Changes in Microbial Communities Associated with the Sea Anemone Anemonia viridis in a Natural pH Gradient

Microbial Ecology

Volumn 65, Issue 2, 2013, Pages 269-276

  Meron, Dalit ^a   Buia, Maria Cristina ^b   Fine, Maoz ^a,c   Banin, Ehud ^a  

^a BAR ILAN UNIVERSITY   (Israel)

^b STAZIONE ZOOLOGICA ANTON DOHRN   (Italy)

^c The Interuniversity Institute for Marine Science Eilat   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

ACTINIARIA; ANEMONIA; ANEMONIA VIRIDIS; SYMBIODINIUM;

EID: 84873521993     PISSN: 00953628     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00248-012-0127-6     Document Type: Article

References (63)

1. Caldeira K, Wickett ME (2005) Ocean model predictions of chemistry changes from carbon dioxide emissions to the atmosphere and ocean. Geophys Res 110.
2. 2. Nature 407: 311-313.
3. 3 system in the oceans. Science 305: 362-366.
4. Petit JR, Jouzel J, Raynaud D, Barkov NI, Barnola JM, Basile I et al (1999) Climate and atmospheric history of the past 420, 000years from the Vostok ice core, Antarctica. Nature 399: 429-436.
5. IPCC (2007) Climate change 2007. www. ipcc. ch.
6. Bibby R, Cleall-Harding P, Rundle S, Widdicombe S, Spicer J (2007) Ocean acidification disrupts induced defences in the intertidal gastropod Littorina littorea. Biol Lett 3: 699-701.
7. Fabricius KE, Langdon C, Uthicke S, Humphrey C, Noonan S, De'ath G et al (2011) Losers and winners in coral reefs acclimatized to elevated carbon dioxide concentrations. Nat Clim Chang 1: 165-169.
8. Fine M, Tchernov D (2007) Scleractinian coral species survive and recover from decalcification. Science 315: 1811.
9. Ishimatsu A, Hayashi M, Lee K-S, Kikkawa T, Kita J (2005) Physiological effects on fishes in a high-CO2 world. J Geophys Res 110: C09S09.
10. Kuffner BI, Andersson JA, Jokiel LP, Rodgers SK, Mackenize TF (2007) Decreases abundance of crustose coralline algae due to ocean acidification. Nature 1: 114-117.
11. Martin S, Rodolfo-Metalpa R, Ransome E, Rowley S, Buia MC, Gattuso JP (2008) Effects of naturally acidified seawater on seagrass calcareous epibionts. Biol Lett 4: 689-692.
12. Orr JC, Fabry VJ, Aumont O, Bopp L, Doney SC, Feely RA et al (2005) Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature 437: 681-686.
13. Kroeker KJ, Kordas RL, Crim RN, Singh GG (2010) Meta-analysis reveals negative yet variable effects of ocean acidification on marine organisms. Ecol Lett 13: 1419-1434.
14. 2 problem. Annu Rev Mar Sci 1: 169-192.
15. 2 vents. Mar Biol 157: 2489-2502.
16. Hall-Spencer JM, Rodolfo-Metalpa R, Martin S, Ransome E, Fine M, Turner SM et al (2008) Volcanic carbon dioxide vents show ecosystem effects of ocean acidification. Nature 454: 96-99.
17. Ritchie KB (2006) Regulation of microbial population by coral surface mucus and mucus-associated bacteria. Mar Ecol Prog Ser 322: 1-14.
18. 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.
19. Sunagawa S, DeSantis TZ, Piceno YM, Brodie EL, DeSalvo MK, Voolstra CR et al (2009) Bacterial diversity and White Plague Disease-associated community changes in the Caribbean coral Montastraea faveolata. ISME J 3: 512-521.
20. Meron D, Rodolfo-Metalpa R, Cunning R, Baker AC, Fine M, Banin E (2012) Changes in coral microbial communities in response to a natural pH gradient. ISME J. doi: 0. 1038/ismej. 2012. 19.
21. Dowd SE, Wolcott RD, Sun Y, McKeehan T, Smith E, Rhoads D (2008) Polymicrobial nature of chronic diabetic foot ulcer biofilm infections determined using bacterial tag encoded FLX amplicon pyrosequencing (bTEFAP). PLoS One 3: e3326.
22. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB et al (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75: 7537-7541.
23. Meron D, Atias E, Iasur Kruh L, Elifantz H, Minz D, Fine M et al (2011) The impact of reduced pH on the microbial community of the coral Acropora eurystoma. ISME J 5: 51-60.
24. Shnit-Orland M, Kushmaro A (2009) Coral mucus-associated bacteria: a possible first line of defense. FEMS Microbiol Ecol 67: 371-380.
25. Ben-Haim Y, Thompson FL, Thompson CC, Cnockaert MC, Hoste B, Swings J et al (2003) Vibrio coralliilyticus sp. nov., a temperature-dependent pathogen of the coral Pocillopora damicornis. Int J Syst Evol Microbiol 53: 309-315.
26. Jeffrey S, Humphrey G (1975) New spectrophotometry equations for determining Chl a, b, c1, c2 in higher plants, algae and natural phytoplankton. Biochem Physiol Pflanzen 167: 191-194.
27. McGuire M, Szmant A (1997) Time course of physiological responses to NH4+ enrichment by a coral-zooxanthellae symbiosis. Proc 8th Int Coral Reef Symp Panama 1: 909-914.
28. Spotte S (1996) Supply of regenerated nitrogen to sea anemones by their symbiotic shrimp. J Exp Mar Biol Ecol 198: 27-36.
29. Stambler N, Dubinsky Z (1987) Energy relationships between Anemonia sulcata and its endosymbiotic zooxanthellae. Symbiosis 3: 233-248.
30. 2, pH and light. Mar Ecol Prog Ser 117: 159-172.
31. 2 partial pressure and temperature on photosynthesis and calcification in a scleractinian coral. Glob Chang Biol 9: 1660-1668.
32. 2-induced acidification on the intertidal sea anemone Anthopleura elegantissima (Cnidaria: Anthozoa) and its algal symbiont Symbiodinium muscatinei (Dinomastigota: Dinophyceae). Unpublished MSc Thesis, Evergreen State College, Washington, 42pp.
33. Dunn S, Thomason J, Le Tissier M, Bythell J (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.
34. Perez S, Cook C, Brooks W (2001) The role of symbiotic dinoflagellates in the temperature-induced bleaching response of the subtropical sea anemone Aiptasia pallida. J Exp Mar Biol Ecol 256: 1-14.
35. Kelman D, Kashman Y, Rosenberg E, Ilan M, Ifrach I, Loya Y (2001) Antimicrobial activity of the reef sponge Amphimedon viridis from the Red Sea: evidence for selective toxicity. Aquat Microb Ecol 24: 9-16.
36. Harder T, Lau S, Dobretsov S, Fang T, Qian P (2003) A distinctive epibiotic bacterial community on the soft coral Dendronephthya sp. and antibacterial activity of coral tissue extracts suggest a chemical mechanism against bacterial epibiosis. FEMS Microbiol Ecol 43: 337-347.
37. Kelman D, Kushmaro A, Loya Y, Kashman Y, Benayahu Y (1998) Antimicrobial activity of a Red Sea soft coral, Parerythropodium fulvum fulvum: reproductive and developmental considerations. Mar Ecol Prog Ser 169: 87-95.
38. Puglisi M, Paul V, Biggs J, Slattery M (2002) Co-occurrence of chemical and structural defenses in the gorgonian corals of Guam. Mar Ecol Prog Ser 239: 105-114.
39. Geffen Y, Rosenberg E (2005) Stress-induced rapid release of antibacterials by scleractinian corals. Mar Biol 146: 931-935.
40. Koh E (1997) Do scleractinian corals engage in chemical warfare against microbes? J Chem Ecol 23: 379-398.
41. Marquis C, Baird A, De Nys R, Holmstrom C, Koziumi N (2005) An evaluation of the antimicrobial properties of the eggs of 11 species of scleractinian corals. Coral Reefs 24: 248-253.
42. Williams G, Babu S, Ravikumar S, Kathiresan K, Prathap S, Chinnapparaj S et al (2007) Antimicrobial activity of tissue and associated bacteria from benthic sea anemone Stichodactyla haddoni against microbial pathogens. J Environ Biol 28: 789-793.
43. Nissimov J, Rosenberg E, Munn CB (2009) Antimicrobial properties of resident coral mucus bacteria of Oculina patagonica. FEMS Microbiol Lett 292: 210-215.
