Advertisement

An Integrated Model of the Biology of the Marine Symbiosis Maristentor dinoferus

  • Christopher S. Lobban
  • María Schefter
Chapter

Abstract

Maristentor dinoferus (Heterotrichida: Maristentoridae) is a symbiosis comprising a very large ciliate with hundreds of endosymbiotic zooxanthellae (Symbiodinium sp.). Its large size, large amounts of pigment that make it appear black, tendency to cluster, and preferred substratum of the light-colored blades of the seaweed Padina make it visible to the naked eye and observable in the field. Here we review the knowledge of Maristentor behavior and ecology through the lens of biocommunication theory and use analogies with other organisms to develop an integrated framework of understanding as a basis for future experimental and observational research. We are particularly interested in the roles and integration of the three most outstanding features of this symbiosis: the zooxanthellae, the densely pigmented cortical granules, and the complex clustering/dispersal behavior of the cells.

Keywords

Crustose Coralline Alga Pigment Granule Cortical Granule Oral Apparatus Motor Home 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgements

Many people have contributed to discussions of Maristentor over two decades. Here we wish to thank G. Curt Fiedler for reviewing a draft manuscript and Toshiyuki Nakajima for sharing a draft of his chapter for this book.

References

  1. Ame JM, Halloy J, Rivault C, Detrain C, Deneubourg JL (2006) Collegial decision making based on social amplification leads to optimal group formation. Proc Natl Acad Sci USA 103:5835–5840CrossRefPubMedPubMedCentralGoogle Scholar
  2. Buonanno F, Saltalamacchia P, Miyake A (2005) Defence function of pigmentocysts in the karyorelictid ciliate Loxodes striatus. Eur J Protistol 41:151–158CrossRefGoogle Scholar
  3. Buonanno F, Anesi A, Guella G, Kumar S, Bharti D, La Terza A, Quassinti L, Bramucci M, Ortenzi C (2014) Chemical offense by means of toxicysts in the freshwater ciliate, Coleps hirtus. J Eukaryot Microbiol 61:293–304CrossRefPubMedGoogle Scholar
  4. Camazine S, Deneubourg J-L, Franks NR, Sneyd J, Theraulaz G, Bonaneau E (2001) Self-organization in biological systems. Princeton University Press, PrincetonGoogle Scholar
  5. Chen S-T, Li C-W (1991) Relationships between the movements of chloroplasts and cytoskeletons in diatoms. Bot Mar 34:505–511CrossRefGoogle Scholar
  6. Demoulin G (1962) Comportement des chenilles de Thaumetopoea pityocampa Schiff. au cours des processions de nymphose. Comptes Rendues de l’Academie des Sciences de Paris 254:733–734Google Scholar
  7. Deneubourg J-L, Grégoire J-C, Le Fort E (1990) Kinetics of larval gregarious behavior in the bark beetle Dendroctonus micans (Coleoptera: Scolytidae). J Insect Behav 3:169–182CrossRefGoogle Scholar
  8. Dziallas C, Allgaier M, Monaghan MT, Grossart H-P (2012) Act together—implications of symbioses in aquatic ciliates. Frontiers Microbiol 3(288):17Google Scholar
  9. Emmeche C (2002) Taking the semiotic turn, or how significant philosophy of biology should be done. Nord J Philos 3:155–162Google Scholar
  10. Fenchel T, Blackburn N (1999) Motile chemosensory behaviour of phagotrophic protists: mechanisms for and efficiency in congregating at food patches. Protist 150:325–336CrossRefPubMedGoogle Scholar
