Seagrass biofilm communities at a naturally CO2-rich vent

Environmental Microbiology Reports

Volumn 7, Issue 3, 2015, Pages 516-525

  Hassenrück, Christiane ^a   Hofmann, Laurie C ^b   Bischof, Kai ^b   Ramette, Alban ^a,c  

^a MAX PLANCK INSTITUTE FOR MARINE MICROBIOLOGY   (Germany)

^b UNIVERSITY OF BREMEN   (Germany)

^c UNIVERSITY OF BERN   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ALGAE; ANTHOZOA; BACTERIA (MICROORGANISMS); ENHALUS; EUKARYOTA; FUSOBACTERIA; THALASSOMONAS;

ALGAL DNA; BACTERIAL DNA; CARBON DIOXIDE; DNA DIRECTED DNA POLYMERASE; PLANT DNA; RIBOSOME DNA; RNA 16S; RNA 18S; TLI POLYMERASE;

AQUATIC SPECIES; BACTERIUM; BIOFILM; BIOTA; CHEMISTRY; CLASSIFICATION; DNA SEQUENCE; EUKARYOTE; GENETICS; GROWTH, DEVELOPMENT AND AGING; HYDROCHARITACEAE; METABOLISM; MICROBIOLOGY; PAPUA NEW GUINEA;

AQUATIC ORGANISMS; BACTERIA; BIOFILMS; BIOTA; CARBON DIOXIDE; DNA, ALGAL; DNA, BACTERIAL; DNA, PLANT; DNA, RIBOSOMAL; DNA-DIRECTED DNA POLYMERASE; EUKARYOTA; HYDROCHARITACEAE; PAPUA NEW GUINEA; RNA, RIBOSOMAL, 16S; RNA, RIBOSOMAL, 18S; SEQUENCE ANALYSIS, DNA;

EID: 84929269737     PISSN: None     EISSN: 17582229     Source Type: Journal    
DOI: 10.1111/1758-2229.12282     Document Type: Article

References (60)

1. Agawin, N.S.R., Duarte, C.M., Fortes, M.D., Uri, J.S., and Vermaat, J.E. (2001) Temporal changes in the abundance, leaf growth and photosynthesis of three co-occurring Philippine seagrasses. J Exp Mar Bio Ecol 260: 217-239.
2. Bourne, D.G., van der Zee, M.J.J., Botté, E.S., and Sato, Y. (2013) Sulfur-oxidizing bacterial populations within cyanobacterial dominated coral disease lesions. Environ Microbiol Rep 5: 518-524.
3. Brodie, J., Williamson, C.J., Smale, D.A., Kamenos, N.A., Mieszkowska, N., Santos, R., etal. (2014) The future of the northeast Atlantic benthic flora in a high CO2 world. Ecol Evol 4: 2787-2798.
4. Brouns, J.J.W.M., and Heijs, F.M.L. (1986) Production and biomass of the seagrass Enhalus acoroides (L.f.) Royle and its epiphytes. Aquat Bot 25: 21-45.
5. Celdrán, D., Espinosa, E., Sánchez-Amat, A., and Marín, A. (2012) Effects of epibiotic bacteria on leaf growth and epiphytes of the seagrass Posidonia oceanica. Mar Ecol Prog Ser 456: 21-27.
6. Corlett, H., and Jones, B. (2007) Epiphyte communities on Thalassia testudinum from Grand Cayman, British West Indies: their composition, structure, and contribution to lagoonal sediments. Sediment Geol 194: 245-262.
7. Dishaw, L.J., Flores-Torres, J., Lax, S., Gemayel, K., Leigh, B., Melillo, D., etal. (2014) The gut of geographically disparate Ciona intestinalis harbors a core microbiota. PLoS ONE 9: e93386.
8. Donnarumma, L., Lombardi, C., Cocito, S., and Gambi, M.C. (2014) Settlement pattern of Posidonia oceanica epibionts along a gradient of ocean acidification: an approach with mimics. Mediterr Mar Sci 15: 498-509.
9. Fabricius, K.E., Langdon, C., Uthicke, S., Humphrey, C., Noonan, S., De'ath, G., etal. (2011) Losers and winners in coral reefs acclimatized to elevated carbon dioxide concentrations. Nat Clim Chang 1: 165-169.
10. Frias-Lopez, J., Zerkle, A.L., Bonheyo, G.T., and Fouke, B.W. (2002) Partitioning of bacterial communities between seawater and healthy, black band diseased, and dead coral surfaces. Appl Environ Microbiol 68: 2214-2228.
11. Frias-Lopez, J., Klaus, J.S., Bonheyo, G.T., and Fouke, B.W. (2004) Bacterial community associated with black band disease in corals. Appl Environ Microbiol 70: 5955-5962.
12. Garcia, G.D., Gregoracci, G.B., Santos, E.D.O., Meirelles, P.M., Silva, G.G.Z., Edwards, R., etal. (2013) