Skip to main content
Log in

The immunotranscriptome of the Caribbean reef-building coral Pseudodiploria strigosa

  • Original Paper
  • Published:
Immunogenetics Aims and scope Submit manuscript

Abstract

The viability of coral reefs worldwide has been seriously compromised in the last few decades due in part to the emergence of coral diseases of infectious nature. Despite important efforts to understand the etiology and the contribution of environmental factors associated to coral diseases, the mechanisms of immune response in corals are just beginning to be studied systematically. In this study, we analyzed the set of conserved immune response genes of the Caribbean reef-building coral Pseudodiploria strigosa by Illumina-based transcriptome sequencing and annotation of healthy colonies challenged with whole live Gram-positive and Gram-negative bacteria. Searching the annotated transcriptome with immune-related terms yielded a total of 2782 transcripts predicted to encode conserved immune-related proteins that were classified into three modules: (a) the immune recognition module, containing a wide diversity of putative pattern recognition receptors including leucine-rich repeat-containing proteins, immunoglobulin superfamily receptors, representatives of various lectin families, and scavenger receptors; (b) the intracellular signaling module, containing components from the Toll-like receptor, transforming growth factor, MAPK, and apoptosis signaling pathways; and (3) the effector module, including the C3 and factor B complement components, a variety of proteases and protease inhibitors, and the melanization-inducing phenoloxidase. P. strigosa displays a highly variable and diverse immune recognition repertoire that has likely contributed to its resilience to coral diseases.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Augustin R, Fraune S, Bosch TCG (2010) How Hydra senses and destroys microbes. Semin Immunol 22:54–58

    Article  CAS  PubMed  Google Scholar 

  • Bayer T, Aranda M, Sunagawa S, Yum LK, Desalvo MK, Lindquist E, Coffroth MA, Voolstra CR, Medina M (2012) Symbiodinium transcriptomes: genome insights into the dinoflagellate symbionts of reef-building corals. PLoS One 7, e35269

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Beisel HG, Kawabata S, Iwanaga S, Huber R, Bode W (1999) Tachylectin-2: crystal structure of a specific GlcNAc/GalNAc-binding lectin involved in the innate immunity host defense of the Japanese horseshoe crab Tachypleus tridentatus. EMBO J 18:2313–2322

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Bianchet MA, Odom EW, Vasta GR, Amzel LM (2002) A novel fucose recognition fold involved in innate immunity. Nature Struct Mol Biol 9:628–634

    CAS  Google Scholar 

  • Bosch TC (2013) Cnidarian-microbe interactions and the origin of innate immunity in metazoans. Annu Rev Microbiol 67:499–518

    Article  CAS  PubMed  Google Scholar 

  • Bosch TCG, Augustin R, Anton-Erxleben F, Fraune S, Hemmrich G, Zill H, Rosenstiel P, Jacobs G, Schreiber S, Leippe M, Stanisak M, Grötzinger J, Jung S, Podschun R, Bartels J, Harder J, Schröder J-M (2009) Uncovering the evolutionary history of innate immunity: the simple metazoan Hydra uses epithelial cells for host defence. Dev Comp Immunol 33:559–569

    Article  CAS  PubMed  Google Scholar 

  • Carpenter KE, Abrar M, Aeby G, Aronson RB, Banks S, Bruckner A, Chiriboga A, Cortés J, Delbeek JC, Devantier L, Edgar GJ, Edwards AJ, Fenner D, Guzmán HM, Hoeksema BW, Hodgson G, Johan O, Licuanan WY, Livingstone SR, Lovell ER, Ja M, Obura DO, Ochavillo D, Ba P, Precht WF, Quibilan MC, Reboton C, Richards ZT, Rogers AD, Sanciangco J, Sheppard A, Sheppard C, Smith J, Stuart S, Turak E, Veron JEN, Wallace C, Weil E, Wood E (2008) One-third of reef-building corals face elevated extinction risk from climate change and local impacts. Science 321:560–563