  11. Fitt WK (1985) Chemosensory responses of the symbiotic dinoflagellates Symbiodinium microadriaticum (Dinophyceae). J Phycol 21:62–67CrossRefGoogle Scholar
  12. Fitt WK, Trench RK (1983) The relation of diel patterns of cell division to diel pattern of motility in the symbiotic dinoflagellate Symbiodinium microadriaticum Freudenthal in culture. New Phytol 94:421–432CrossRefGoogle Scholar
  13. Foissner W (1996) Ontogenesis in ciliated protozoa with emphasis on stomatogenesis. In: Hausmann K, Bradbury PC (eds) Ciliates. Cells as organisms. Gustav Fischer Verlag, Stuttgart, pp 95–177Google Scholar
  14. Foissner W (2006) Biogeography and dispersal of micro-organisms: a review emphasizing protists. Acta Protozoologica 45:111–136Google Scholar
  15. Germond A, Nakajima T (this volume) Symbiotic associations in ciliates: ecological and evolutionary perspectives. In: Witzany G, Nowacki M (eds) Biocommunication of ciliates. SpringerGoogle Scholar
  16. Gilbert SF (2013) Developmental Biology, 10th edn. Sinauer, Sunderland, USA 719 ppGoogle Scholar
  17. Greenberg PE (2003) Bacterial communication: tiny teamwork. Nature 424:134Google Scholar
  18. Hansen G, Daugbjerg N (2009) Symbiodinium natans sp. nov.: a ‘‘free-living’’ dinoflagellate from Tenerife (Northeast-Atlantic Ocean). J Phycol 21:251–263CrossRefGoogle Scholar
  19. Hartmann C, Özmutlu Ö, Petermeier H, Fried J, Delgado A (2007) Analysis of the flow field induced by the sessile peritrichous ciliate Opercularia asymmetrica. J Biomech 40:137–148Google Scholar
  20. Heyward AJ, Negri AP (1999) Natural inducers for coral larval metamorphosis. Coral Reefs 18:273–279CrossRefGoogle Scholar
  21. Hollingsworth LL, Kinzie RA III, Lewis TD, Krupp DA, Leong JAC (2005) Phototaxis of motile zooxanthellae to green light may facilitate symbiont capture by coral larvae. Coral Reefs 24:523CrossRefGoogle Scholar
  22. Hori M, Tomikawa I, Przybos E, Fuishima M (2006) Comparison of the evolutionary distances among syngens and sibling species of Paramecium. Mol Phylogenet Evol 38:697–704CrossRefPubMedGoogle Scholar
  23. Hurd CL, Harrison PJ, Bischof K, Lobban CS (2014) Seaweed ecology and physiology, 2nd edn. Cambridge University Press, Cambridge 562 ppCrossRefGoogle Scholar
  24. Jones R, Yellowlees D (1997) Regulation and control of intracellular algae (=zooxanthellae) in hard corals. Philos Trans R Soc Lond B 352:457–468CrossRefGoogle Scholar
  25. Kiørboe T, Visser AW (1999) Predator and prey perception in copepods due to hydromechanical signals. Mar Ecol Prog Ser 179:81–95CrossRefGoogle Scholar
  26. LaJeunesse TC, Parkinson JE, Reimer JD (2012) A genetics-based description of Symbiodinium minutum sp. nov. and S. psygmophilum sp. Nov. (Dinophyceae), two dinoflagellates symbiotic with cnidaria. J Phycol 48:1380–1391CrossRefPubMedGoogle Scholar
  27. Lenci F, Ghetti F, Song P-S (2001) Photomovement in ciliates. In: Häder D-P, Lebert M (eds) Photomovement. Elsevier Science B.V, Amsterdam, The Netherlands, pp 475–503CrossRefGoogle Scholar
  28. Lobban CS (2015) A second species of Microtabella (Grammatophoraceae, Bacillariophyta) from Guam. Mar Biodivers Rec 8:e151, 5 ppGoogle Scholar
