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The cell-surface protein composition of a coral symbiont, Breviolum psygmophilum, reveals a mechanism for host specificity and displays dynamic regulation during temperature stress

Abstract

The symbiosis between corals and dinoflagellates in the family Symbiodiniaceae is threatened by warming trends that induce coral bleaching, or symbiosis breakdown. Current models of symbiosis breakdown involve an immune response to an elevation in reactive oxygen species that ultimately results in the loss of the symbiont. However, the intimate nature of the symbiosis implies an important role for the symbiont surface as a point of interaction between partners. The response of symbiont cell surface proteins to experimental temperature stress was, therefore, investigated using a cell surface biotin probe. Cell-surface protein composition was found to be dynamically regulated in response to heat stress, particularly after 24 h of exposure to heat treatment. This pattern was primarily driven by an increased abundance in heat shock proteins, demonstrating that stress experienced by the symbiont can manifest at the cell surface. Elements known to activate host immunity were also increased in response to temperature stress, further demonstrating an avenue by which the symbiont can elicit a host immune response independent of reactive oxygen species. This work documents the cell surface protein composition of a Symbiodiniaceae species for the first time and highlights host–symbiont interaction mechanisms that may be important during symbiosis breakdown.

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Data availability statement

All proteomic data collected and analyzed within the current study are in the Supplementary Tables, or available from the corresponding author upon request. Sequences listed in supplementary material were identified using a translated Breviolum psygmophilum transcriptome publicly available from Reef Genomics databases.

References

  1. Aisina RB, Mukhametova LI (2014) Structure and function of plasminogen/plasmin system. Russ J Bioorg 40:590–605

    CAS  Google Scholar 

  2. Aizawa K, Miyachi S (1984) Carbonic anhydrase located on cell surface increases the affinity for inorganic carbon in photosynthesis of Dunaliella tertiolecta. FEBS J 173:41–44

    CAS  Google Scholar 

  3. Allemand D, Furla P, Bénazet-Tambutté S (1998) Mechanisms of carbon acquisition for endosymbiont photosynthesis in Anthozoa. Can J Bot 76:925–941

    CAS  Google Scholar 

  4. Amblee V, Jeffery CJ (2015) Physical features of intracellular proteins that moonlight on the cell surface. PLoS ONE 10(6):e0130575. https://doi.org/10.1371/journal.pone.0130575

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  5. Arike L, Peil L (2014) Spectral counting label-free proteomics. In: Martins-de-Souza D (ed) Shotgun proteomics: methods and protocols. Springer, New York, pp 213–222

    Google Scholar 

  6. Asea A, Rehli M, Kabingu E, Boch JA, Bare O, Auron PE, Stevenson MA, Calderwood SK (2002) Novel signal transduction pathway utilized by extracellular HSP70: role of toll-like receptor (TLR) 2 and TLR4. J Biol Chem 277:15028–15034

    CAS  PubMed  Google Scholar 

  7. Audrito V, Serra S, Brusa D, Mazzola F, Arruga F, Vaisitti T, Coscia M, Maffei R, Rossi D, Wang T, Inghirami G, Rizzi M, Gaidano G, Garcia JG, Wolberger C, Raffaelli N, Deaglio S (2015) Extracellular nicotinamide phosphoribosyltransferase (NAMPT) promotes M2 macrophage polarization in chronic lymphocytic leukemia. Blood 125:111–123

    CAS  PubMed  Google Scholar 

  8. Ayón-Núñez DA, Fragoso G, Bobes RJ, Laclette JP (2018) Plasminogen-binding proteins as an evasion mechanism of the host’s innate immunity in infectious diseases. Biosci Rep. https://doi.org/10.1042/BSR20180705

    Article  PubMed  PubMed Central  Google Scholar 

  9. Baker A (2003) Flexibility and specificity in coral-algal symbiosis: diversity, ecology, and biogeography of symbiodinium. Annu Rev Ecol Evol Syst 34:661–689

    Google Scholar 

  10. Banerjee R (2012) Redox outside the box: linking extracellular redox remodeling with intracellular redox metabolism. J Biol Chem 287:4397–4402

    CAS  PubMed  Google Scholar 

  11. Berthelier J, Schnitzler CE, Wood-Charlson EM, Poole AZ, Weis VM, Detournay O (2017) Implication of the host TGFβ pathway in the onset of symbiosis between larvae of the coral Fungia scutaria and the dinoflagellate Symbiodinium sp. (clade C1f). Coral Reefs 36:1263–1268

    Google Scholar 

  12. Bertucci A, Tambutté E, Tambutté S, Allemand D, Zoccola D (2010) Symbiosis-dependent gene expression in coral–dinoflagellate association: cloning and characterization of a P-type H+-ATPase gene. Proc Biol Sci 277:87–95

    CAS  PubMed  Google Scholar 

  13. Bonifati V, Rizzu P, van Baren MJ, Schaap O, Breedveld GJ, Krieger E, Dekker MC, Squitieri F, Ibanez P, Joosse M, van Dongen JW, Vanacore N, van Swieten JC, Brice A, Meco G, van Duijn CM, Oostra BA, Heutink P (2003) Mutations in the DJ-1 gene associated with autosomal recessive early-onset parkinsonism. Science 299:256–259

    CAS  PubMed  Google Scholar 

  14. Brodersen DE, Nissen P (2005) The social life of ribosomal proteins. FEBS J 272:2098–2108

    CAS  PubMed  Google Scholar 

  15. Calderan-Rodrigues MJ, Jamet E, Bonassi MB, Guidetti-Gonzalez S, Begossi AC, Setem LV, Franceschini LM, Fonseca JG, Labate CA (2014) Cell wall proteomics of sugarcane cell suspension cultures. Proteomics 14:738–749

    CAS  PubMed  Google Scholar 

  16. Carta S, Castellani P, Delfino L, Tassi S, Venè R, Rubartelli A (2009) DAMPs and inflammatory processes: the role of redox in the different outcomes. J Leukoc Biol 86:549–555

    CAS  PubMed  Google Scholar 

  17. Chakrabarty J, Naik A, Fessler M, Munske G, Chowdhury S (2016) Differential tandem mass spectrometry-based cross-linker: a new approach for high confidence in identifying protein cross-linking. Anal Chem 18:10215–10222

    Google Scholar 

  18. Chan J, Crowell E, Eder M, Calder G, Bunnewell S, Findlay K, Vernhettes S, Höfte H, Lloyd C (2010) The rotation of cellulose synthase trajectories is microtubule dependent and influences the texture of epidermal cell walls in Arabidopsis hypocotyls. J Cell Sci 123:3490–3495

    CAS  PubMed  Google Scholar 

  19. Chana-Muñoz A, Jendroszek A, Sønnichsen M, Wang T, Ploug M, Jensen JK, Andreasen PA, Bendixen C, Panitz F (2019) Origin and diversification of the plasminogen activation system among chordates. BMC Evol Biol 19:27

    PubMed  PubMed Central  Google Scholar 

  20. Chang SS, Prezelin BB, Trench RK (1983) Mechanisms of photoadaptation in three strains of the symbiotic dinoflagellate Symbiodinium microadriaticum. Mar Biol 76:219–229

    CAS  Google Scholar 

  21. Chao Y, Fan C, Liang Y, Gao B, Zhang S (2012) A novel serpin with antithrombin-like activity in Branchiostoma japonicum: implications for the presence of a primitive coagulation system. PLoS ONE 7(3):e32392. https://doi.org/10.1371/journal.pone.0032392

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  22. Chivasa S, Murphy AM, Hamilton JM, Lindsey K, Carr JP, Slabas AR (2009) Extracellular ATP is a regulator of pathogen defence in plants. Plant J 60:436–448

    CAS  PubMed  Google Scholar 

  23. Clarke KR (1993) Non-parametric multivariate analyses of changes in community structure. Aust Ecol 18:117–143

    Google Scholar 

  24. Cohen J (1992a) A power primer. Psychol Bull 112:155–159

    CAS  PubMed  Google Scholar 

  25. Cohen J (1992b) Statistical power analysis. Curr Dir Psychol Sci 1:98–101

    Google Scholar 

  26. Colombo-Pallotta MF, Rodriguez-Roman A, Iglesias-Prieto R (2010) Calcification in bleached and unbleached Montastraea faveolata: evaluating the role of oxygen and glycerol. Coral Reefs 29:899–907

    Google Scholar 

  27. Cvitanovic C, Wilson SK, Fulton CJ, Almany GR, Anderson P, Babcock RC, Ban NC, Beeden RJ, Beger M, Cinner J, Dobbs K, Evans LS, Farnham A, Friedman KJ, Gale K, Gladstone W, Grafton Q, Graham NAJ, Gudge S, Harrison PL, Holmes TH, Johnstone N, Jones GP, Jordan A, Kendrick AJ, Klein CJ, Little LR, Malcolm HA, Morris D, Possingham HP, Prescott J, Pressey RL, Skilleter GA, Simpson C, Waples K, Wilson D, Williamson DH (2013) Critical research needs for managing coral reef marine protected areas: perspectives of academics and managers. J Environ Manag 114:84–91

    CAS  Google Scholar 

  28. Davy SK, Allemand D, Weis VM (2012) Cell biology of cnidarian-dinoflagellate symbiosis. Microbiol Mol Biol Rev 76:229–261

    CAS  PubMed  PubMed Central  Google Scholar 

  29. Deniaud-Bouët E, Hardouina K, Potina P, Kloarega B, Hervé C (2017) A review about brown algal cell walls and fucose-containing sulfated polysaccharides: cell wall context, biomedical properties and key research challenges. Carbohydr Polym 175:395–408

    PubMed  Google Scholar 

  30. Ebnet K (2017) Junctional adhesion molecules (JAMs): cell adhesion receptors with pleiotropic functions in cell physiology and development. Physiol Rev 97:1529–1554

    CAS  PubMed  Google Scholar 

  31. Edmunds PJ, Spencer Davies P (1986) An energy budget for Porites porites (Scleractinia). Mar Biol 92:339–347

    Google Scholar 

  32. Elschenbroich S, Kim Y, Medin JA, Kislinger T (2010) Isolation of cell surface proteins for mass spectrometry-based proteomics. Expert Rev Proteom 7:141–154

    CAS  Google Scholar 

  33. Federica T, Antonio G (2018) Systematic review of plasma-membrane ecto-ATP synthase: a new player in health and disease. Exp Mol Pathol 104:59–70

    Google Scholar 

  34. Ferro M, Seigneurin-Berny D, Rolland N, Chapel A, Salvi D, Garin J, Joyard J (2000) Organic solvent extraction as a versatile procedure to identify hydrophobic chloroplast membrane proteins. Electrophoresis 21:3517–3526

    CAS  PubMed  Google Scholar 

  35. Friedrich S, Konietschke F, Pauly M (2018) MANOVA.RM: analysis of multivariate data and repeated measures designs. R package version 0.3.2. https://github.com/smn74/MANOVA.RM

  36. Furla P, Allemand D, Orsenigo MN (2000) Involvement of H(+)-ATPase and carbonic anhydrase in inorganic carbon uptake for endosymbiont photosynthesis. Am J Physiol Regul Integr Comp Physiol 278:R870–R881

    CAS  PubMed  Google Scholar 

  37. Gancedo C, Flores CL, Gancedo JM (2016) The expanding landscape of moonlighting proteins in yeasts. Microbiol Mol Biol Rev 80:765–777

    CAS  PubMed  PubMed Central  Google Scholar 

  38. Gates RD, Baghdasarian G, Muscatine L (1992) Temperature stress causes host cell detachment in symbiotic cnidarians: implications for. Biol Bull 182:324–332

    CAS  PubMed  Google Scholar 

  39. Greenland S, Stephen J, Senn SJ, Rothman KJ, Carlin JB, Poole C, Goodman SN, Altman DG (2016) Statistical tests, P values, confidence intervals, and power: a guide to misinterpretations. Eur J Epidemiol 31:337–350

    PubMed  PubMed Central  Google Scholar 

  40. Hahn M, Mendgen K (2001) Signal and nutrient exchange at biotrophic plant-fungus interfaces. Curr Opin Plant Biol 4:322–327

    CAS  PubMed  Google Scholar 

  41. Hasanuzzaman M, Nahar K, Alam MM, Roychowdhury R, Fujita M (2013) Physiological, biochemical, and molecular mechanisms of heat stress tolerance in plants. Int J Mol Sci 14:9643–9684

    PubMed  PubMed Central  Google Scholar 

  42. Hassan S, Mathesius U (2012) The role of flavonoids in root-rhizosphere signalling: opportunities and challenges for improving plant–microbe interactions. J Exp Bot 63:3429–3444

    CAS  PubMed  Google Scholar 

  43. Hoegh-Guldberg (1999) Climate change, coral bleaching and the future of the worldís coral reefs. Mar Freshw Res 50:839–866

    Google Scholar 

  44. Hoegh-Guldberg O, Mumby PJ, Hooten AJ, Steneck RS, Greenfield P, Gomez E, Harvell CD, Sale PF, Edwards AJ, Caldeira K, Knowlton N, Eakin CM, Iglesias-Prieto R, Muthiga N, Bradbury RH, Dubi A, Hatziolos ME (2007) Coral reefs under rapid climate change and ocean acidification. Science 318:1737–1742

    CAS  PubMed  PubMed Central  Google Scholar 

  45. Howes MT, Kirkham M, Riches J, Cortese K, Walser PJ, Simpson F, Hill MM, Jones A, Lundmark R, Lindsay MR, Hernandez-Deviez DJ, Hadzic G, McCluskey A, Bashir R, Liu L, Pilch P, McMahon H, Robinson PJ, Hancock JF, Mayor S, Parton RG (2010) Clathrin-independent carriers form a high capacity endocytic sorting system at the leading edge of migrating cells. J Cell Biol 190:675–691

    CAS  PubMed  PubMed Central  Google Scholar 

  46. Jeffery CJ (2015) Why study moonlighting proteins? Front genet 6:211. https://doi.org/10.3389/fgene.2015.00211

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  47. Jimbo M, Yamashita H, Koike K, Sakai R, Kamiya H (2010) Effects of lectin in the scleractinian coral Ctenactis echinata on symbiotic zooxanthellae. Fish Sci 76:355–363

    CAS  Google Scholar 

  48. Jo E, Webb S, Klemke G (2010) Cell signaling by urokinase-type plasminogen activator receptor induces stem cell–like properties in breast cancer cells. Cancer Res 70:8948–8958

    CAS  PubMed  PubMed Central  Google Scholar 

  49. Jones AR IV, Meshulam T, Oliveira MF, Burritt N, Corkey BE (2015) Extracellular redox regulation of intracellular reactive oxygen generation, mitochondrial function and lipid turnover in cultured human adipocytes. PLoS ONE 11(10):e0164011. https://doi.org/10.1371/journal.pone.0164011

    CAS  Article  Google Scholar 

  50. Kamal AHM, Chakrabarty JK, Udden SMN, Zaki MdH, Chowdhury SM (2018) Inflammatory proteomic network analysis of statin-treated and lipopolysaccharide-activated macrophages. Sci Rep 8:164. https://doi.org/10.1038/s41598-017-18533-1

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  51. Karim W, Kaswadji R, Prartono T, Gorettipanggabean LM (2011) Growth and extracellular carbonic anhydrase activity of zooxanthellae Symbiodinium sp. in response of zinc enrichment. Hayati J Biosci 18:157–163

    Google Scholar 

  52. Koike K, Jimbo M, Sakai R, Kaeriyama M, Muramoto K, Ogata T, Maruyama T, Kamiya H (2004) Octocoral chemical signaling selects and controls dinoflagellate symbionts. Biol Bull 207:80–86

    CAS  PubMed  Google Scholar 

  53. 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 

  54. Lee SK, Kim Y, Kim SS, Lee JH, Cho K, Lee SS, Lee ZW, Kwon KH, Kim YH, Suh-Kim H, Yoo JS, Park YM (2009) Differential expression of cell surface proteins in human bone marrow mesenchymal stem cells cultured with or without basic fibroblast growth factor containing medium. Proteomics 9:4389–4405

    CAS  PubMed  Google Scholar 

  55. Lee SY, Jeong HJ, Kang MS, Jang TY, Jang SH, Lim AS (2014) Morphological characterization of Symbiodinium minutum and S. psygmophilum belonging to clade B. Algae 29:299–310

    Google Scholar 

  56. Lemmon MA, Freed DM, Schlessinger J, Kiyatkin A (2016) The dark side of cell signaling: positive roles for negative regulators. Cell 164:1172–1184

    CAS  PubMed  PubMed Central  Google Scholar 

  57. Li C, Wang DaZhi, Dong H, Xie Z, Hong H (2012) Proteomics of a toxic dinoflagellate Alexandrium catenella DH01: detection and identification of cell surface proteins using fluroescent labeling. Sci Bull 57:3320–3327