    Article  CAS  PubMed  Google Scholar 

  • Cerenius L, Lee BL, Söderhäll K (2008) The proPO-system: pros and cons for its role in invertebrate immunity. Trends Immunol 29:263–271

    Article  CAS  PubMed  Google Scholar 

  • Constanza R, dArge R, deGroot R, Farber S, Grasso M, Hannon B (1997) The value of the world’s ecosystem services and natural capital. Nature 387:253–260

    Article  Google Scholar 

  • Conus S, Simon H-U (2010) Cathepsins and their involvement in immune responses. Swiss Med Weekly 140:w13042

    Google Scholar 

  • DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, Huber T, Dalevi D, Hu P, Andersen GL (2006) Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol 72:5069–5072

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Dishaw LJ, Smith SL, Bigger CH (2005) Characterization of a C3-like cDNA in a coral: phylogenetic implications. Immunogenetics 57:535–548

    Article  CAS  PubMed  Google Scholar 

  • Doolittle RF, McNamara K, Lin K (2012) Correlating structure and function during the evolution of fibrinogen-related domains. Protein Sci 21:1808–1823

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Dunn SR (2009) Immunorecognition and immunoreceptors in the Cnidaria. Invert Surv J 6:7–14

    Google Scholar 

  • Franchi L, Warner N, Viani K, Nunez G (2009) Function of Nod-like receptors in microbial recognition and host defense. Immunol Rev 227:106–128

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Fujito NT, Sugimoto S, Nonaka M (2010) Evolution of thioester-containing proteins revealed by cloning and characterization of their genes from a cnidarian sea anemone, Haliplanella lineate. Dev Comp Immunol 34:775–784

    Article  CAS  PubMed  Google Scholar 

  • Gewurz H, Zhang XH, Lint TF (1995) Structure and function of the pentraxins. Curr Opin Immunol 7:54–64

    Article  CAS  PubMed  Google Scholar 

  • Gokudan S, Muta T, Tsuda R, Koori K, Kawahara T, Seki N, Mizunoe Y, Wai SN, Iwanaga S, Kawabata S (1999) Horseshoe crab acetyl group-recognizing lectins involved in innate immunity are structurally related to fibrinogen. Proc Natl Acad Sci U S A 96:10086–10091

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Grabherr MG, Haas BJ, Yassour M, Levin JZ, Da T, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q, Chen Z, Mauceli E, Hacohen N, Gnirke A, Rhind N, di Palma F, Birren BW, Nusbaum C, Lindblad-Toh K, Friedman N, Regev A (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nature Biotechnol 29:644–652

    Article  CAS  Google Scholar 

  • Griffiths-Jones S, Bateman A, Marshall M, Khanna A, Eddy SR (2003) Rfam: an RNA family database. Nucleic Acids Res 31:439–441

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Series 41:95–98

    CAS  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

    Article  Google Scholar 

  • Hayes ML, Eytan RI, Hellberg ME (2010) High amino acid diversity and positive selection at a putative coral immunity gene (tachylectin-2). BMC Evol Biol 10:150

    Article  PubMed Central  PubMed  Google Scholar 

  • Hughes TP, Baird AH, Bellwood DR, Card M, Connolly SR, Folke C, Grosberg R, Hoegh-Guldberg O, Jackson JBC, Kleypas J, Lough JM, Marshall P, Nyström M, Palumbi SR, Pandolfi JM, Rosen B, Roughgarden J (2003) Climate change, human impacts, and the resilience of coral reefs. Science 301:929–933

    Article  CAS  PubMed  Google Scholar 

  • Jackson JBC, Donovan MK, Cramer KL, Lam V (2014) Status and trends of Caribbean coral reefs: 1970-2012. Global Coral Reef Monitoring, IUCN, Gland

    Google Scholar 

  • Johansson MW (1999) Cell adhesion molecules in invertebrate immunity. Dev Comp Immunol 23:303–315

    Article  CAS  PubMed  Google Scholar 

  • Kang JY, Lee JO (2011) Structural biology of the Toll-like receptor family. Annu Rev Biochem 80:917–941