  29. Lobban CS, Schefter M (1996) An abundance of marine Stentor (Ciliophora: Spirotrichea) epiphytic on Padina (Phaeophyta). Micronesica 29:99–100Google Scholar
  30. Lobban CS, Schefter M (2012) Blooms of a benthic ciliate, Maristentor dinoferus (Heterotrichida: Maristentoridae), on coral reefs of Guam, Mariana Islands. Micronesica 43:114–127Google Scholar
  31. Lobban CS, Schefter M, Simpson AGB, Pochon X, Pawlowski J, Foissner W (2002) Maristentor dinoferus n. gen., n. sp., a giant heterotrich ciliate (Spirotrichea: Heterotrichida) with zooxanthellae, from coral reefs on Guam, Mariana Islands. Mar Biol 140:411–423+141: 207–208Google Scholar
  32. Lobban CS, Modeo L, Verni F, Rosati G (2005) Euplotes uncinatus (Ciliophora, Hypotrichia), a new species with zooxanthellae. Mar Biol 147:1055–1061CrossRefGoogle Scholar
  33. Lobban CS, Hallam SJ, Mukherjee P, Petrich JW (2007) Photophysics and multifunctionality of hypericin-like pigments in heterotrich ciliates: a phylogenetic perspective. Photochem Photobiol 83:1074–1094CrossRefPubMedGoogle Scholar
  34. Lobban CS, Schefter M, Donaldson TJ (2014) Cluster dynamics in Maristentor dinoferus, a gregarious benthic ciliate with zooxanthellae and a hypericin-like pigment, in relation to biofilm grazing by the fish Ctenochaetus striatus. Symbiosis 63:137–147CrossRefGoogle Scholar
  35. Lynn DH (2008) The Ciliated Protozoa. Characterization, classification, and guide to the literature. 3rd edn. Springer, New York, 605 ppGoogle Scholar
  36. Madl P, Witzany G (2014) How corals coordinate and organize: an ecosystemic analysis based on biocommunication and fractal properties. In: Witzany G (ed) Biocommunication of animals, Springer Science+Business Media, Dordrecht, Germany, pp 351–382Google Scholar
  37. Mansfield M, Turner SL (2002) Quorum sensing in context: out of molecular biology and into microbial ecology. Microbiology 148:3762–3764Google Scholar
  38. Mayr E (1982) The Growth of Biological Thought: diversity, evolution and inheritance. Belknap Press, Cambridge 974 ppGoogle Scholar
  39. McManus GB, Schoener DM, Haberlandt K (2012) Chloroplast symbionts in a marine ciliate: ecophysiology and the risks and rewards of hosting foreign organelles. Frontiers Microbiol 3:321. doi: 10.3389/fmicb.2012.00321
  40. Miao W, Simpson AGB, Fu C, Lobban CS (2005) The giant zooxanthellae-bearing ciliate Maristentor dinoferus is closely related to Folliculinidae. J Eukaryot Microbiol 52:11–16CrossRefPubMedGoogle Scholar
  41. Miyake A, Harumoto, Iio H (2001) Defense function of pigment granules in Stentor coeruleus. Eur J Protistol 37:77–88CrossRefGoogle Scholar
  42. Miyake AF, Buonanno P, Saltalamacchia P, Masaki ME, Iio H (2003) Chemical defense by means of extrusive cortical granules in the heterotrich ciliate Climacostomum virens. Eur J Protistol 39:25–36Google Scholar
  43. Mordret S, Romac S, Henry N, Colin S, Carmichael M, Berney C, Audic S, Richter DJ, Pochon X, de Vargas C, Decelle J (2015) The symbiotic life of Symbiodinium in the open ocean within a new species of calcifying ciliate (Tiarina sp). ISME J (in press)Google Scholar
  44. Mukherjee P, Fulton DB, Halder M, Han X, Armstrong DW, Petrich J, Lobban CS (2006) Maristentorin, a novel pigment from the positively phototactic marine ciliate Maristentor dinoferus, is structurally related to hypericin and stentorin. J Phys Chem B 110:6359–6364CrossRefPubMedGoogle Scholar
