Cnidarian Immunity and the Repertoire of Defense Mechanisms in Anthozoans
Abstract
:1. Introduction
2. Allorecognition in Anthozoans
3. Symbiosis and Immunity
4. Interaction with Microbial Communities
5. Repertoire of Immune Receptors Signaling Pathways (PRRs)
5.1. Toll-Like Receptors (TLRs)
5.2. NOD-Like Receptors (NLRs)
5.3. Lectins
5.4. Integrin
5.5. Other PRRs
6. Molecular Signaling
6.1. Melanin Synthesis Pathways Activation
6.2. Complement System
7. Effector Responses
7.1. The Powerful Role of Mucus
7.2. Cellular Responses
7.2.1. Phagocytosis
7.2.2. Cytotoxicity
7.2.3. Reactive Oxygen Species (ROS) and Antioxidant
8. Inflammatory Processes in Model Anemonia viridis
9. Conclusions
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Petralia, R.S.; Mattson, M.P.; Yao, P.J. Aging and longevity in the simplest animals and the quest for immortality. Ageing Res. Rev. 2014, 16, 66–82. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Miller, D.J.; Hemmrich, G.; Ball, E.E.; Hayward, D.C.; Khalturin, K.; Funayama, N.; Agata, K.; Bosch, T.C.G. The innate immune repertoire in cnidaria--ancestral complexity and stochastic gene loss. Genome Biol. 2007, 8, R59. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- McFall-Ngai, M.; Hadfield, M.G.; Bosch, T.C.G.; Carey, H.V.; Domazet-Lošo, T.; Douglas, A.E.; Dubilier, N.; Eberl, G.; Fukami, T.; Gilbert, S.F.; et al. Animals in a bacterial world, a new imperative for the life sciences. Proc. Natl. Acad. Sci. USA 2013, 110, 3229–3236. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Soza-Ried, J.; Hotz-Wagenblatt, A.; Glatting, K.-H.; del Val, C.; Fellenberg, K.; Bode, H.R.; Frank, U.; Hoheisel, J.D.; Frohme, M. The transcriptome of the colonial marine hydroid Hydractinia echinata. FEBS J. 2010, 277, 197–209. [Google Scholar] [CrossRef] [PubMed]
- Chapman, J.A.; Kirkness, E.F.; Simakov, O.; Hampson, S.E.; Mitros, T.; Weinmaier, T.; Rattei, T.; Balasubramanian, P.G.; Borman, J.; Busam, D.; et al. The dynamic genome of Hydra. Nature 2010, 464, 592–596. [Google Scholar] [CrossRef]
- Wenger, Y.; Galliot, B. RNAseq versus genome-predicted transcriptomes: A large population of novel transcripts identified in an Illumina-454 Hydra transcriptome. BMC Genom. 2013, 14, 204. [Google Scholar] [CrossRef]
- Putnam, N.H.; Srivastava, M.; Hellsten, U.; Dirks, B.; Chapman, J.; Salamov, A.; Terry, A.; Shapiro, H.; Lindquist, E.; Kapitonov, V.V.; et al. Sea anemone genome reveals ancestral eumetazoan gene repertoire and genomic organization. Science 2007, 317, 86–94. [Google Scholar] [CrossRef] [Green Version]
- Buchmann, K. Evolution of Innate Immunity: Clues from Invertebrates via Fish to Mammals. Front. Immunol. 2014, 5, 459. [Google Scholar] [CrossRef] [Green Version]
- Vidal-Dupiol, J.; Adjeroud, M.; Roger, E.; Foure, L.; Duval, D.; Mone, Y.; Ferrier-Pages, C.; Tambutte, E.; Tambutte, S.; Zoccola, D.; et al. Coral bleaching under thermal stress: Putative involvement of host/symbiont recognition mechanisms. BMC Physiol. 2009, 9, 14. [Google Scholar] [CrossRef] [Green Version]
- Augustin, R.; Bosch, T.C.G. Cnidarian immunity: A tale of two barriers. Adv. Exp. Med. Biol. 2010, 708, 1–16. [Google Scholar] [CrossRef]
- Augustin, R.; Siebert, S.; Bosch, T.C.G. Identification of a kazal-type serine protease inhibitor with potent anti-staphylococcal activity as part of Hydra’s innate immune system. Dev. Comp. Immunol. 2009, 33, 830–837. [Google Scholar] [CrossRef] [PubMed]
- Stabili, L.; Schirosi, R.; Parisi, M.G.; Piraino, S.; Cammarata, M. The mucus of Actinia equina (Anthozoa, Cnidaria): An unexplored resource for potential applicative purposes. Mar. Drugs 2015, 13, 5276–5296. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Rinkevich, B. Neglected Biological Features in Cnidarians Self-Nonself Recognition. Adv. Exp. Med. Biol. 2012, 738, 46–59. [Google Scholar] [CrossRef] [PubMed]
- Campbell, R.D.; Bibb, C. Transplantation in coelenterates. Transplant. Proc. 1970, 2, 202–211. [Google Scholar] [PubMed]
- Hildemann, W.H.; Jokiel, P.L.; Bigger, C.H.; Johnston, I.S. Allogeneic polymorphism and alloimmune memory in the coral, Montipora verrucosa. Transplantation 1980, 30, 297–301. [Google Scholar] [CrossRef]
- Lubbock, R. Clone-specific cellular recognition in a sea anemone. Proc. Natl. Acad. Sci. USA 1980, 77, 6667–6669. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Palmer, C.V.; Traylor-Knowles, N. Towards an integrated network of coral immune mechanisms. Proc. Biol. Sci. 2012, 279, 4106–4114. [Google Scholar] [CrossRef] [Green Version]