    CAS  Google Scholar 

  58. Li H, Huang Z, Ye S, Lu C, Cheng P, Chen S, Chen C (2013) Membrane labeling of coral gastrodermal cells by biotinylation: the proteomic identification of surface proteins involving cnidaria-dinoflagellate endosymbiosis. PLoS ONE 9(1):e85119. https://doi.org/10.1371/journal.pone.0085119

    CAS  Article  Google Scholar 

  59. Liew YJ, Aranda M, Voolstra CR (2016) Reefgenomics.Org—a repository for marine genomics data. Database. https://doi.org/10.1093/database/baw152

    Article  PubMed  PubMed Central  Google Scholar 

  60. Lin S, Cheng S, Song B, Zhong X, Lin X, Li W, Li L, Zhang Y, Zhang H, Ji Z, Cai M, Zhuang Y, Shi X, Lin L, Wang L, Wang Z, Liu X, Yu S, Zeng P, Hao H, Zou Q, Chen C, Li Y, Wang Y, Xu C, Meng S, Xu X, Wang J, Yang H, Campbell DA, Sturm NR, Dagenais-Bellefeuille S, Morse D (2015) The Symbiodinium kawagutii genome illuminates dinoflagellate gene expression and coral symbiosis. Science 350:691–694

    CAS  PubMed  Google Scholar 

  61. Little AF, van Oppen MJ, Willis BL (2004) Flexibility in algal endosymbioses shapes growth in reef corals. Science 304:1492–1494

    CAS  PubMed  Google Scholar 

  62. Logan D, LaFlamme A, Weis V, Davy S (2010) Flow-cytometric characterization of the cell-surface glycans of symbiotic dinoflagellates (Symbiodinium Spp.). J Phycol 46:525–533

    CAS  Google Scholar 

  63. Madeira F, Park YM, Lee J, Buso N, Gur T, Madhusoodanan N, Basutkar P, Tivey ARN, Potter SC, Finn RD, Lopez R (2019) The EMBL-EBI search and sequence analysis tools APIs in 2019. Nucleic Acids Res. https://doi.org/10.1093/nar/gkz268

    Article  PubMed  PubMed Central  Google Scholar 

  64. Madsen EB, Antolín-Llovera M, Grossmann C, Ye J, Vieweg S, Broghammer A, Krusell L, Radutoiu S, Jensen ON, Stougaard J, Parniske M (2011) Autophosphorylation is essential for the in vivo function of the Lotus japonicus Nod factor receptor 1 and receptor-mediated signalling in cooperation with Nod factor receptor 5. Plant J 65:404–417

    CAS  PubMed  Google Scholar 

  65. Majetschak M (2011) Extracellular ubiquitin: immune modulator and endogenous opponent of damage-associated molecular pattern molecules. J Leukoc Biol 89:205–219

    CAS  PubMed  Google Scholar 

  66. Mayfield AB, Chen Y-J, Lu C-Y, Chen C-S (2018) The proteomic response of the reef coral Pocillopora acuta to experimentally elevated temperatures. PLoS ONE 13(1):e0192001. https://doi.org/10.1371/journal.pone.0192001

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  67. McGinty E, Pieczonka J, Mydlarz L (2012) Variations in reactive oxygen release and antioxidant activity in multiple symbiodinium types in response to elevated temperature. Microb Ecol 64:1000–1007

    CAS  PubMed  Google Scholar 

  68. Merselis DG, Lirman D, Rodriguez-Lanetty M (2018) Symbiotic immuno-suppression: is disease susceptibility the price of bleaching resistance? PeerJ 6:e4494. https://doi.org/10.7717/peerj.4494

    Article  PubMed  PubMed Central  Google Scholar 

  69. Miles M, Voolstra CR, Castro CB, Pires DO, Calderon EN, Sumida PYG (2017) Expression of a symbiosis-specific gene in Symbiodinium type A1 associated with coral, nudibranch and giant clam larvae. R Soc Open Sci 4:170253. https://doi.org/10.1098/rsos.170253

    CAS  Article  Google Scholar 

  70. 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 

  71. Mustaffa NIH, Striebel M, Wurl O (2017) Enrichment of extracellular carbonic anhydrase in the sea surface microlayer and its effect on air–sea CO2 exchange. Geophys Res Lett 44:324–330

    Google Scholar 

  72. Oakley CA, Davy SK (2018) Cell biology of coral bleaching. In: van Oppen MJH, Lough JM (eds) Coral bleaching: patterns, processes, causes and consequences. Springer International Publishing, Switzerland, pp 189–211