  45. Mulisch M, Patterson DJ (1988) Stomatogenesis during cell division in the loricate ciliate Eufolliculina uhligi: a scanning electron microscope study. Eur J Protistol 23:193–201CrossRefPubMedGoogle Scholar
  46. Negri AP, Webster NS, Hill RT, Heyward AJ (2001) Metamorphosis of broadcast spawning corals in response to bacteria isolated from crustose algae. Mar Ecol Prog Ser 223:121–131CrossRefGoogle Scholar
  47. Nowack ECM, Melkonian M (2010) Endosymbiotic associations within protists. Philos Trans R Soc Lond B Biol Sci 365:699–712CrossRefPubMedPubMedCentralGoogle Scholar
  48. Parkinson JE, Coffroth MA, LaJeunesse TC (2015) New species of Clade B Symbiodinium (Dinophyceae) from the greater Caribbean belong to different functional guilds: S. aenigmaticum sp. nov., S. antillogorgium sp. nov., S. endomadracis sp. nov., and S. pseudominutum sp. nov. J Phycol 51:850–858CrossRefPubMedGoogle Scholar
  49. Pochon X, Putnam HM, Gates RD (2014) Multi-gene analysis of Symbiodinium dinoflagellates: a perspective on rarity, symbiosis, and evolution. PeerJ 2:e394. https://dx.doi.org/10.7717/peerj.394
  50. Podestà A, Marangoni R, Villani C, Colombetti G (1994) A rhodopsin-like molecule on the plasma membrane of Fabrea salina. J Eukaryot Microbiol 41:565–569CrossRefGoogle Scholar
  51. Schlichter D, Meier U, Fricke HW (1994) Improvement of photosynthesis in zooxanthellate corals by autofluorescent chromatophores. Oecologia 99:124–131CrossRefGoogle Scholar
  52. Sobierajska K, Fabczak H, Fabczak S (2006) Photosensory transduction in unicellular eukaryotes: a comparison between related ciliates Blepharisma japonicum and Stentor coeruleus and photoreceptor cells of higher organisms. J Photochem Photobiol B Biol 83:163–171CrossRefGoogle Scholar
  53. Sommaruga R, Whitehead K, Shick JM, Lobban CS (2006) Mycosporine-like amino acids in the zooxanthella-ciliate symbiosis Maristentor dinoferus. Protist 157:185–191CrossRefPubMedGoogle Scholar
  54. Song P-S, Kim I-H, Rhee JS, Huh J, Florell S, Faure B, Lee KW, Kahsai T, Tamai N, Yamazaki T, Yamazaki I (1991) Photoreception and photomovements in Stentor coeruleus. In: Lenci F, Ghetti F, Colombett G, Häder D-P, Song P-S (eds) Biophysics of photoreceptors and photomovements in microorganisms. Plenum Press, New York, pp 267–279CrossRefGoogle Scholar
  55. Stanley GD, Swart PK (1995) Evolution of the coral-zooxanthella symbiosis during the Triassic: a geochemical approach. Paleobiology 21:179–199Google Scholar
  56. Stat M, Carter D, Hoegh-Guldberg O (2006) The evolutionary history of Symbiodinium and scleractinian hosts—symbiosis, diversity, and the effect of climate change. Perspect Plant Ecol Evol Syst 8:23–43CrossRefGoogle Scholar
  57. Stoecker DK, Silver MW, Michaels AE, Davis LH (1988) Enslavement of algal chloroplasts by four Strombidium spp (Ciliophora, Oligotrichida). Mar Microb Food Webs 3:79–100Google Scholar
  58. Stoecker DK, Johnson MD, de Vargas C, Not F (2009) Acquired phototrophy in aquatic protists. Aquat Microb Ecol 57:279–310CrossRefGoogle Scholar
  59. Summerer M, Sonntag B, Sommaruga R (2007) An experimental test of the symbiosis specificity between the ciliate Paramecium bursaria and strains of the unicellular green alga Chlorella. Environ Microbiol 9:2117–2122CrossRefPubMedGoogle Scholar
