Relative contributions of various cellular mechanisms to loss of algae during cnidarian bleaching

PLoS ONE

Volumn 11, Issue 4, 2016, Pages

  Bieri, Tamaki ^a,b   Onishi, Masayuki ^a   Xiang, Tingting ^c   Grossman, Arthur R ^b,c   Pringle, John R ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b STANFORD UNIVERSITY   (United States)

^c GEOPHYSICAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AIPTASIA; ALGA; BLEACHING; COLD STRESS; DEGRADATION; EXPOSURE; HOST CELL; HUMAN VERSUS ANIMAL COMPARISON; QUANTITATIVE STUDY; ANIMAL; CNIDARIA; ENVIRONMENT; GREEN ALGA; PHYSIOLOGICAL STRESS; PHYSIOLOGY; PIGMENTATION; SEA ANEMONE; SYMBIOSIS; TEMPERATURE;

ANIMALS; CHLOROPHYTA; CNIDARIA; ENVIRONMENT; PIGMENTATION; SEA ANEMONES; STRESS, PHYSIOLOGICAL; SYMBIOSIS; TEMPERATURE;

EID: 84974577278     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0152693     Document Type: Article

References (59)

1. National Oceanic and Athmospheric Administration (2011) Value of Coral Ecosystems. http://coralreef.noaa.gov/aboutcorals/values/.
2. Hoegh-Guldberg O, Mumby PJ, Hooten AJ, Steneck RS, Greenfield P, Gomez E, et al. (2007) Coral reefs under rapid climate change and ocean acidification. Science 318: 1737-1742. PMID: 18079392
3. Yellowlees D, Rees TA, Leggat W (2008) Metabolic interactions between algal symbionts and invertebrate hosts. Plant Cell Environ 31: 679-694. doi: 10.1111/j.1365-3040.2008.01802.x PMID: 18315536
4. Davy SK, Allemand D, Weis VM (2012) Cell biology of cnidarian-dinoflagellate symbiosis. Microbiol Mol Biol Rev 76: 229-261. doi: 10.1128/MMBR.05014-11 PMID: 22688813
5. Douglas AE (2003) Coral bleaching - how and why? Mar Pollut Bull 46: 385-392. PMID: 12705909
6. Weis VM (2008) Cellular mechanisms of Cnidarian bleaching: stress causes the collapse of symbiosis. J Exp Biol 211: 3059-3066. doi: 10.1242/jeb.009597 PMID: 18805804
7. Luzio JP, Pryor PR, Bright NA (2007) Lysosomes: fusion and function. Nat Rev Mol Cell Biol 8: 622-632. PMID: 17637737
8. Ohsumi Y (2014) Historical landmarks of autophagy research. Cell Res 24: 9-23. doi: 10.1038/cr.2013.169 PMID: 24366340
9. Parzych KR, Klionsky DJ (2014) An overview of autophagy: morphology, mechanism, and regulation. Antioxid Redox Signal 20: 460-473. doi: 10.1089/ars.2013.5371 PMID: 23725295
10. Ainsworth TD, Hoegh-Guldberg O (2008) Cellular processes of bleaching in the Mediterranean coral Oculina patagonica. Coral Reefs 27: 593-597.
11. Brown BE, Tissier MDA, Bythell JC (1995) Mechanisms of bleaching deduced from histological studies of reef corals sampled during a natural bleaching event. Mar Biol 122: 655-663.
12. Downs CA, Kramarsky-Winter E, Martinez J, Kushmaro A, Woodley CM, Loya Y, et al. (2009) Symbiophagy as a cellular mechanism for coral bleaching. Autophagy 5: 211-216. PMID: 19066451
13. Dunn SR, Bythell JC, Le Tissier MDA, Burnett WJ, Thomason JC (2002) Programmed cell death and cell necrosis activity during hyperthermic stress-induced bleaching of the symbiotic sea anemone Aiptasia sp. J Exp Mar Biol Ecol 272: 29-53.
