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

Abstract

Ocean acidification, resulting from rising atmospheric carbon dioxide concentrations, is a pervasive stressor that can affect many marine organisms and their symbionts. Studies which examine the host physiology and microbial communities have shown a variety of responses to the ocean acidification process. Recently, several studies were conducted based on field experiments, which take place in natural CO2 vents, exposing the host to natural environmental conditions of varying pH. This study examines the sea anemone Anemonia viridis which is found naturally along the pH gradient in Ischia, Italy, with an aim to characterize whether exposure to pH impacts the holobiont. The physiological parameters of A. viridis (Symbiodinium density, protein, and chlorophyll a+c concentration) and its microbial community were monitored. Although reduction in pH was seen to have had an impact on composition and diversity of associated microbial communities, no significant changes were observed in A. viridis physiology, and no microbial stress indicators (i.e., pathogens, antibacterial activity, etc.) were detected. In light of these results, it appears that elevated CO2 does not have a negative influence on A. viridis that live naturally in the site. This suggests that natural long-term exposure and dynamic diverse microbial communities may contribute to the acclimation process of the host in a changing pH environment.

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

Figure 1
Figure 2
Figure 3
Figure 4

References

  1. 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.

    Gattuso J-P, Buddemeier RW (2000) Ocean biogeochemistry: calcification and CO2. Nature 407:311–313

    PubMed  Article  CAS  Google Scholar 

  3. 3.

    Feely RA, Sabine CL, Lee K, Berelson W, Kleypas J, Fabry VJ, Millero FJ (2004) Impact of anthropogenic CO2 on the CaCO3 system in the oceans. Science 305:362–366

    PubMed  Article  CAS  Google Scholar 

  4. 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

    Article  CAS  Google Scholar 

  5. 5.

    IPCC (2007) Climate change 2007. www.ipcc.ch.

  6. 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

    PubMed  Article  Google Scholar 

  7. 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

    Article  CAS  Google Scholar 

  8. 8.

    Fine M, Tchernov D (2007) Scleractinian coral species survive and recover from decalcification. Science 315:1811

    PubMed  Article  CAS  Google Scholar 

  9. 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

    Article  Google Scholar 

  10. 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

    Google Scholar 

  11. 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

    PubMed  Article  Google Scholar 

  12. 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

    PubMed  Article  CAS  Google Scholar 

  13. 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

    PubMed  Article  Google Scholar 

  14. 14.

    Doney S, Fabry V, Feely R, Kleypas J (2009) Ocean acidification: the other CO2 problem. Annu Rev Mar Sci 1:169–192

    Article  Google Scholar 

  15. 15.

    Cigliano M, Gambi M, Rodolfo-Metalpa R, Patti F, Hall-Spencer J (2010) Effects of ocean acidification on invertebrate settlement at volcanic CO2 vents. Mar Biol 157:2489–2502

    Article  Google Scholar 

  16. 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

    PubMed  Article  CAS  Google Scholar 

  17. 17.

    Ritchie KB (2006) Regulation of microbial population by coral surface mucus and mucus-associated bacteria. Mar Ecol Prog Ser 322:1–14

    Article  CAS  Google Scholar 

  18. 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

    PubMed  Article  CAS  Google Scholar 

  19. 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

    PubMed  Article  CAS  Google Scholar 

  20. 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. 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

    PubMed  Article  Google Scholar 

  22. 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

    PubMed  Article  CAS  Google Scholar 

  23. 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

    PubMed  Article  Google Scholar 

  24. 24.

    Shnit-Orland M, Kushmaro A (2009) Coral mucus-associated bacteria: a possible first line of defense. FEMS Microbiol Ecol 67:371–380

    PubMed  Article  CAS  Google Scholar 

  25. 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

    PubMed  Article  CAS  Google Scholar 

  26. 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

    CAS  Google Scholar 

  27. 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

    CAS  Google Scholar 

  28. 28.

    Spotte S (1996) Supply of regenerated nitrogen to sea anemones by their symbiotic shrimp. J Exp Mar Biol Ecol 198:27–36

    Article  Google Scholar 

  29. 29.

    Stambler N, Dubinsky Z (1987) Energy relationships between Anemonia sulcata and its endosymbiotic zooxanthellae. Symbiosis 3:233–248

    Google Scholar 

  30. 30.