  60. Summerer M, Sonntag B, Sommaruga R (2008) Ciliate-symbiont specificity of freshwater endosymbiotic Chlorella (Trebouxiophyceae, Chlorophyta). J Phycol 44:77–84CrossRefPubMedGoogle Scholar
  61. Sumpter DJT, Pratt SC (2009) Quorum responses and consensus decision making. Philos Trans R Soc B 364:743–753CrossRefGoogle Scholar
  62. Titlyanov EA, Titlyanova TV, Leletkin VA, Tsukahara J, van Woesik R, Yamazato K (1996) Degradation of zooxanthellae and regulation of their density in hermatyopic corals. Mar Ecol Prog Ser 139:167–178CrossRefGoogle Scholar
  63. Visser AW (2001) Hydromechanical signals in the plankton. Mar Ecol Prog Ser 222:1–24CrossRefGoogle Scholar
  64. Wahl M (2008) Ecological lever and interface ecology: epibiosis modulates the interface between host and environment. Biofouling 24:427–438CrossRefPubMedGoogle Scholar
  65. Ward AJW, Sumpter DJT, Couzin ID, Hart PJB, Krause J (2008) Quorum decision-making facilitates information transfer in fish shoals. Proc Natl Acad Sci USA 105:6948–6953CrossRefPubMedPubMedCentralGoogle Scholar
  66. Wilkerson FP, Grunseich G (1990) Formation of blooms by the symbiotic ciliate Mesodinium rubrum: the significance of nitrogen uptake. J Plankton Res 12:973–989CrossRefGoogle Scholar
  67. Witzany G (2008) Biocommunication of unicellular and multicellular organisms. The biosemiotic categorization of rule-governed sign-mediated interactions within and between bacteria, fungi and plants. TripleC (Cognition, Communication, Co-operation) 6:24–53Google Scholar
  68. Wölfl S, Geller W (2002) Chlorella-bearing ciliates dominate in an oligotrophic North Patagonian lake (Lake Pirehueico, Chile): abundance, biomass and symbiotic photosynthesis. Freshw Biol 47:231–242CrossRefGoogle Scholar
  69. Wood DC (1989) Localization of mechanoreceptors in the protozoan, Stentor coeruleus. J Comp Physiol A 165:229–235CrossRefPubMedGoogle Scholar
  70. Wood DC (2001) Electrophysiology and light responses in Stentor and Blepharisma. In: Häder D-P, Lebert M (eds) Photomovement. Elsevier Science BV, Amsterdam, pp 505–518CrossRefGoogle Scholar
  71. Wood-Charlson EM, Hollingsworth LL, Krupp DA, Weis VM (2006) Lectin/glycan interactions play a role in recognition in a coral/dinoflagellate symbiosis. Cell Microbiol 8:1985–1993CrossRefPubMedGoogle Scholar
  72. Yamashita H, Kobiyama A, Koike K (2009) Do uric acid deposits in zooxanthellae function as eye-spots? PLoS One 4(7):e6303. doi: 10.1371/journal.pone.0006303 CrossRefPubMedPubMedCentralGoogle Scholar
  73. Yamashita H, Suzuki G, Kai S, Hayashibara T, Koike K (2014) Establishment of coral–algal symbiosis requires attraction and selection. PLoS One 9(5):e97003. doi: 10.1371/journal.pone.0097003 CrossRefPubMedPubMedCentralGoogle Scholar
  74. Zagata P, Greczek-Stachura M, Tarcz S, Rautian M (2015) Molecular identification of Paramecium bursaria syngens and studies on geographic distribution using mitochondrial cytochrome c oxidase subunit I (COI). Folia Biol (Krakow) 63:77–83CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  1. 1.Division of Natural SciencesUniversity of GuamMangilaoUSA
  2. 2.UOG StationMangilaoUSA

Personalised recommendations