    Article  CAS  PubMed  Google Scholar 

  • Kenkel CD, Aglyamova G, Alamaru A, Bhagooli R, Capper R, Cunning R, deVillers A, Ja H, Hédouin L, Keshavmurthy S, Ka K, Mahmoud H, McGinty ES, Montoya-Maya PH, Palmer CV, Pantile R, Ja S, Schils T, Silverstein RN, Squiers LB, Tang P-C, Goulet TL, Matz MV (2011) Development of gene expression markers of acute heat-light stress in reef-building corals of the genus Porites. PLoS One 6, e26914

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kimura A, Sakaguchi E, Nonaka M (2009) Multi-component complement system of Cnidaria: C3, Bf, and MASP genes expressed in the endodermal tissues of a sea anemone, Nematostella vectensis. Immunobiology 214:165–178

    Article  CAS  PubMed  Google Scholar 

  • Kuehl K, Jones R, Gibbs D, Richardson L (2011) The roles of temperature and light in black band disease (BBD) progression on corals of the genus Diploria in Bermuda. J Invertebr Pathol 106:366–370

    Article  PubMed  Google Scholar 

  • Kvennefors ECE, Leggat W, Hoegh-Guldberg O, Degnan BM, Barnes AC (2008) An ancient and variable mannose-binding lectin from the coral Acropora millepora binds both pathogens and symbionts. Dev Comp Immunol 32:1582–1592

    Article  CAS  PubMed  Google Scholar 

  • Lange C, Hemmrich G, Klostermeier UC, López-Quintero JA, Miller DJ, Rahn T, Weiss Y, Bosch TCG, Rosenstiel P (2011) Defining the origins of the NOD-like receptor system at the base of animal evolution. Mol Biol Evol 28:1687–1702

    Article  CAS  PubMed  Google Scholar 

  • Lehnert EM, Burriesci MS, Pringle JR (2012) Developing the anemone Aiptasia as a tractable model for cnidarian-dinoflagellate symbiosis: the transcriptome of aposymbiotic A. pallida. BMC Genomics 13:271

    Article  PubMed Central  CAS  PubMed  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

    Article  PubMed Central  PubMed  Google Scholar 

  • Maidak BL, Cole JR, Lilburn TG, Parker CT Jr, Saxman PR, Stredwick JM, Garrity GM, Li B, Olsen GJ, Pramanik S, Schmidt TM, Tiedje JM (2000) The RDP (Ribosomal Database Project) continues. Nucleic Acids Res 28:173–174

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Martin JA, Wang Z (2011) Next-generation transcriptome assembly. Nat Rev Genet 12:671–682

    Article  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 

  • Miller DJ, Hemmrich G, Ball EE, Hayward DC, Khalturin K, Funayama N, Agata K, Bosch TCG (2007) The innate immune repertoire in cnidaria—ancestral complexity and stochastic gene loss. Genome Biol 8:R59

    Article  PubMed Central  PubMed  Google Scholar 

  • Moita LF, Vriend G, Mahairaki V, Louis C, Kafatos FC (2006) Integrins of Anopheles gambiae and a putative role of a new beta integrin, BINT2, in phagocytosis of E. coli. Insect Biochem Mol Biol 36:282–290

    Article  CAS  PubMed  Google Scholar 

  • Mukhopadhyay S, Gordon S (2004) The role of scavenger receptors in pathogen recognition and innate immunity. Immunobiology 209:39–49

    Article  CAS  PubMed  Google Scholar 

  • Mydlarz LD, Palmer CV (2011) The presence of multiple phenoloxidases in Caribbean reef-building corals. Comp Biochem Physiol Part A, Mol Integr Physiol 159:372–378

    Article  Google Scholar 

  • Mydlarz LD, Couch CS, Weil E, Smith G, Harvell CD (2009) Immune defenses of healthy, bleached and diseased Montastraea faveolata during a natural bleaching event. Dis Aquat Organ 87:67–78