- Rinkevich, B. Allorecognition and xenorecognition in reef corals: A decade of interactions. Hydrobiologia 2004, 530, 443–450. [Google Scholar] [CrossRef]
- Netea, M.G.; Quintin, J.; van der Meer, J.W.M. Trained immunity: A memory for innate host defense. Cell Host Microbe 2011, 9, 355–361. [Google Scholar] [CrossRef] [Green Version]
- Karadge, U.B.; Gosto, M.; Nicotra, M.L. Allorecognition proteins in an invertebrate exhibit homophilic interactions. Curr. Biol. 2015, 25, 2845–2850. [Google Scholar] [CrossRef] [Green Version]
- Frank, U.; Rinkevich, B. Alloimmune memory is absent in the Red Sea hydrocoral Millepora dichotoma. J. Exp. Zool. 2001, 291, 25–29. [Google Scholar] [CrossRef] [PubMed]
- Chadwick-Furman, N.; Rinkevich, B. A complex allorecognition system in a reef-building coral: Delayed responses, reversals and nontransitive hierarchies. Coral Reefs 1994, 13, 57–63. [Google Scholar] [CrossRef]
- Nicotra, M.L. Invertebrate allorecognition. Curr. Biol. 2019, 29, R463–R467. [Google Scholar] [CrossRef]
- Cadavid, L.F.; Powell, A.E.; Nicotra, M.L.; Moreno, M.; Buss, L.W. An invertebrate histocompatibility complex. Genetics 2004, 167, 357–365. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Dishaw, L.J.; Litman, G.W. Invertebrate Allorecognition: The Origins of Histocompatibility. Curr. Biol. 2009, 19, 6–10. [Google Scholar] [CrossRef] [Green Version]
- Kuznetsov, S.G.; Bosch, T.C.G. Self/nonself recognition in Cnidaria: Contact to allogeneic tissue does not result in elimination of nonself cells in Hydra vulgaris. Zoology 2003, 106, 1–8. [Google Scholar] [CrossRef]
- Tremblay, P.; Grover, R.; Maguer, J.F.; Legendre, L.; Ferrier-Pagès, C. Autotrophic carbon budget in coral tissue: A new 13C-based model of photosynthate translocation. J. Exp. Biol. 2012, 215, 1384–1393. [Google Scholar] [CrossRef] [Green Version]
- Allemand, D.; Furla, P.; Tambutté, S. Mechanisms of carbon acquisition for endosymbiont photosynthesis in Anthozoa. Can. J. Bot. 2011, 76, 925–941. [Google Scholar] [CrossRef]
- Santos, S.R.; Taylor, D.J.; Kinzie, R.A.; Hidaka, M.; Sakai, K.; Coffroth, M.A. Molecular phylogeny of symbiotic dinoflagellates inferred from partial chloroplast large subunit (23S)-rDNA sequences. Mol. Phylogenet. Evol. 2002, 23, 97–111. [Google Scholar] [CrossRef]
- LaJeunesse, T.C.; Parkinson, J.E.; Gabrielson, P.W.; Jeong, H.J.; Reimer, J.D.; Voolstra, C.R.; Santos, S.R. Systematic Revision of Symbiodiniaceae Highlights the Antiquity and Diversity of Coral Endosymbionts. Curr. Biol. 2018, 28, 2570–2580.e6. [Google Scholar] [CrossRef] [Green Version]
- Burns, J.A.; Zhang, H.; Hill, E.; Kim, E.; Kerney, R. Transcriptome analysis illuminates the nature of the intracellular interaction in a vertebrate-algal symbiosis. Elife 2017, 6. [Google Scholar] [CrossRef]
- Mansfield, K.M.; Carter, N.M.; Nguyen, L.; Cleves, P.A.; Alshanbayeva, A.; Williams, L.M.; Crowder, C.; Penvose, A.R.; Finnerty, J.R.; Weis, V.M.; et al. Transcription factor NF-κB is modulated by symbiotic status in a sea anemone model of cnidarian bleaching. Sci. Rep. 2017, 7, 16025. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Pinzón, J.H.; Kamel, B.; Burge, C.A.; Harvell, C.D.; Medina, M.; Weil, E.; Mydlarz, L.D. Whole transcriptome analysis reveals changes in expression of immune-related genes during and after bleaching in a reef-building coral. R. Soc. Open Sci. 2015, 2. [Google Scholar] [CrossRef] [Green Version]
- Caroselli, E.; Goffredo, S. Population Dynamics of Temperate Corals in a Changing Climate. In The Cnidaria, Past, Present and Future. The World of Medusa and Her Sisters; Springer: Berlin, Germany, 2016; pp. 317–328. [Google Scholar]
- Merselis, D.G.; Lirman, D.; Rodriguez-Lanetty, M. Symbiotic immuno-suppression: Is disease susceptibility the price of bleaching resistance? PeerJ 2018, 6, e4494. [Google Scholar] [CrossRef] [PubMed]
- Dunn, S.R.; Schnitzler, C.E.; Weis, V.M. Apoptosis and autophagy as mechanisms of dinoflagellate symbiont release during cnidarian bleaching: Every which way you lose. Proc. Biol. Sci. 2007, 274, 3079–3085. [Google Scholar] [CrossRef] [Green Version]
- Brumell, J.H.; Scidmore, M.A. Manipulation of rab GTPase function by intracellular bacterial pathogens. Microbiol. Mol. Biol. Rev. 2007, 71, 636–652. [Google Scholar] [CrossRef] [Green Version]
- Chen, M.C.; Hong, M.C.; Huang, Y.S.; Liu, M.C.; Cheng, Y.M.; Fang, L.S. ApRab11, a cnidarian homologue of the recycling regulatory protein Rab11, is involved in the establishment and maintenance of the Aiptasia-Symbiodinium endosymbiosis. Biochem. Biophys. Res. Commun. 2005, 338, 1607–1616. [Google Scholar] [CrossRef] [PubMed]