    Google Scholar 

  73. Ochs J, LaRue T, Tinaz B, Yongue C, Domozych DS (2014) The cortical cytoskeletal network and cell-wall dynamics in the unicellular charophycean green alga Penium margaritaceum. Ann Bot 114:1237–1249

    CAS  PubMed  PubMed Central  Google Scholar 

  74. Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O'Hara RB, Simpson GL, Solymos P, Stevens MHH, Szoecs E, Wagner H (2018) vegan: Community Ecology Package. R package version 2.5–3. https://CRAN.R-project.org/package=vegan

  75. Oldroyd GE, Downie JA (2004) Calcium, kinases and nodulation signalling in legumes. Nat Rev Mol Cell Biol 5:566–576

    CAS  PubMed  Google Scholar 

  76. Orjalo AV, Bhaumik D, Gengler BK, Scott GK, Campisi J (2009) Cell surface-bound IL-1alpha is an upstream regulator of the senescence-associated IL-6/IL-8 cytokine network. Proc Natl Acad Sci USA 106:17031–17036

    CAS  PubMed  Google Scholar 

  77. Park SY, Kim IS (2017) Engulfment signals and the phagocytic machinery for apoptotic cell clearance. Exp Mol Med 49:e331

    CAS  PubMed  PubMed Central  Google Scholar 

  78. Parkinson JE, Baumgarten S, Michell CT, Baums IB, LaJeunesse TC, Voolstra CR (2016) Gene Expression variation resolves species and individual strains among coral-associated dinoflagellates within the genus Symbiodinium. Genome Biol Evol 8:665–680

    PubMed  PubMed Central  Google Scholar 

  79. Parkinson JE, Tivey TR, Mandelare PE, Adpressa DA, Loesgen S, Weis VM (2018) Subtle differences in symbiont cell surface glycan profiles do not explain species-specific colonization rates in a model cnidarian-algal symbiosis. Front Microbiol 9:842. https://doi.org/10.3389/fmicb.2018.00842

    Article  PubMed  PubMed Central  Google Scholar 

  80. Pelz T, Drose DR, Fleck D, Henkel B, Ackels T, Spehr M, Neuhaus EM (2018) An ancestral TMEM16 homolog from Dictyostelium discoideum forms a scramblase. PLoS ONE 13(2):e0191219. https://doi.org/10.1371/journal.pone.0191219

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  81. R Development Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/

  82. Rice ME, Harris GT (2005) Comparing effect sizes in follow-up studies: ROC area, Cohen’s d, and r. Law Hum Behav 5:615–620

    Google Scholar 

  83. Robinson DG, Ding Y, Jiang L (2016) Unconventional protein secretion in plants: a critical assessment. Protoplasma 253:31–43

    CAS  PubMed  Google Scholar 

  84. Roche P, Maillet F, Plazanet C, Debellé F, Ferro M, Truchet G, Promé JC, Dénarié J (1996) The common nodABC genes of Rhizobium meliloti are host-range determinants. Proc Natl Acad Sci 93:15305–15310

    CAS  PubMed  Google Scholar 

  85. Rodrigues ML, Godinho RM, Zamith-Miranda D, Nimrichter L (2015) Traveling into outer space: unanswered questions about fungal extracellular vesicles. PLoS Pathog 11:e1005240

    PubMed  PubMed Central  Google Scholar 

  86. Samuel M, Bleackley M, Anderson M, Mathivanan S (2015) Extracellular vesicles including exosomes in cross kingdom regulation: a view-point from plant–fungal interactions. Front Plant Sci 6:766

    PubMed  PubMed Central  Google Scholar 

  87. Sarras M, Deutzmann R (2001) Hydra and Niccolo Paganini (1782–1840)—two peas in a pod? The molecular basis of extracellular matrix structure in the invertebrate, Hydra. BioEssays 23:716–724

    CAS  PubMed  Google Scholar 

  88. Scotcher D, Billington S, Brown J, Jones CR, Brown CDA, Rostami-Hodjegan A, Galetin A (2017) Microsomal and cytosolic scaling factors in dog and human kidney cortex and application for in vitro-in vivo extrapolation of renal metabolic clearance. Drug Metab Dispos 45:556–568