    Kuhl M, Cohen Y, Dalsgaard T, Jorgensen BB, Revsbech NP (1995) Microenvironment and photosynthesis of zooxanthellae in scleractinian corals studied with microsensors for O2, pH and light. Mar Ecol Prog Ser 117:159–172

    Article  Google Scholar 

  31. 31.

    Reynaued S, Leclercq N, Romaine-Lioud S, Ferrier-Pages C, Jaubert J, Gattuso JP (2003) Interacting effects of CO2 partial pressure and temperature on photosynthesis and calcification in a scleractinian coral. Glob Chang Biol 9:1660–1668

    Article  Google Scholar 

  32. 32.

    Towanda T (2008) Effects of CO2-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

    Google Scholar 

  33. 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

    PubMed  Article  CAS  Google Scholar 

  34. 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

    PubMed  Article  Google Scholar 

  35. 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

    Article  Google Scholar 

  36. 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

    PubMed  Article  CAS  Google Scholar 

  37. 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

    Article  Google Scholar 

  38. 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

    Article  Google Scholar 

  39. 39.

    Geffen Y, Rosenberg E (2005) Stress-induced rapid release of antibacterials by scleractinian corals. Mar Biol 146:931–935

    Article  Google Scholar 

  40. 40.

    Koh E (1997) Do scleractinian corals engage in chemical warfare against microbes? J Chem Ecol 23:379–398

    Article  CAS  Google Scholar 

  41. 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

    Article  Google Scholar 

  42. 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

    PubMed  Google Scholar 

  43. 43.

    Nissimov J, Rosenberg E, Munn CB (2009) Antimicrobial properties of resident coral mucus bacteria of Oculina patagonica. FEMS Microbiol Lett 292:210–215

    PubMed  Article  CAS  Google Scholar 

  44. 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

    Article  Google Scholar 

  45. 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

    Article  Google Scholar 

  46. 46.

    Legendre P, Gallagher E (2001) Ecologically meaningful transformations for ordination of species data. Oecologia 129:271–280

    Article  Google Scholar 

  47. 47.

    Feingersch R, Beja O (2009) Bias in assessments of marine SAR11 biodiversity in environmental fosmid and BAC libraries? ISME J 3:1117–1119

    PubMed  Article  Google Scholar 

  48. 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

    Article  Google Scholar 

  49. 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

    Article  Google Scholar 

  50. 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

    Article  Google Scholar 

  51. 51.

    Connell H (1978) Diversity in tropical rain forests and coral reefs. Science 199:1302–1310

    PubMed  Article  CAS  Google Scholar 

  52. 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

    Article  CAS  Google Scholar 

  53. 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

    PubMed  Article  Google Scholar 

  54. 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

    PubMed  Article  Google Scholar 

  55. 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

    Article  CAS  Google Scholar 

  56. 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

    Article  Google Scholar 

  57. 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

    PubMed  CAS  Google Scholar 

  58. 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

    Article  Google Scholar 

  59. 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

    CAS  Google Scholar 

  60. 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

    CAS  Google Scholar 

  61. 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

    PubMed  CAS  Google Scholar 

  62. 62.

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

    Article  Google Scholar 

  63. 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

    Article  Google Scholar 

Download references

Acknowledgments

The work was partially supported by the US-Israel Binational Science Foundation grant no. 2006318 to EB and by the Israel Science Foundation 09/328 to MF. This project was also partially funded by a grant (PH-MICROB) from the Association of European Marine Biology Laboratory (ASSEMBLE) to EB and DM. Partial contribution was also provided by the European Project “Mediterranean Sea Acidification under a changing climate” (MedSeA; grant agreement 265103). Thanks are due to all collaborators from Stazione Zoologica “A. Dohrn” for their help during the fieldwork.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Ehud Banin.

Additional information

Maoz Fine and Ehud Banin contributed equally to this work.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(DOCX 24 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Meron, D., Buia, M., Fine, M. et al. Changes in Microbial Communities Associated with the Sea Anemone Anemonia viridis in a Natural pH Gradient. Microb Ecol 65, 269–276 (2013). https://doi.org/10.1007/s00248-012-0127-6

Download citation

Keywords

  • Microbial Community
  • Ocean Acidification
  • Symbiodinium Cell
  • Symbiodinium Density
  • Coral Pathogen