- Rohwer, F.; Seguritan, V.; Knowlton, N.; Rohwer, F.; Seguritan, V.; Azam, F.; Knowlton, N. Diversity and distribution of coral-associated bacteria. Mar. Ecol. Prog. Ser. 2002, 243, 1–10. [Google Scholar] [CrossRef] [Green Version]
- Vega Thurber, R.; Correa, A. Viruses of reef-building scleractinian corals. J. Exp. Mar. Biol. Ecol. 2011, 408, 102–113. [Google Scholar] [CrossRef]
- Rivera, H.; Thompson, J.; Medina, M.; Closek, C. Microbes in the coral holobiont: Partners through evolution, development, and ecological interactions. Front. Cell. Infect. Microbiol. 2015, 4. [Google Scholar] [CrossRef]
- Deschaseaux, E.S.M.; Jones, G.B.; Deseo, M.A.; Shepherd, K.M.; Kiene, R.P.; Swan, H.B.; Harrison, P.L.; Eyre, B.D. Effects of environmental factors on dimethylated sulfur compounds and their potential role in the antioxidant system of the coral holobiont. Limnol. Oceanogr. 2014, 59, 758–768. [Google Scholar] [CrossRef]
- Cróquer, A.; Bastidas, C.; Elliott, A.; Sweet, M. Bacterial assemblages shifts from healthy to yellow band disease states in the dominant reef coral Montastraea faveolata. Environ. Microbiol. Rep. 2013, 5, 90–96. [Google Scholar] [CrossRef] [PubMed]
- Tinta, T.; Kogovšek, T.; Klun, K.; Malej, A.; Herndl, G.J.; Turk, V. Jellyfish-Associated Microbiome in the Marine Environment: Exploring Its Biotechnological Potential. Mar. Drugs 2019, 17, 94. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Weiland-Bräuer, N.; Neulinger, S.C.; Pinnow, N.; Künzel, S.; Baines, J.F.; Schmitz, R.A. Composition of bacterial communities associated with Aurelia aurita changes with compartment, life stage, and population. Appl. Environ. Microbiol. 2015, 81, 6038–6052. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kos Kramar, M.; Tinta, T.; Lučić, D.; Malej, A.; Turk, V. Bacteria associated with moon jellyfish during bloom and post-bloom periods in the Gulf of Trieste (northern Adriatic). PLoS ONE 2019, 14, e0198056. [Google Scholar] [CrossRef] [Green Version]
- Basso, L.; Rizzo, L.; Marzano, M.; Intranuovo, M.; Fosso, B.; Pesole, G.; Piraino, S.; Stabili, L. Jellyfish summer outbreaks as bacterial vectors and potential hazards for marine animals and humans health? The case of Rhizostoma pulmo (Scyphozoa, Cnidaria). Sci. Total Environ. 2019, 692, 305–318. [Google Scholar] [CrossRef] [PubMed]
- Stabili, L.; Rizzo, L.; Basso, L.; Marzano, M.; Fosso, B.; Pesole, G.; Piraino, S. The Microbial Community Associated with Rhizostoma pulmo: Ecological Significance and Potential Consequences for Marine Organisms and Human Health. Mar. Drugs 2020, 18, 437. [Google Scholar] [CrossRef]
- Lawson, C.; Raina, J.; Kahlke, T.; Seymour, J.; Suggett, D. Defining the Core Microbiome of the Symbiotic Dinoflagellate, Symbiodinium. Environ. Microbiol. Rep. 2017, 10. [Google Scholar] [CrossRef]
- Rosenberg, E.; Kushmaro, A.; Kramarsky-Winter, E.; Banin, E.; Yossi, L. The role of microorganisms in coral bleaching. ISME 2009, 3, 139–146. [Google Scholar] [CrossRef] [Green Version]
- Porporato, E.M.; Lo Giudice, A.; Michaud, L.; De Domenico, E.; Spanò, N. Diversity and antibacterial activity of the bacterial communities associated with two Mediterranean sea pens, Pennatula phosphorea and Pteroeides spinosum (Anthozoa: Octocorallia). Microb. Ecol. 2013, 66, 701–714. [Google Scholar] [CrossRef]
- Ocampo, I.D.; Cadavid, L.F. Mechanisms of immune responses in Cnidarians. Acta Biol. Colomb. 2015, 20, 5–11. [Google Scholar] [CrossRef]
- Chimetto, L.A.; Cleenwerck, I.; Alves, N., Jr.; Silva, B.S.; Brocchi, M.; Willems, A.; De Vos, P.; Thompson, F.L. Vibrio communis sp. nov., isolated from the marine animals Mussismilia hispida, Phyllogorgia dilatata, Palythoa caribaeorum, Palythoa variabilis and Litopenaeus vannamei. Int. J. Syst. Evol. Microbiol. 2011, 61, 362–368. [Google Scholar] [CrossRef] [PubMed]
- Reshef, L.; Koren, O.; Loya, Y.; Zilber-Rosenberg, I.; Rosenberg, E. The coral probiotic hypothesis. Environ. Microbiol. 2006, 8, 2068–2073. [Google Scholar] [CrossRef] [Green Version]
- Calow, P. Why some metazoan mucus secretions are more susceptible to microbial attack than others. Am. Nat. 1979, 114, 149–152. [Google Scholar] [CrossRef]
- Sharp, K.H.; Distel, D.; Paul, V.J. Diversity and dynamics of bacterial communities in early life stages of the Caribbean coral Porites astreoides. ISME 2012, 6, 790–801. [Google Scholar] [CrossRef] [PubMed]
- Rosenberg, E.; Zilber-Rosenberg, I. Symbiosis and development: The hologenome concept. Birth Defects Res. C Embryo Today 2011, 93, 56–66. [Google Scholar] [CrossRef] [PubMed]