14. Dunn SR, Thomason JC, Le Tissier MD, Bythell JC (2004) Heat stress induces different forms of cell death in sea anemones and their endosymbiotic algae depending on temperature and duration. Cell Death Differ 11: 1213-1222. PMID: 15286684
15. Franklin DJ, Hoegh-Guldberg O, Jones RJ, Berges JA (2004) Cell death and degeneration in the symbiotic dinoflagellates of the coral Stylophora pistillata during bleaching Mar Ecol Prog Ser 272: 117-130.
16. Strychar KB, Sammarco PW, Piva TJ (2004) Apoptotic and necrotic stages of Symbiodinium (Cinophyceae) cell death activity: bleaching of soft and scleractinian corals. Phycologia 43: 768-777.
17. Le Tissier MD, Brown BE (1996) Dynamics of solar bleaching in the intertidal reef coral Goniastrea aspera at KO Phuket, Thailand. Mar Ecol Prog Ser 136: 235-244.
18. Muscatine L, Grossman D, Doino J (1991) Release of symbiotic algae by tropical sea anemones and corals after cold shock. Mar Ecol Prog Ser 77: 233-243.
19. Strychar KB, Coates M, Sammarco PW (2004) Loss of Symbiodinium from bleached Australian scleractinian corals (Acropora hyacinthus, Favites complanata and Porites solida). Mar Freshwater Res 55: 135-144.
20. Steele RD (1976) Light intensity as a factor in the regulation of the density of symbiotic zooxanthellae in Aiptasia tagetes (Coelenterats, Anthozoa). J Zool 179: 387-405.
21. Hanes SD, Kempf SC (2013) Host autophagic degradation and associated symbiont loss in response to heat stress in the symbiotic anemone, Aiptasia pallida. Invertebr Biol 132: 95-107.
22. Fujise L, Yamashita H, Suzuki G, Koike K (2013) Expulsion of zooxanthellae (Symbiodinium) from several species of scleractinian corals: comparison under non-stress conditions and thermal stress conditions. Galaxea 15: 29-36.
23. Steen RG, Muscatine L (1987) Low temperature evokes rapid exocytosis of symbiotic algae by sea anemone. Biol Bull 172: 246-263.
24. Gates RD, Baghdasarian G, Muscatine L (1992) Temperature stress causes host cell detachment in symbiotic cnidarians: implications for coral bleaching. Biol Bull 182: 324-332.
25. Sawyer SJ, Muscatine L (2001) Cellular mechanisms underlying temperature-induced bleaching in the tropical sea anemone Aiptasia pulchella. J Exp Biol 204: 3443-3456. PMID: 11707495
26. Dunn SR, Schnitzler CE, Weis VM (2007) Apoptosis and autophagy as mechanisms of dinoflagellate symbiont release during cnidarian bleaching: every which way you lose. Proc R Soc Lond B 274: 3079-3085.
27. Glynn PW, Peters EC, Muscatine L (1985) Coral tissue microstructure and necrosis: relation to catastrophic coral mortality in Panama. Dis Aquat Org 1: 29-37.
28. Hawkins TD, Bradley BJ, Davy SK (2013) Nitric oxide mediates coral bleaching through an apoptoticlike cell death pathway: evidence from a model sea anemone-dinoflagellate symbiosis. FASEB J 27: 4790-4798. doi: 10.1096/fj.13-235051 PMID: 23934282
29. Kvitt H, Rosenfeld H, Zandbank K, Tchernov D (2011) Regulation of apoptotic pathways by Stylophora pistillata (Anthozoa, Pocilloporidae) to survive thermal stress and bleaching. PLoS ONE 6: e28665. doi: 10.1371/journal.pone.0028665 PMID: 22194880
30. Pernice M, Dunn SR, Miard T, Dufour S, Dove S, Hoegh-Guldberg O (2011) Regulation of apoptotic mediators reveals dynamic responses to thermal stress in the reef building coral Acropora millepora. PLoS ONE 6: e16095. doi: 10.1371/journal.pone.0016095 PMID: 21283671