    Article  CAS  PubMed  Google Scholar 

  • Nawijn MC, Hackett TL, Postma DS, van Oosterhout AJ, Heijink IH (2011) E-cadherin: gatekeeper of airway mucosa and allergic sensitization. Trends Immunol 32:248–255

    Article  CAS  PubMed  Google Scholar 

  • Nonaka M, Kimura A (2006) Genomic view of the evolution of the complement system. Immunogenetics 58:701–713

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Nonaka S, Nagaosa K, Mori T, Shiratsuchi A, Nakanishi Y (2013) Integrin alphaPS3/betanu-mediated phagocytosis of apoptotic cells and bacteria in Drosophila. J Biol Chem 288:10374–10380

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Palmer CV, Mydlarz LD, Willis BL (2008) Evidence of an inflammatory-like response in non-normally pigmented tissues of two scleractinian corals. Proc Biol Sci 275:2687–2693

    Article  PubMed Central  PubMed  Google Scholar 

  • Parra G, Bradnam K, Korf I (2007) CEGMA: a pipeline to accurately annotate core genes in eukaryotic genomes. Bioinformatics 23:1061–1067

    Article  CAS  PubMed  Google Scholar 

  • Parra G, Bradnam K, Ning Z, Keane T, Korf I (2009) Assessing the gene space in draft genomes. Nucleic Acids Res 37:289–297

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Petes LE, Harvell CD, Peters EC (2003) Pathogens compromise reproduction and induce melanization in Caribbean sea fans. Mar Ecol 264:167–171

    Article  Google Scholar 

  • Polato NR, Vera JC, Baums IB (2011) Gene discovery in the threatened elkhorn coral: 454 sequencing of the Acropora palmata transcriptome. PLoS One 6, e28634

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Poole AZ, Weis VM (2014) TIR-domain-containing protein repertoire of nine anthozoan species reveals coral-specific expansions and uncharacterized proteins. Dev Comp Immunol 46:480–488

    Article  CAS  PubMed  Google Scholar 

  • Proell M, Riedl SJ, Fritz JH, Rojas AM, Schwarzenbacher R (2008) The Nod-like receptor (NLR) family: a tale of similarities and differences. PLoS One 3, e2119

    Article  PubMed Central  PubMed  Google Scholar 

  • Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glockner FO (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41:D590–D596

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Rabinovich GA, Toscano MA (2009) Turning ‘sweet’ on immunity: galectin–glycan interactions in immune tolerance and inflammation. Nat Rev Immunol 9:338–352

    Article  CAS  PubMed  Google Scholar 

  • Rodriguez-Lanetty M, Harii S, Hoegh-Guldberg O (2009) Early molecular responses of coral larvae to hyperthermal stress. Mol Ecol 18:5101–5114

    Article  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

    Article  CAS  PubMed  Google Scholar 

  • Schmieder R, Lim YW, Edwards R (2011) Identification and removal of ribosomal RNA sequences from metatranscriptomes. Bioinformatics 433–435

  • Schwarz RS, Hodes-Villamar L, Fitzpatrick KA, Fain MG, Hughes AL, Cadavid LF (2007) A gene family of putative immune recognition molecules in the hydroid Hydractinia. Immunogenetics 59:233–246

    Article  CAS  PubMed  Google Scholar 

  • Schwarz JA, Brokstein PB, Voolstra C, Terry AY, Manohar CF, Miller DJ, Szmant AM, Coffroth MA, Medina M (2008) Coral life history and symbiosis: functional genomic resources for two reef building Caribbean corals, Acropora palmata and Montastraea faveolata. BMC Genomics 9:97

    Article  PubMed Central  PubMed  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

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Takeuchi O, Akira S (2010) Pattern recognition receptors and inflammation. Cell 140:805–820

    Article  CAS  PubMed  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Tateno H, Ogawa T, Muramoto K, Kamiya H, Saneyoshi M (2002) Distribution and molecular evolution of rhamnose-binding lectins in Salmonidae: isolation and characterization of two lectins from white-spotted Charr (Salvelinus leucomaenis) eggs. Biosci Biotechnol Biochem 66:1356–1365