- Ainsworth, T.D.; Fine, M.; Roff, G.; Hoegh-Guldberg, O. Bacteria are not the primary cause of bleaching in the Mediterranean coral Oculina patagonica. ISME 2008, J2, 67–73. [Google Scholar] [CrossRef] [Green Version]
- Miller, A.; Richardson, L. Emerging coral diseases: A temperature-driven process? Mar. Ecol. 2014, 36. [Google Scholar] [CrossRef]
- Weis, V. Cellular mechanisms of Cnidarian bleaching: Stress causes the collapse of symbiosis. J. Exp. Biol. 2008, 211, 3059–3066. [Google Scholar] [CrossRef] [Green Version]
- Brennan, J.J.; Messerschmidt, J.L.; Williams, L.M.; Matthews, B.J.; Reynoso, M.; Gilmore, T.D. 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. USA 2017, 114, E10122–E10131. [Google Scholar] [CrossRef] [Green Version]
- O’Neill, L.; Golenbock, D.; Bowie, A. The history of Toll-like receptors—Redefining innate immunity. Nat. Rev. Immunol. 2013, 13, 453–460. [Google Scholar] [CrossRef] [PubMed]
- Medzhitov, R.; Janeway, C. Innate immune recognition: Mechanisms and pathways. Immunol. Rev. 2000, 173, 89–97. [Google Scholar] [CrossRef]
- Cerenius, L.; Kawabata, S.; Lee, B.; Nonaka, M.; Soderhall, K. Proteolytic cascades and their involvement in invertebrate immunity. Trends Biochem. Sci. 2010, 35, 575–583. [Google Scholar] [CrossRef]
- Augustin, R.; Fraune, S.; Franzenburg, S.; Bosch, T. Where simplicity meets complexity: Hydra, a model for hostmicrobe interactions. Adv. Exp. Med. Biol. 2012, 710, 71–80. [Google Scholar] [CrossRef]
- Palmer, C.; Bythell, J.; Willis, B. Enzyme activity demonstrates multiple pathways of innate immunity in Indo-Pacific anthozoans. Proc. R. Soc. B Biol. Sci. 2012, 279, 3879–3887. [Google Scholar] [CrossRef] [Green Version]
- Janeway, C.; Medzhitov, R. Innate immune recognition. Annu. Rev. Immunol. 2002, 20, 197–216. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hemmrich, G.; Miller, D.; Bosch, T. The evolution of immunity: A low-life perspective. Trends Immunol. 2007, 28, 449–454. [Google Scholar] [CrossRef] [PubMed]
- Van der Burg, C.; Prentis, P.; Surm, J.; Pavasovic, A. Insights into the innate immunome of actiniarians using a comparative genomic approach. BMC Genom. 2016, 17, 850. [Google Scholar] [CrossRef]
- Baumgarten, S.; Simakov, O.; Esherick, L.Y.; Leiw, Y.J.; Lehnert, E.M.; Michell, C.; Li, Y.; Hambleton, E.A.; Guse, A.; Oates, M.E.; et al. The genome of Aiptasia, a sea anemone model for coral symbiosis. Proc. Natl. Acad. Sci. USA 2015, 22, 11893–11898. [Google Scholar] [CrossRef] [Green Version]
- Reitzel, A.; Sullivan, J.; Traylor-Knowles, N.; Finnerty, J. Genomic survey of candidatestress-response genes in the esturine anemone Nematostella vectensis. Biol Bull. 2008, 214, 233–254. [Google Scholar] [CrossRef] [Green Version]
- Armulik, A.; Velling, T.; Johansson, S. The integrin beta1 subunit transmembrane domain regulates phosphatidylinositol 3-kinase-dependent tyrosine phosphorylation of Crk-associated substrate. Mol. Biol. Cell 2004, 15, 2558–2567. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Knack, B.; Iguchi, A.; Shinzato, C.; Hayward, D.; Ball, E.; Miller, D. Unexpected diversity of cnidarian integrins: Expression during coral gastrulation. BMC Evol. Biol. 2008, 8, 136. [Google Scholar] [CrossRef] [Green Version]
- Schwarz, J.; Brokstein, P.; Voolstra, C.; Terry, A.; Miller, D.; Szmant, A.; Coffroth, M.; Medina, M. Coral life history and symbiosis: Functional genomic resources for two reef building Caribbean corals, Acropora palmata and Montastraea faveolata. BMC Genom. 2008, 97, 1471–2164. [Google Scholar]
- Kvennefors, E.C.E.; Leggat, W.; Hoegh-Guldberg, O.; Degnan, B.M.; Barnes, A.C. An ancient and variable mannose-binding lectin from the coral Acropora millepora binds both pathogens and symbionts. Dev. Comp. Immunol. 2008, 32, 1582–1592. [Google Scholar] [CrossRef]
- Desalvo, M.; Voolstra, C.; Sunagawa, S.; Schwarz, J.; Stillman, J.; Coffroth, M.; Szmant, A.; Medina, M. Differential gene expression during thermal stress and bleaching in the Caribbean coral Montastraea faveolata. Mol. Ecol. 2008, 17, 3952–3971. [Google Scholar] [CrossRef]
- Elisha, M.W.-C.; Virginia, W.V. The diversity of C-Type lectin in the genome of a basal metazoan nematostella vectensis. Dev. Comp. Immunol. 2014, 33, 881–889. [Google Scholar]
