van Oppen M (2012) Coral thermal tolerance shaped by local adaptation of photosymbionts. Nat Clim Chang 2:116–120

    Google Scholar 

  • Hu G, Gong A, Roth AL, Huang BQ, Ward HD, Zhu G, Larusso NF, Hanson ND, Chen X (2013) Release of luminal exosomes contributes to TLR4-mediated epithelial antimicrobial defense. PLoS Pathog 9:e1003261

    CAS  PubMed  PubMed Central  Google Scholar 

  • Huang DW, Sherman BT, Lempicki RA (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4:44–57

    CAS  Google Scholar 

  • Hynes RO (2009) The extracellular matrix: not just pretty fibrils. Science 326:1216–1219

    CAS  PubMed  PubMed Central  Google Scholar 

  • Inoue M, Shinmen K, Kawahata H, Nakamura T, Tanaka Y, Kato A, Shinzato C, Iguchi A, Kan H, Suzuki A, Sakai K (2012) Estimate of calcification responses to thermal and freshening stresses based on culture experiments with symbiotic and aposymbiotic primary polyps of a coral, Acropora digitifera. Glob Planet Chang 92:1–7

    Google Scholar 

  • Iwao K, Fujisawa T, Hatta M (2002) A cnidarian neuropeptide of the GLWamide family induces metamorphosis of reef-building corals in the genus Acropora. Coral Reefs 21:127–129

    Google Scholar 

  • James R, Thampuran N, Lalitha KV, Rajan LA, Joseph TC (2010) Differential gene expression profile of the hepatopancreas of white spot syndrome virus infected Fenneropenaeus indicus by suppression subtractive hybridization. Fish Shellfish Immunol 29:884–889

    CAS  PubMed  Google Scholar 

  • Kanneganti T, Lamkanfi M, Núñez G (2007) Intracellular NOD-like receptors in host defense and disease. Immunity 27:549–559

    CAS  PubMed  Google Scholar 

  • Kimes NE, Grim CJ, Johnson WR, Hasan NA, Tall BD, Kothary MH, Kiss H, Munk AC, Tapia R, Green L, Detter C, Bruce DC, Brettin TS, Colwell RR, Morris PJ (2012) Temperature regulation of virulence factors in the pathogen Vibrio coralliilyticus. ISME J 6:835–846

    CAS  PubMed  Google Scholar 

  • Koenig JE, Bourne DG, Curtis B, Dlutek M, Stokes HW, Doolittle WF, Boucher Y (2011) Coral-mucus-associated Vibrio integrons in the great barrier reef: genomic hotspots for environmental adaptation. ISME J 5:962–972

    CAS  PubMed  PubMed Central  Google Scholar 

  • Koopman WJ, Nijtmans LG, Dieteren CE, Roestenberg P, Valsecchi F, Smeitink JA, Willems PH (2010) Mammalian mitochondrial complex I: biogenesis, regulation, and reactive oxygen species generation. Antioxid Redox Signal 12:1431–1470

    CAS  PubMed  Google Scholar 

  • Kvennefors ECE, Sampayo E, Ridgway T, Barnes AC, Hoegh-Guldberg O (2010) Bacterial communities of two ubiquitous great barrier reef corals reveals both site-and species-specificity of common bacterial associates. PLoS One 5:e10401

    PubMed  PubMed Central  Google Scholar 

  • Kvitt H, Kramarsky-Winter E, Maor-Landaw K, Zandbank K, Kushmaro A, Rosenfeld H, Fine M, Tchernov D (2015) Breakdown of coral colonial form under reduced pH conditions is initiated in polyps and mediated through apoptosis. Proc Natl Acad Sci U S A 112:2082–2086

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kwon S, Kim EJE, Lee SV (2018) Mitochondria-mediated defense mechanisms against pathogens in Caenorhabditis elegans. BMB Rep 51:274–279

    CAS  PubMed  PubMed Central  Google Scholar 

  • LaJeunesse TC, Parkinson JE, Gabrielson PW, Jeong HJ, Reimer JD, Voolstra CR, Santos SR (2018) Systematic revision of Symbiodiniaceae highlights the antiquity and diversity of coral endosymbionts. Curr Biol 28:2570–2580