    Article  CAS  PubMed  Google Scholar 

  • Vidal-Dupiol J, Ladrière O, Destoumieux-Garzón D, Sautière P-E, Meistertzheim A-L, 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Vidal-Dupiol J, Zoccola D, Tambutté E, Grunau C, Cosseau C, Smith KM, Freitag M, Dheilly NM, Allemand D, Tambutté S (2013) Genes related to ion-transport and energy production are upregulated in response to CO2-driven pH decrease in corals: new insights from transcriptome analysis. PLoS One 8, e58652

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Weil E, Rogers CS (2011) Coral reef diseases in the Atlantic-Caribbean. In: Dubinsky Z, Stambler N (eds) Coral Reefs: An Ecosystem in Transition. Springer, Amsterdam

    Google Scholar 

  • Weil E, Smith G, Gil-Agudelo DL (2006) Status and progress in coral reef disease research. Dis Aquat Organ 69:1–7

    Article  PubMed  Google Scholar 

  • Weiss Y, Forêt S, Hayward DC, Ainsworth T, King R, Ball EE, Miller DJ (2013) 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 Genomics 14:400

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wilkinson C (2008) Status of coral reefs of the world: 2008. Global Coral Reef Monitoring Network and Reef and Rainforest Research Center, Townsville

    Google Scholar 

  • Zdobnov EM, Apweiler R (2001) InterProScan—an integration platform for the signature-recognition methods in InterPro. Bioinformatics 17:847–848

    Article  CAS  PubMed  Google Scholar 

  • Zhang Y, Wang L, Wu N, Zhou Z, Song L (2012) An integrin from shrimp Litopenaeus vannamei mediated microbial agglutination and cell proliferation. PLoS One 7, e40615

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zhao P, Dong Z, Duan J, Wang G, Wang L, Li Y, Xiang Z, Xia Q (2012) Genome-wide identification and immune response analysis of serine protease inhibitor genes in the silkworm, Bombyx mori. PLoS One 7, e31168

    Article  PubMed Central  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Dr. Catalina Arévalo-Ferro for technical support and Andrea González, Iván Páez, and Juan Lugo for comments on the manuscript. This work was supported by a grant from Colombia’s Departamento Administrativo de Ciencia, Tecnología e Innovación - COLCIENCIAS (contract 322-2011) to LFC. This funding agency had no involvement in the design, sample collection, analysis, and interpretation of data, writing, or in the decision to submit the report for publication.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Luis F. Cadavid.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Figure S1

Size distribution of contigs (in bp) after assembling the processed sequence reads. (GIF 13 kb)

High resolution image (TIFF 131 kb)

Figure S2

Number of best BLAST hits by species resulting from comparing the P. strigosa transcriptome annotated with the Swissprot database (A) and the RefSeq database (B). (GIF 10 kb)

High resolution image (TIFF 374 kb)

Table S1

Number of sequence reads for the non-stimulated and immune-stimulated cDNA libraries in the pre-processing of the P. strigosa transcriptome. (DOCX 57 kb)

Table S2

Summary of the general assembly statistics for the P. strigosa transcriptome. (DOCX 50 kb)

Table S3

KEGG metabolic pathway analysis of the P. strigosa transcriptome comparing the number of transcripts for each sub-pathway between representative species. (DOCX 121 kb)

Table S4

Keyword list of immune-related terms used to search the annotated transcriptome of P. strigosa. (DOCX 70 kb)

Table S5

Predicted proteins of the P. strigosa immune recognition module. (DOCX 138 kb)

Table S6

Components of intracellular signaling pathways involved in immune responses predicted from the P. strigosa transcriptome. (DOCX 124 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ocampo, I.D., Zárate-Potes, A., Pizarro, V. et al. The immunotranscriptome of the Caribbean reef-building coral Pseudodiploria strigosa . Immunogenetics 67, 515–530 (2015). https://doi.org/10.1007/s00251-015-0854-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00251-015-0854-1

Keywords

Navigation