- Burge, C.; Mouchka, M.; Harvell, C.; Roberts, C. Immune response of the Caribbean sea fan, Gorgonia ventalina, exposed to an Aplanochytrium parasite as revealed by transcriptome sequencing. Front. Physiol. 2013, 4, 180. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bosch, T.; Augustin, R.; Anton-Erxleben, F.; Fraune, S.; Hemmrich, G.; Zill, H.; Rosenstiel, P.; Jacobs, G.; Schreiber, S.; Leippe, M.; et al. Uncovering the evolutionary history of innate immunity: The simple metazoan Hydra uses epithelial cells for host defence. Dev. Comp. Immunol. 2009, 33, 559–569. [Google Scholar] [CrossRef] [PubMed]
- Shinzato, C.; Shoguchi, E.; Kawashima, T.; Hamada, M.; Hisata, K.; Tanaka, M.; Fujie, M.; Fujiwara, M.; Koyanagi, R.; Ikuta, T.; et al. Using the Acropora digitifera genome to understand coral responses to environmental change. Nature 2011, 476, 320–323. [Google Scholar] [CrossRef]
- Hamada, M.; Shoguchi, E.; Shinzato, C.; Kawashima, T.; Miller, D.J.; Satoh, N. The complex NOD-like receptor repertoire of the coral Acropora digitifera includes novel domain combinations. Mol. Biol. Evol. 2013, 30, 167–176. [Google Scholar] [CrossRef]
- Leclerc, M. Humoral Factors in Marine Invertebrates. In Invertebrate Immnology. Progress in Molecular and Subcellular Biology; Rinkevich, B., Müller, W.E.G., Eds.; Springer: Berlin/Heidelberg, Germany, 1996; Volume 15, ISBN 9783642797378. [Google Scholar]
- Kvennefors, E.C.E.; Leggat, W.; Kerr, C.C.; Ainsworth, T.D.; Hoegh-Guldberg, O.; Barnes, A.C. Analysis of evolutionarily conserved innate immune components in coral links immunity and symbiosis. Dev. Comp. Immunol. 2010, 34, 1219–1229. [Google Scholar] [CrossRef] [PubMed]
- Dunn, S.R. Immunorecognition and immunoreceptors in the Cnidaria. ISJ 2009, 6, 7–14. [Google Scholar]
- Hayes, M.; Eytan, R.I.; Hellberg, M. High amino acid diversity and positive selection at a putative coral immunity gene (tachylectin-2). BMC Evol. Biol. 2010, 10, 150. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mcguinness, D.; Dehal, P.; Pleass, R. Pattern recognition molecules and innate immunity to parasites. Trends Parasitol. 2003, 19, 312–319. [Google Scholar] [CrossRef]
- Lopez, J.; Fain, M.; Cadavid, L. The evolution of the immunetype gene family Rhamnospondin in cnidarians. Gene 2011, 473, 119–124. [Google Scholar] [CrossRef]
- Detournay, O.; Schnitzler, C.; Poole, A.; Weis, V. Regulation of cnidarian–dinoflagellate mutualisms: Evidence that activation of a host TGFβ innate immune pathway promotes tolerance of the symbiont. Dev. Comp. Immunol. 2012, 38, 525–537. [Google Scholar] [CrossRef] [Green Version]
- Weiss, Y.; Foret, S.; Hayward, D.; Ainsworth, T.; King, R.; Ball, E.; Miller, D.J. The acute transcriptional response of the coral Acropora millepora to immune challenge: Expression of GiMAP/IAN genes links the innate immune responses of corals with those of mammals and plants. BMC Genom. 2013, 14, 400. [Google Scholar] [CrossRef] [Green Version]
- Palmer, C.V.; Mydlarz, L.D.; Willis, B.L. Evidence of an inflammatory-like response in non-normally pigmented tissues of two scleractinian corals. Proc. R. Soc. B Biol. Sci. 2008, 275, 2687–2693. [Google Scholar] [CrossRef] [Green Version]
- Luna-Acosta, A.; Rosenfeld, E.; Amari, M.; Fruitier-Arnaudin, I.; Bustamante, P.; Thomas-Guyon, H. First evidence of laccase activity in the Pacific oyster Crassostrea gigas. Fish Shellfish Immunol. 2010, 28, 719–726. [Google Scholar] [CrossRef] [Green Version]
- Takahashi, D.; Garcia, B.L.; Kanost, M.R. Initiating protease with modular domains interacts with β-glucan recognition protein to trigger innate immune response in insects. Proc. Natl. Acad. Sci. USA 2015, 112, 13856–13861. [Google Scholar] [CrossRef] [Green Version]
- Vidal-Dupiol, J.; Dheilly, N.; Rondon, R.; Grunau, C.; Cosseau, C.; Smith, K.; Freitag, M.; Adjeroud, M.; Mitta, G. Thermal stress triggers broad Pocillopora damicornis transcriptomic remodeling, while Vibrio coralliilyticus infection induces a more targeted immunosuppression response. PLoS ONE 2014, 9, e107672. [Google Scholar] [CrossRef] [Green Version]
- Esposito, R.; D’Aniello, S.; Squarzoni, P.; Pezzotti, M.; Ristoratore, F.; Spagnuolo, A. New insights into the evolution of Metazoan tyrosinase gene family. PLoS ONE 2012, 7, e35731. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mydlarz, L.D.; Jones, L.E.; Harvell, C.D. Innate Immunity, Environmental Drivers, and Disease Ecology of Marine and Freshwater Invertebrates. Annu. Rev. Ecol. Evol. Syst. 2006, 37, 251–288. [Google Scholar] [CrossRef] [Green Version]
- Schultz, G.S.; Chin, G.A.; Moldawer, L.; Diegelmann, R.F. Principles of Wound Healing. In Mechanisms of Vascular Disease: A Reference Book for Vascular Specialists; Fitridge, R., Thompson, M., Eds.; University of Adelaide Press: Adelaide, Australia, 2011; ISBN 9780987171825. [Google Scholar]