    CAS  PubMed  PubMed Central  Google Scholar 

  89. Shi L, Dong H, Reguera G, Beyenal H, Lu A, Liu J, Yu HQ, Fredrickson JK (2016) Extracellular electron transfer mechanisms between microorganisms and minerals. Nat Rev Microbiol 1:651–662

    Google Scholar 

  90. Shimus, Levy, Herman (1985) A chemically cleavable biotinylated nucleotide: usefulness in the recovery of protein-DNA complexes from avidin affinity columns. Proc Natl Acad Sci 82:2593–2597

    Google Scholar 

  91. Shomer, Novacky, Pike, Yermiyahu, Kinraide (2003) Electrical potentials of plant cell walls in response to the ionic environment. Plant Physiol 133:411–422

    CAS  PubMed  PubMed Central  Google Scholar 

  92. Slabas AR, Ndimba B, Simon WJ, Chivasa S (2004) Proteomic analysis of the Arabidopsis cell wall reveals unexpected proteins with new cellular locations. Biochem Soc Trans 32:524–528

    CAS  PubMed  Google Scholar 

  93. Smith S, Boitz J, Chidambaram ES, Chatterjee A, AitTihyaty M, Ullman B, Jardim A (2016) The cystathionine-β-synthase domains on the guanosine 5″-monophosphate reductase and inosine 5′-monophosphate dehydrogenase enzymes from Leishmania regulate enzymatic activity in response to guanylate and adenylate nucleotide levels. Mol Microbiol 100:824–840

    CAS  PubMed  PubMed Central  Google Scholar 

  94. Sogin EM, Putnam HM, Nelson CE, Anderson P, Gates RD (2017) Correspondence of coral holobiont metabolome with symbiotic bacteria, archaea and Symbiodinium communities. Environ Microbiol Rep 9:310–315

    PubMed  Google Scholar 

  95. Spalding M, Burke L, Wood SA, Ashpole J, Hutchison J, Ermgassen P (2017) Mapping the global value and distribution of coral reef tourism. Mar Policy 82:104–113

    Google Scholar 

  96. Suzuki M, Van Paesschen W, Stalmans I, Horita S, Yamada H, Bergmans BA, Legius E, Riant F, De Jonghe P, Lia Y, Sekine T, Igarashi T, Fujimoto I, Mikoshiba K, Shimadzu M, Shiohara M, Braverman N, Al-Gazali L, Fujita T, Seki G (2010) Defective membrane expression of the Na+–HCO3 cotransporter NBCe1 is associated with familial migraine. Proc Natl Acad Sci 107:15963–15968

    CAS  PubMed  Google Scholar 

  97. Torchiano M (2018) Efficient effect size computation. R package version 0.7.4. https://github.com/mtorchiano/effsize/

  98. Ünal CM, Steinert M (2014) Microbial peptidyl-prolyl cis/trans isomerases (PPIases): virulence factors and potential alternative drug targets. Microbiol Mol Biol Rev 78:544–571

    PubMed  PubMed Central  Google Scholar 

  99. Vu V (2011) A ggplot2 based biplot. R package version 0.55. https://github.com/vqv/ggbiplot

  100. Wang W, Jeffery CJ (2016) An analysis of surface proteomics results reveals novel candidates for intracellular/surface moonlighting proteins in bacteria. Mol Biosyst 12:1420–1431

    CAS  PubMed  Google Scholar 

  101. Wang SB, Hu Q, Sommerfeld M, Chen F (2004a) Cell wall proteomics of the green alga Haematococcus pluvialis (Chlorophyceae). Proteomics 4:692–708

    CAS  PubMed  Google Scholar 

  102. Wang W, Vinocur B, Shoseyov O, Altman A (2004b) Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trends Plant Sci 9:244–252

    CAS  PubMed  Google Scholar 

  103. Wang R, Town T, Gokarn V, Flavell RA, Chandawarkar RY (2006) HSP70 enhances macrophage phagocytosis by interaction with lipid raft-associated TLR-7 and upregulating p38 MAPK and PI3K pathways. J Surg Res 36:58–69

    Google Scholar 

  104. Wang DZ, Dong HP, Li C, Xie ZX, Lin L, Hong HS (2011) Identification and characterization of cell wall proteins of a toxic dinoflagellate Alexandrium catenella using 2-D DIGE and MALDI TOF-TOF mass spectrometry. Evid Based Complement Alternat Med 2011:984080. https://doi.org/10.1155/2011/984080