44. Bragadeeswaran S, Thangaraj S, Prabhu K, Sophia Rani S (2011) Antifouling activity by sea anemone (Heteractis magnifica and H. aurora) extracts against marine biofilm bacteria. Lat Am J Aquat Res 39: 385-389.
45. Thangaraj S, Bragadeeswaran S, Suganthi K, Kumaran NS (2011) Antimicrobial properties of sea anemone Stichodactyla mertensii and Stichodactyla gigantea from Mandapam coast of India. Asian Pac J Trop Biomed 1: S43-S46.
46. Legendre P, Gallagher E (2001) Ecologically meaningful transformations for ordination of species data. Oecologia 129: 271-280.
47. Feingersch R, Beja O (2009) Bias in assessments of marine SAR11 biodiversity in environmental fosmid and BAC libraries? ISME J 3: 1117-1119.
48. Agawin N, Agusti S (1997) Abundance, frequency of dividing cells and growth rates of Synechococcus sp. (cyanobacteria) in the stratified Northwest Mediterranean Sea. J Plankton Res 19: 1599-1615.
49. Agawin N, Carlos M, Susana A (1998) Growth and abundance of Synechococcus sp. in a Mediterranean Bay: seasonality and relationship with temperature. Mar Ecol Prog Ser 170: 45-53.
50. Mella-Flores D, Mazard S, Humily F, Partensky F, Mah'e F, Bariat L et al (2011) Is the distribution of Prochlorococcus and Synechococcus ecotypes in the Mediterranean Sea affected by global warming. Biogeosciences 8: 4281-4330.
51. Connell H (1978) Diversity in tropical rain forests and coral reefs. Science 199: 1302-1310.
52. Littman R, Bette L, Willis BL, Bourne DG (2011) Metagenomic analysis of the coral holobiont during a natural bleaching event on the Great Barrier Reef. Environ Microbiol Rep 3: 651-660.
53. Garren M, Raymundo L, Guest J, Harvell CD, Azam F (2009) Resilience of coral-associated bacterial communities exposed to fish farm effluent. PLoS One 4: e7319.
54. Vega-Thurber R, Willner-Hall D, Rodriguez-Mueller B, Desnues C, Edwards RA, Angly F et al (2009) Metagenomic analysis of stressed coral holobionts. Environ Microbiol 11: 2148-2163.
55. Du Z, Zhang W, Xia H, Lü G, Chen G (2010) Isolation and diversity analysis of heterotrophic bacteria associated with sea anemones. Acta Oceanol Sin 29: 62-69.
56. Palincsar E, Jones W, Palincsar J, Glogowski M, Mastro J (1989) Bacterial aggregates within the epidermis of the sea anemone Aiptasia pallida. Biol Bull 177: 130-140.
57. Xiao H, Chen Y, Liu Z, Huang K, Li W, Cui X et al (2009) Phylogenetic diversity of cultivable bacteria associated with a sea anemone from coast of the Naozhou island in Zhanjiang, China. Wei Sheng Wu Xue Bao 49: 246-250.
58. Schuett C, Doepke H, Grathoff A, Gedde M (2007) Bacterial aggregates in the tentacles of the sea anemone Metridium senilet. Helgol Mar Res 61: 211-216.
59. Al-Horani FA, Al-Moghrabi SM, de Beer D (2003) The mechanism of calcification and its relation to photosynthesis and respiration in the scleractinian coral Galaxea fascicularis. Mar Biol 142: 419-426.
60. Furla P, Bénazet-Tambutté S, Jaubert J, Allemand D (1998) Functional polarity of the tentacle of the sea anemone Anemonia viridis: role in inorganic carbon acquisition. Am J Physiol Regul Integr Comp Physiol 274: R303-R310.
61. Furla P, Galgani I, Durand I, Allemand D (2000) Sources and mechanisms of inorganic carbon transport for coral calcification and photosynthesis. J Exp Biol 203: 3445-3457.
62. Hoegh-Guldberg O (1999) Climate change, coral bleaching and the future of the world's coral reefs. Mar Freshw Res 50: 839-866.
63. Kitano H, Oda K (2006) Robustness trade-offs and host-microbial symbiosis in the immune system. Mol Syst Biol 2: 22. doi: 10. 1038/msb4100039.