- Fitt, W.; Gates, R.; Hoegh-Guldberg, O.; Bythell, J.C.; Grottoli, A.; Gomez Cabrera, K.-L.; Fisher, P.L.; Pantos, O.; Iglesias-Prieto, R.; Rodrigues, L.; et al. Response of two species of Indo-Pacific corals, Porites cylindrica and Stylophora pistillata, to short-term thermal stress: The host does matter in determining the tolerance of corals to bleaching. J. Exp. Mar. Biol. Ecol. 2009, 373, 102–110. [Google Scholar] [CrossRef]
- Sarma, J.V.; Ward, P.A. The complement system. Cell Tissue Res. 2011, 343, 227–2358. [Google Scholar] [CrossRef] [PubMed]
- Noris, M.; Remuzzi, G. Overview of complement activation and regulation. Semin. Nephrol. 2013, 33, 479–492. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Nonaka, M. The complement C3 protein family in invertebrates. Invertebr. Surviv. J. 2011, 8, 21–32. [Google Scholar]
- Endo, Y.; Nonaka, M.; Saiga, H.; Kakinuma, Y.; Matsushita, A.; Takahashi, M.; Matsushita, M.; Fujita, T. Origin of mannose-binding lectin-associated serine protease (MASP)-1 and MASP-3 involved in the lectin complement pathway traced back to the invertebrate, amphioxus. J. Immunol. 2003, 170, 4701–4707. [Google Scholar] [CrossRef] [Green Version]
- Kimura, A.; Sakaguchi, E.; Nonaka, M. Multi-component complement system of Cnidaria: C3, Bf, and MASP genes expressed in the endodermal tissues of a sea anemone, Nematostella vectensis. Immunobiology 2009, 214, 165–178. [Google Scholar] [CrossRef]
- Dishaw, L.J.; Smith, S.L.; Bigger, C.H. Characterization of a C3-like cDNA in a coral: Phylogenetic implications. Immunogenetics 2005, 57, 535–548. [Google Scholar] [CrossRef]
- Fujito, N.T.; Sugimoto, S.; Nonaka, M. Evolution of thioester-containing proteins revealed by cloning and characterization of their genes from a cnidarian sea anemone, Haliplanella lineate. Dev. Comp. Immunol. 2010, 34, 775–784. [Google Scholar] [CrossRef] [PubMed]
- Frazão, B.; Vasconcelos, V.; Antunes, A. Sea anemone (Cnidaria, Anthozoa, Actiniaria) toxins: An overview. Mar. Drugs 2012, 10, 1812–1851. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Castañeda, O.; Harvey, A.L. Discovery and characterization of cnidarian peptide toxins that affect neuronal potassium ion channels. Toxicon 2009, 54, 1119–1124. [Google Scholar] [CrossRef] [PubMed]
- Chi, V.; Pennington, M.W.; Norton, R.S.; Tarcha, E.J.; Londono, L.M.; Sims-Fahey, B.; Upadhyay, S.K.; Lakey, J.T.; Iadonato, S.; Wulff, H.; et al. Development of a sea anemone toxin as an immunomodulator for therapy of autoimmune diseases. Toxicon 2012, 59, 529–546. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Parisi, M.G.; Cammarata, M. Granulocytes of sea anemone Actinia equina (Linnaeus, 1758) body fluid contain and release cytolysins forming plaques of lysis Abstract the Cnidaria phylum includes organisms that are among the most poisonous animals. The exact composit. Invertebr. Surviv. J. 2014, 11, 39–46. [Google Scholar]
- Olano, C.T.; Bigger, C.H. Phagocytic activities of the gorgonian coral Swiftia exserta. J. Invertebr. Pathol. 2000, 76, 176–184. [Google Scholar] [CrossRef]
- Mydlarz, L.D.; Holthouse, S.F.; Peters, E.C.; Harvell, C.D. Cellular responses in sea fan corals: Granular amoebocytes react to pathogen and climate stressors. PLoS ONE 2008, 3, e1811. [Google Scholar] [CrossRef]
- Toledo-hernandez, C.; Ruiz-Diaz, C. The immune responses of the coral. Invertebr. Surviv. J. 2014, 11, 319–328. [Google Scholar]
- Honma, T.; Shiomi, K. Peptide toxins in sea anemones: Structural and functional aspects. Mar. Biotechnol. 2006, 8, 1–10. [Google Scholar] [CrossRef] [Green Version]
- Honma, T.; Minagawa, S.; Nagai, H.; Ishida, M.; Nagashima, Y.; Shiomi, K. Novel peptide toxins from acrorhagi, aggressive organs of the sea anemone Actinia equina. Toxicon Off. J. Int. Soc. Toxinology 2005, 46, 768–774. [Google Scholar] [CrossRef]
- Parisi, M.G.; Trapani, M.R.; Cardinale, L.; Cammarata, M. Evidence of cytotoxic activity against mammalian red blood cell of Na+ channel neurotoxin (Ae1) from sea anemone (Actinia equina). Invertebr. Surviv. J. 2016, 13. [Google Scholar] [CrossRef]
- Evans, P.; Halliwell, B. Free radicals and hearing. Cause, consequence, and criteria. Ann. NY Acad. Sci. 1999, 884, 19–40. [Google Scholar] [CrossRef] [PubMed]
- Mydlarz, L.; Jacobs, R. An inducible release of reactive oxygen radicals in four species of gorgonian corals. Mar. Freshw. Behav. Physiol. 2006, 39, 143–152. [Google Scholar] [CrossRef]