    Article  PubMed  PubMed Central  Google Scholar 

  105. Wang Q, Liu J, Zhu H (2018) Genetic and molecular mechanisms underlying symbiotic specificity in legume–rhizobium interactions. Front Plant Sci 9:313

    PubMed  PubMed Central  Google Scholar 

  106. Warton DI, Wright ST, Wang Y (2012) Distance-based multivariate analyses confound location and dispersion effects. Methods Ecol Evol 3:89–101

    Google Scholar 

  107. Wasserstein RL, Lazar NA (2016) ASA statement on statistical significance and P values. Am Stat 70:129–133

    Google Scholar 

  108. Weis V (2008) Cellular mechanisms of Cnidarian bleaching: stress causes the collapse of symbiosis. J Exp Biol 211:3059–3066

    CAS  PubMed  Google Scholar 

  109. Weston AJ, Dunlap WC, Shick JM, Klueter A, Iglic K, Vukelic A, Starcevic A, Ward M, Wells ML, Trick CG, Long PF (2012) A profile of an endosymbiont-enriched fraction of the coral Stylophora pistillata reveals proteins relevant to microbial-host interactions. Mol Cell Proteomics 11(M111):015487. https://doi.org/10.1074/mcp.M111.015487

    CAS  Article  PubMed  Google Scholar 

  110. Wiersma VR, Michalak M, Abdullah TM, Bremer E, Eggleton P (2015) Mechanisms of translocation of ER chaperones to the cell surface and immunomodulatory roles in cancer and autoimmunity. Front Oncol 5:7. https://doi.org/10.3389/fonc.2015.00007

    Article  PubMed  PubMed Central  Google Scholar 

  111. Wilhelm M, Schlegl J, Hahne JH, Gholami AM, Lieberenz M, Savitski MM, Ziegler E, Butzmann L, Gessulat S, Marx H, Mathieson T, Lemeer S, Schnatbaum K, Reimer U, Wenschuh H, Mollenhauer M, Slotta-Huspenina J, Boese JH, Bantscheff M, Gerstmair A, Faerber F, Kuster B (2014) Mass-spectrometry-based draft of the human proteome. Nature 509:582–587

    CAS  PubMed  Google Scholar 

  112. Wood-Charlson E, Hollingworth L, Krupp D, Weis V (2006) Lectin/glycan interactions play a role in recognition in a coral/dinoflagellate symbiosis. Cell Microbiol 8:1985–1993

    CAS  PubMed  Google Scholar 

  113. Wrobel L, Topf U, Bragoszewski P, Wiese S, Sztolsztener ME, Oeljeklaus S, Varabyova A, Lirski M, Chroscicki P, Mroczek S, Januszewicz E, Dziembowski A, Koblowska M, Warscheid B, Chacinska A (2015) Mistargeted mitochondrial proteins activate a proteostatic response in the cytosol. Nature 524:485–488

    CAS  PubMed  Google Scholar 

  114. Yang SH, Liu R, Perez EJ, Wen Y, Stevens SM Jr, Valencia T, Brun-Zinkernagel AM, Prokai L, Will Y, Dykens J, Koulen P, Simpkins JW (2004) Mitochondrial localization of estrogen receptor beta. Proc Natl Acad Sci 101:4130–4135

    CAS  PubMed  Google Scholar 

  115. Yellowlees D, Dionisio-Sese ML, Masuda K, Maruyama T, Abe T, Baillie B, Tsuzuki M, Miyachi S (1993) Role of carbonic anhydrase in the supply of inorganic carbon to the giant clam—zooxanthellate symbiosis. Mar Biol 115:605–611

    CAS  Google Scholar 

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Acknowledgements

The authors would like to acknowledge funding from awards IOS-1831860 and OCE-1712134 from the National Science Foundation to LDM. This material is based on work supported by the LSAMP bridge to doctorate fellowship programs under Grant no.1026806 to CAR. We also acknowledge funding from the UT System Proteomics Core Facility Network for a mass spectrometer.

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Ricci, C.A., Kamal, A., Chakrabarty, J.K. et al. The cell-surface protein composition of a coral symbiont, Breviolum psygmophilum, reveals a mechanism for host specificity and displays dynamic regulation during temperature stress. Mar Biol 167, 66 (2020). https://doi.org/10.1007/s00227-020-03680-3

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