31. Tchernov D, Kvitt H, Haramaty L, Bibby TS, Gorbunov MY, Rosenfeld H, et al. (2011) Apoptosis and the selective survival of host animals following thermal bleaching in zooxanthellate corals. Proc Natl Acad Sci USA 108: 9905-9909. doi: 10.1073/pnas.1106924108 PMID: 21636790
32. Richier S, Sabourault C, Courtiade J, Zucchini N, Allemand D, Furla P (2006) Oxidative stress and apoptotic events during thermal stress in the symbiotic sea anemone, Anemonia viridis. FEBS J 273: 4186-4198. PMID: 16907933
33. Dunn SR, Pernice M, Green K, Hoegh-Guldberg O, Dove SG (2012) Thermal stress promotes host mitochondrial degradation in symbiotic cnidarians: Are the batteries of the reef going to run out? PLoS ONE 7: e39024. doi: 10.1371/journal.pone.0039024 PMID: 22815696
34. Paxton CW, Davy SK, Weis VM (2013) Stress and death of cnidarian host cells play a role in cnidarian bleaching. J Exp Biol 216: 2813-2820. doi: 10.1242/jeb.087858 PMID: 23619418
35. Burriesci MS, Raab TK, Pringle JR (2012) Evidence that glucose is the major transferred metabolite in dinoflagellate-cnidarian symbiosis. J Exp Biol 215: 3467-3477. doi: 10.1242/jeb.070946 PMID: 22956249
36. Lehnert EM, Mouchka ME, Burriesci MS, Gallo ND, Schwarz JA, Pringle JR (2014) Extensive differences in gene expression between symbiotic and aposymbiotic cnidarians. G3 4: 277-295. doi: 10.1534/g3.113.009084 PMID: 24368779
37. Leal MC, Hoadley K, Pettay DT, Grajales A, Calado R, Warner ME (2015) Symbiont type influences trophic plasticity of a model cnidarian-dinoflagellate symbiosis. J Exp Biol 218: 858-863. doi: 10.1242/jeb.115519 PMID: 25617454
38. Tolleter D, Seneca FO, DeNofrio JC, Krediet CJ, Palumbi SR, Pringle JR, et al. (2013) Coral bleaching independent of photosynthetic activity. Curr Biol 23: 1782-1786. doi: 10.1016/j.cub.2013.07.041 PMID: 24012312
39. Weis VM, Davy SK, Hoegh-Guldberg O, Rodriguez-Lanetty M, Pringle JR (2008) Cell biology in model systems as the key to understanding corals. Trends Ecol Evol 23: 369-376. doi: 10.1016/j.tree.2008.03.004 PMID: 18501991
40. Voolstra CR (2013) A journey into the wild of the cnidarian model system Aiptasia and its symbionts. Mol Ecol 22: 4366-4368. PMID: 24137737
41. Baumgarten S, Simakov O, Esherick LY, Liew YJ, Lehnert EM, Michell CT, et al. (2015) The genome of Aiptasia, a sea anemone model for coral symbiosis. Proc Natl Acad Sci USA doi: 10.1073/PNAS.1513318112
42. Hambleton EA, Guse A, Pringle JR (2014) Similar specificities of symbiont uptake by adults and larvae in an anemone model system for coral biology. J Exp Biol 217: 1613-1619. doi: 10.1242/jeb.095679 PMID: 24526722
43. 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. doi: 10.1186/1471-2164-13-271 PMID: 22726260
44. Schoenberg DA, Trench RK (1980) Genetic variation in Symbiodinium (= Gymnodinium) microadriaticum Freudenthal, and specificity in its symbiosis with marine invertebrates. III. Specificity and infectivity of Symbiodinium microadriaticum. Proc R Soc Lond B 207: 445-460.