- Robb, C.; Dyrynda, E.; Gray, R.; Rossi, A.; Smith, V. Invertebrate extracellular phagocyte traps show that chromatin is an ancient defence weapon. Nat. Commun. 2014, 5, 4627. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Perez, S.; Weis, V. Nitric oxide and cnidarian bleaching: An eviction notice mediates breakdown of a symbiosis. J. Exp. Biol. 2006, 209, 2804–2810. [Google Scholar] [CrossRef] [Green Version]
- Birben, E.; Sahiner, U.M.; Sackesen, C.; Erzurum, S.; Kalayci, O. Oxidative stress and antioxidant defense. World Allergy Organ. J. 2012, 5, 9–19. [Google Scholar] [CrossRef] [Green Version]
- Mydlarz, L.D.; Harvell, C.D. Peroxidase activity and inducibility in the sea fan coral exposed to a fungal pathogen. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 2007, 146, 54–62. [Google Scholar] [CrossRef]
- Diaz, J.M.; Hansel, C.M.; Apprill, A.; Brighi, C.; Zhang, T.; Weber, L.; McNally, S.; Xun, L. Species-specific control of external superoxide levels by the coral holobiont during a natural bleaching event. Nat. Commun. 2016, 7, 13801. [Google Scholar] [CrossRef] [Green Version]
- Merle, P.-L.; Sabourault, C.; Richier, S.; Allemand, D.; Furla, P. Catalase characterization and implication in bleaching of a symbiotic sea anemone. Free Radic. Biol. Med. 2007, 42, 236–246. [Google Scholar] [CrossRef]
- Hawkridge, J.M.; Pipe, R.K.; Brown, B.E. Localisation of antioxidant enzymes in the cnidarians Anemonia viridis and Goniopora stokesi. Mar. Biol. 2000, 137, 1–9. [Google Scholar] [CrossRef]
- Goulet, T.L.; Shirur, K.P.; Ramsby, B.D.; Iglesias-Prieto, R. The effects of elevated seawater temperatures on Caribbean gorgonian corals and their algal symbionts, Symbiodinium spp. PLoS ONE 2017, 12, e0171032. [Google Scholar] [CrossRef] [PubMed]
- Saragosti, E.; Tchernov, D.; Katsir, A.; Shaked, Y. Extracellular production and degradation of superoxide in the coral Stylophora pistillata and cultured Symbiodinium. PLoS ONE 2010, 5, e12508. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Tchernov, D.; Kvitt, H.; Haramaty, L.; Bibby, T.S.; Gorbunov, M.Y.; Rosenfeld, H.; Falkowski, P.G. Apoptosis and the selective survival of host animals following thermal bleaching in zooxanthellate corals. Proc. Natl. Acad. Sci. USA 2011, 108, 9905–9909. [Google Scholar] [CrossRef] [Green Version]
- Downs, C.A.; Fauth, J.; Halas, J.; Dustan, P.; Bemiss, J.; Woodley, C.M. Oxidative stress and seasonal coral bleaching. Free Radic. Biol. Med. 2002, 33, 533–543. [Google Scholar] [CrossRef]
- Lesser, M.P. Oxidative stress in marine environments: Biochemistry and physiological ecology. Annu. Rev. Physiol. 2006, 68, 253–278. [Google Scholar] [CrossRef] [Green Version]
- Palmer, C.V.; Modi, C.K.; Mydlarz, L.D. Coral fluorescent proteins as antioxidants. PLoS ONE 2009, 4, e7298. [Google Scholar] [CrossRef] [Green Version]
- Daly, M.; Chaudhuri, A.; Gusmão, L.; Rodríguez, E. Phylogenetic relationships among sea anemones (Cnidaria: Anthozoa: Actiniaria). Mol. Phylogenet. Evol. 2008, 48, 292–301. [Google Scholar] [CrossRef]
- Daly, M.; Brugler, M.; Cartwright, P.; Collins, A.; Dawson, M.; Fautin, D.; France, S.; McFadden, C.; Opresko, D.; Rodriguez, E.; et al. The Phylum Cnidaria: A Review of Phylogenetic Patterns and Diversity 300 Years After Linnaeus. Zootaxa 2006, 1668. [Google Scholar] [CrossRef]
- Fautin, D.G.; Malarky, L.; Soberón, J. Latitudinal diversity of sea anemones (Cnidaria: Actiniaria). Biol. Bull. 2013, 224, 89–98. [Google Scholar] [CrossRef] [Green Version]
- Geller, J.; Fitzgerald, L.; King, C. Fission in Sea Anemones: Integrative Studies of Life Cycle Evolution. Integr. Comp. Biol. 2005, 45, 615–622. [Google Scholar] [CrossRef]
- Ganot, P.; Moya, A.; Magnone, V.; Allemand, D.; Furla, P.; Sabourault, C. Adaptations to endosymbiosis in a Cnidarian-Dinoflagellate association: Differential gene expression and specific gene duplications. PLoS Genet. 2011, 7. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Trapani, M.R.; Parisi, M.G.; Parrinello, D.; Sanfratello, M.A.; Benenati, G.; Palla, F.; Cammarata, M. Specific inflammatory response of Anemonia sulcata (Cnidaria) after bacterial injection causes tissue reaction and enzymatic activity alteration. J. Invertebr. Pathol. 2016, 135, 15–21. [Google Scholar] [CrossRef] [PubMed]
- Wiedenmann, J.; Elke, C.; Spindler, K.D.; Funke, W. Cracks in the beta-can: Fluorescent proteins from Anemonia sulcata (Anthozoa, Actinaria). Proc. Natl. Acad. Sci. USA 2000, 97, 14091–14096. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Parisi, M.G.; Lentini, A.; Cammarata, M. Seasonal changes in morpho-functional aspects of two Anemonia sulcata (Pennant, 1777) wild populations. Mar. Biodivers. 2017, 47, 561–573. [Google Scholar] [CrossRef]