    CAS  PubMed  Google Scholar 

  • Lesser MP, Bythell JC, Gates RD, Johnstone RW, Hoegh-Guldberg O (2007) Are infectious diseases really killing corals? Alternative interpretations of the experimental and ecological data. J Exp Mar Biol Ecol 346:36–44

    Google Scholar 

  • Libro S, Kaluziak ST, Vollmer SV (2013) RNA-seq profiles of immune related genes in the staghorn coral Acropora cervicornis infected with white band disease. PLoS One 8:e81821

    PubMed  PubMed Central  Google Scholar 

  • Martin M (2011) Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J 17:10–12

    Google Scholar 

  • Maynard J, Van Hooidonk R, Eakin CM, Puotinen M, Garren M, Williams G, Heron SF, Lamb J, Weil E, Willis B (2015) Projections of climate conditions that increase coral disease susceptibility and pathogen abundance and virulence. Nat Clim Chang 5:688–694

    Google Scholar 

  • Medzhitov R, Preston-Hurlburt P, Janeway CA (1997) A human homologue of the Drosophila toll protein signals activation of adaptive immunity. Nature 388:394–397

    CAS  PubMed  Google Scholar 

  • Meyer E, Aglyamova GV, Matz MV (2011) Profiling gene expression responses of coral larvae (Acropora millepora) to elevated temperature and settlement inducers using a novel RNA-Seq procedure. Mol Ecol 20:3599–3616

    CAS  PubMed  Google Scholar 

  • Moberg F, Folke C (1999) Ecological goods and services of coral reef ecosystems. Ecol Econ 29:215–233

    Google Scholar 

  • Mohamed AR, Cumbo V, Harii S, Shinzato C, Chan CX, Ragan MA, Bourne DG, Willis BL, Ball EE, Satoh N, Miller DJ (2016) The transcriptomic response of the coral Acropora digitifera to a competent Symbiodinium strain: the symbiosome as an arrested early phagosome. Mol Ecol 25:3127–3141

    CAS  PubMed  Google Scholar 

  • Motone K, Takagi T, Aburaya S, Aoki W, Miura N, Minakuchi H, Takeyama H, Nagasaki Y, Shinzato C, Ueda M (2018) Protection of coral larvae from thermally induced oxidative stress by redox nanoparticles. Mar Biotechnol 20:542–548

  • Muller EM, van Woesik R (2012) Caribbean coral diseases: primary transmission or secondary infection? Glob Chang Biol 18:3529–3535

    Google Scholar 

  • Murr C, Widner B, Wirleitner B, Fuchs D (2002) Neopterin as a marker for immune system activation. Curr Drug Metab 3:175–187

    CAS  PubMed  Google Scholar 

  • Mydlarz LD, McGinty ES, Harvell CD (2010) What are the physiological and immunological responses of coral to climate warming and disease? J Exp Biol 213:934–945

    PubMed  Google Scholar 

  • Nair SV, Del Valle H, Gross PS, Terwilliger DP, Smith LC (2005) Macroarray analysis of coelomocyte gene expression in response to LPS in the sea urchin. Identification of unexpected immune diversity in an invertebrate. Physiol Genomics 22:33–47

    CAS  PubMed  Google Scholar 

  • Nishio K, Qiao S, Yamashita H (2005) Characterization of the differential expression of uncoupling protein 2 and ROS production in differentiated mouse macrophage-cells (Mm1) and the progenitor cells (M1). J Mol Histol 36:35–44

    CAS  PubMed  Google Scholar 

  • O’Neill LA, Golenbock D, Bowie AG (2013) The history of toll-like receptors—redefining innate immunity. Nat Rev Immunol 13:453–460

    PubMed  Google Scholar 

  • Orrenius S, Gogvadze V, Zhivotovsky B (2007) Mitochondrial oxidative stress: implications for cell death. Annu Rev Pharmacol Toxicol 47:143–183

    CAS  PubMed  Google Scholar 

  • Palmer CV, Traylor-Knowles N (2012) Towards an integrated network of coral immune mechanisms. Proc Biol Sci 279:4106–4114

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pan B, Johnstone RM (1983) Fate of the transferrin receptor during maturation of sheep reticulocytes in vitro: selective externalization of the receptor. Cell 33:967–978

    CAS  PubMed  Google Scholar 

  • Pimentel H, Bray NL, Puente S, Melsted P, Pachter L (2017) Differential analysis of RNA-seq incorporating quantification uncertainty. Nat Methods 14:687–690

    CAS  PubMed  Google Scholar 

  • Roberts CM, McClean CJ, Veron JE, Hawkins JP, Allen GR, McAllister DE, Mittermeier CG, Schueler FW, Spalding M, Wells F, Vynne C, Werner TB (2002) Marine biodiversity hotspots and conservation priorities for tropical reefs. Science 295:1280–1284

    CAS  PubMed  Google Scholar 

  • Rosenberg E, Koren O, Reshef L, Efrony R, Zilber-Rosenberg I (2007) The role of microorganisms in coral health, disease and evolution. Nat Rev Microbiol 5:355–362

    CAS  PubMed  Google Scholar 

  • Rosic NN, Hoegh-Guldberg O (2010) A method for extracting a high-quality RNA from Symbiodinium sp. J Appl Phycol 22:139–146

    CAS  Google Scholar 

  • Santos EO, Alves J, Nelson DGM, Mazotto AM, Vermelho A, Vora GJ, Wilson B, Beltran VH, Bourne DG, Le Roux F, Thompson FL (2011) Genomic and proteomic analyses of the coral pathogen Vibrio coralliilyticus reveal a diverse virulence repertoire. ISME J 5:1471–1483

    Google Scholar 

  • Sato Y, Bourne DG, Willis BL (2009) Dynamics of seasonal outbreaks of black band disease in an assemblage of Montipora species at Pelorus Island (great barrier reef, Australia). Proc Biol Sci 276:2795–2803

    PubMed  PubMed Central  Google Scholar 

  • Sato K, Casareto BE, Suzuki Y, Kodani S (2013) Antibacterial activity of scleractinian corals in Okinawa, Japan. Galaxea J Coral Reef Stud 15:19–26

    Google Scholar 

  • Shapiro OH, Kramarsky-Winter E, Gavish AR, Stocker R, Vardi A (2016) A coral-on-a-chip microfluidic platform enabling live-imaging microscopy of reef-building corals. Nat Commun 7:1–10

    Google Scholar 

  • Shinzato C, Shoguchi E, Kawashima T, Hamada M, Hisata K, Tanaka M, Fujie M, Fujiwara M, Koyanagi R, Ikuta T, Fujiyama A, Miller DJ, Satoh N (2011) Using the Acropora digitifera genome to understand coral responses to environmental change. Nature 476:320–323

    CAS  PubMed  Google Scholar 

  • Smeds L, Künstner A (2011) ConDeTri-a content dependent read trimmer for Illumina data. PLoS One 6:e26314

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sokolow S (2009) Effects of a changing climate on the dynamics of coral infectious disease: a review of the evidence. Dis Aquat Org 87:5–18

    Google Scholar 

  • Stoorvogel W, Kleijmeer MJ, Geuze HJ, Raposo G (2002) The biogenesis and functions of exosomes. Traffic 3:321–330

    CAS  PubMed  Google Scholar 

  • Sussman M, Willis BL, Victor S, Bourne DG (2008) Coral pathogens identified for white syndrome (WS) epizootics in the Indo-Pacific. PLoS One 3:e2393

    PubMed  PubMed Central  Google Scholar 

  • Sutherland KP, Porter JW, Torres C (2004) Disease and immunity in Caribbean and Indo-Pacific zooxanthellate corals. Mar Ecol Prog Ser 266:273–302

    Google Scholar 

  • Théry C, Zitvogel L, Amigorena S (2002) Exosomes: composition, biogenesis and function. Nat Rev Immunol 2:569–579

    PubMed  Google Scholar 

  • Tomlin H, Piccinini AM (2018) A complex interplay between the extracellular matrix and the innate immune response to microbial pathogens. Immunology 155:186–201

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tout J, Siboni N, Messer LF, Garren M, Stocker R, Webster NS, Ralph PJ, Seymour JR (2015) Increased seawater temperature increases the abundance and alters the structure of natural Vibrio populations associated with the coral Pocillopora damicornis. Front Microbiol 6:432

    PubMed  PubMed Central  Google Scholar 

  • Travers M, Meistertzheim A, Cardinaud M, Friedman CS, Huchette S, Moraga D, Paillard C (2010) Gene expression patterns of abalone, Haliotis tuberculata, during successive infections by the pathogen Vibrio harveyi. J Invertebr Pathol 105:289–297

    CAS  PubMed  Google Scholar 

  • Ushijima B, Videau P, Burger AH, Shore-Maggio A, Runyon CM, Sudek M, Aeby GS, Callahan SM (2014) Vibrio coralliilyticus strain OCN008 is an etiological agent of acute Montipora white syndrome. Appl Environ Microbiol 80:2102–2109

    PubMed  PubMed Central  Google Scholar 

  • Valadi H, Ekström K, Bossios A, Sjöstrand M, Lee JJ, Lötvall JO (2007) Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol 9:654–659

    CAS  PubMed  Google Scholar 

  • van Rensburg MJ, Coyne VE (2009) The role of electron transport in the defence response of the South African abalone, Haliotis midae. Fish Shellfish Immunol 26:171–176

    PubMed  Google Scholar 

  • Vidal-Dupiol J, Ladrière O, Destoumieux-Garzón D, Sautière P, Meistertzheim A, Tambutté E, Tambutté S, Duval D, Fouré L, Adjeroud M, Mitta G (2011) Innate immune responses of a scleractinian coral to vibriosis. J Biol Chem 286:22688–22698

    CAS  PubMed  PubMed Central  Google Scholar 

  • Vidal-Dupiol J, Dheilly NM, Rondon R, Grunau C, Cosseau C, Smith KM, Freitag M, Adjeroud M, Mitta G, Jiravanichpaisal P (2014) Thermal stress triggers broad pocillopora damicornis transcriptomic remodeling, while vibrio coralliilyticus infection induces a more targeted immuno-suppression response. PLoS One 9:e107672

  • Vrijsen KR, Sluijter J, Schuchardt M, Van Balkom B, Noort WA, Chamuleau S, Doevendans P (2010) Cardiomyocyte progenitor cell-derived exosomes stimulate migration of endothelial cells. J Cell Mol Med 14:1064–1070

    CAS  PubMed  PubMed Central  Google Scholar 

  • Weinberg SE, Sena LA, Chandel NS (2015) Mitochondria in the regulation of innate and adaptive immunity. Immunity 42:406–417

    CAS  PubMed  PubMed Central  Google Scholar 

  • West AP, Shadel GS, Ghosh S (2011) Mitochondria in innate immune responses. Nat Rev Immunol 11:389–402

    CAS  PubMed  PubMed Central  Google Scholar 

  • Williamson RD, McCarthy FP, Kenny LC, McCarthy CM (2019) Activation of a TLR9 mediated innate immune response in preeclampsia. Sci Rep 9:1–8

    Google Scholar 

  • Wright RM, Aglyamova GV, Meyer E, Matz MV (2015) Gene expression associated with white syndromes in a reef building coral, Acropora hyacinthus. BMC Genomics 16:371

    PubMed  PubMed Central  Google Scholar 

  • Yellowlees D, Rees TAV, Leggat W (2008) Metabolic interactions between algal symbionts and invertebrate hosts. Plant Cell Environ 31:679–694

    CAS  PubMed  Google Scholar 

  • Yorifuji M, Harii S, Nakamura R, Fudo M (2017) Shift of symbiont communities in Acropora tenuis juveniles under heat stress. Peer J 5:e4055

    PubMed  PubMed Central  Google Scholar 

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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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  1. Atmosphere and Ocean Research Institute, The University of Tokyo, Chiba, 277-8564, Japan

    Toshiyuki Takagi, Yuki Yoshioka & Chuya Shinzato

  2. Graduate School of Frontier Sciences, The University of Tokyo, Chiba, 277-8564, Japan

    Yuki Yoshioka

  3. Marine Genomics Unit, Okinawa Institute of Science and Technology Graduate University, Okinawa, 904-0495, Japan

    Yuna Zayasu & Noriyuki Satoh

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  1. Toshiyuki Takagi
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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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