45. Sunagawa S, Wilson EC, Thaler M, Smith ML, Caruso C, Pringle JR, et al. (2009) Generation and analysis of transcriptomic resources for a model system on the rise: the sea anemone Aiptasia pallida and its dinoflagellate endosymbiont. BMC Genomics 10: 258. doi: 10.1186/1471-2164-10-258 PMID: 19500365
46. Xiang T, Hambleton EA, DeNofrio JC, Pringle JR, Grossman AR (2013) Isolation of clonal axenic strains of the symbiotic dinoflagellate Symbiodinium and their growth and host specificity. J Phycol 49: 447-458. doi: 10.1111/jpy.12055 PMID: 27007034
47. Pochon X, Putnam HM, Gates RD (2014) Multi-gene analysis of Symbiodinium dinoflagellates: a perspective on rarity, symbiosis, and evolution. PeerJ 2: e394. doi: 10.7717/peerj.394 PMID: 24883254
48. 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: 1380-1391. doi: 10.1111/j.1529-8817.2012.01217.x PMID: 27008273
49. Garcia-Calvo M, Peterson EP, Leiting B, Ruel R, Nicholson DW, Thornberry NA (1998) Inhibition of human caspases by peptide-based and macromolecular inhibitors. J Biol Chem 273: 32608-32613. PMID: 9829999
50. Poreba M, Strozyk A, Salvesen GS, Drag M (2013) Caspase substrates and inhibitors. Cold Spring Harb Perspect Biol 5: a008680. doi: 10.1101/cshperspect.a008680 PMID: 23788633
51. Krediet CJ, DeNofrio JC, Caruso C, Burriesci MS, Cella K, Pringle JR (2015) Rapid, precise, and accurate counts of Symbiodinium cells using the Guava flow cytometer, and a comparison to other methods. PLoS ONE 10: e0135725. doi: 10.1371/journal.pone.0135725 PMID: 26291447
52. Xiang T, Nelson W, Rodriguez J, Tolleter D, Grossman AR (2015) Symbiodinium transcriptome and global responses of cells to immediate changes in light intensity when grown under autotrophic or mixotrophic conditions. Plant J 82: 67-80. doi: 10.1111/tpj.12789 PMID: 25664570
53. McIlwain DR, Berger T, Mak TW (2013) Caspase functions in cell death and disease. Cold Spring Harb Perspect Biol 5: a008656. doi: 10.1101/cshperspect.a008656 PMID: 23545416
54. Titlyanov EA, Titlyanova TV, Leletkin VA, Tsukahara J, van Woesik R, Yamazato K (1996) Degradation of zooxanthellae and regulation of their density in hermatypic corals. Mar Ecol Prog Ser 139: 167-178.
55. Fuentes-Prior P, Salvesen GS (2004) The protein structures that shape caspase activity, specificity, activation and inhibition. Biochem J 384: 201-232. PMID: 15450003
56. Dykens JA, Shick JM, Benoit C, Buettner GR, Winston GW (1992) Oxygen radical production in the sea anemone Anthopleura elegantissima and its endosymbiotic algae. J Exp Biol 168: 219-241.
57. Nii CM, Muscatine L (1997) Oxidative stress in the symbiotic sea anemone Aiptasia pulchella (Carlgren, 1943): Contribution of the animal to superoxide ion production at elevated temperature. Biol Bull 192: 444-456.
58. Hoegh-Guldberg O, McCloskey LR, Muscatine L (1986) Expulsion of zooxanthellae by symbiotic cnidarians from the Red Sea. Coral Reefs 5: 201-204.
59. Dunn SR, Phillips WS, Spatafora JW, Green DR, Weis VM (2006) Highly conserved caspase and Bcl-2 homologues from the sea anemone Aiptasia pallida: lower metazoans as models for the study of apoptosis evolution. J Mol Evol 63: 95-107. PMID: 16770683