- Xu, H.; Feng, B.; Xie, M.; Ren, Y.; Xia, J.; Zhang, Y.; Wang, A.; Li, X. Physiological Characteristics and Environment Adaptability of Reef-Building Corals at the Wuzhizhou Island of South China Sea. Front. Physiol. 2020, 11, 390. [Google Scholar] [CrossRef]
- Bruckner, A.W. History of coral disease research. Diseases of Coral. In Diseases of Coral, 1st ed.; Woodley, C.M., Downs, C.A., Eds.; Wiley: New York, NY, USA, 2015; pp. 52–84. [Google Scholar] [CrossRef]
- Reed, K.C.; Muller, E.M.; Van Woesik, R. Coral immunology and resistance to disease. Dis. Aquat. Organ. 2010, 90, 85–92. [Google Scholar] [CrossRef] [Green Version]
- Hutton, D.; Smith, V.J. Antibacterial properties of isolated amoebocytes from the sea anemone Actinia equina. Biol. Bull. 1996, 191, 441–451. [Google Scholar] [CrossRef]
- Kortschak, R.; Samuel, G.; Saint, R.; Miller, D. EST analysis of the Cnidarian Acropora millepora reveals extensive gene loss and rapid sequence divergence in the model invertebrates. Curr. Biol. 2003, 13, 2190–2195. [Google Scholar] [CrossRef]
- Libro, S.; Kaluziak, S.; Vollmer, S. RNA-seq Profiles of Immune Related Genes in the Staghorn Coral Acropora cervicornis Infected with White Band Disease. PLoS ONE 2013, 8, e81821. [Google Scholar] [CrossRef] [Green Version]
- Wright, R.M.; Kenkel, C.D.; Dunn, C.E.; Shilling, E.N.; Bay, L.K.; Matz, M.V. Intraspecific differences in molecular stress responses and coral pathobiome contribute to mortality under bacterial challenge in Acropora millepora. Sci. Rep. 2017, 7. [Google Scholar] [CrossRef] [Green Version]
- Ritchie, K. Regulation of microbial populations by coral surface mucus and mucus-associated bacteria. Mar. Ecol. Prog. Ser. 2006, 322, 1–14. [Google Scholar] [CrossRef]
- Frydenborg, B.R.; Krediet, C.J.; Teplitski, M.; Ritchie, K.B. Temperature-dependent inhibition of opportunistic Vibrio pathogens by native coral commensal bacteria. Microb. Ecol. 2014, 67, 392–401. [Google Scholar] [CrossRef] [PubMed]
- Vargas-Angel, B.; Peters, E.C.; Kramarsky-Winter, E.; Gilliam, D.S.; Dodge, R.E. Cellular reactions to sedimentation and temperature stress in the Caribbean coral Montastraea cavernosa. J. Invertebr. Pathol. 2007, 95, 140–145. [Google Scholar] [CrossRef] [PubMed]
- Palmer, C.V.; Traylor-Knowles, N.G.; Willis, B.L.; Bythell, J.C. Corals use similar immune cells and wound-healing processes as those of higher organisms. PLoS ONE 2011, 6, 1–11. [Google Scholar] [CrossRef] [Green Version]
- Patterson, M.; Landolt, M. Cellular reaction to injury in the anthozoan Anthopleura elegantissima. J. Invertebr. Pathol. 1979, 33, 189–196. [Google Scholar] [CrossRef]
- Meszaros, A.; Bigger, C.H. Qualitative and quantitative study of wound healing 1018 processes in the coelenterate, Plexaurella fusifera: Spatial, temporal, and environmental (light attenuation) influences. J. Invert. Pathol. 1999, 73, 321–331. [Google Scholar] [CrossRef]
- Vargas-Angel, B. Coral health and disease assessment in the US Pacific Remote Island Areas. Bull. Mar. Sci. 2009, 84, 211–227. [Google Scholar]
- Hoffmeister, S. Isolation and characterization of two new morpho-genetically active peptides from Hydra vulgaris. Development 1996, 122, 1941–1948. [Google Scholar]
PRR | MAMP |
---|---|
Toll-like receptor (TLRs) [2,17,61] Extracellular leucine-rich repeat (LRRs) [36,69] Intracellular domain, TIR domain activating NF-κB pathway [17,52,70,71] Integrin [72,73] Scavenger receptors (SR) [74] | Bacterial flagellin, Glycans, lipopolysaccharide (LPS), double-stranded RNA, Peptidoglycan (PG), Glycosylphosphatidylinositol (GPI) anchors |
Lectins [52,75,76,77] | Glycolipids, glycoproteins |
Nucleotide-binding oligomerization domain protein (NOD) [2,8,52,69] | Intracellular MAMPs, including LPS |
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Parisi, M.G.; Parrinello, D.; Stabili, L.; Cammarata, M. Cnidarian Immunity and the Repertoire of Defense Mechanisms in Anthozoans. Biology 2020, 9, 283. https://doi.org/10.3390/biology9090283
Parisi MG, Parrinello D, Stabili L, Cammarata M. Cnidarian Immunity and the Repertoire of Defense Mechanisms in Anthozoans. Biology. 2020; 9(9):283. https://doi.org/10.3390/biology9090283
Chicago/Turabian StyleParisi, Maria Giovanna, Daniela Parrinello, Loredana Stabili, and Matteo Cammarata. 2020. "Cnidarian Immunity and the Repertoire of Defense Mechanisms in Anthozoans" Biology 9, no. 9: 283. https://doi.org/10.3390/biology9090283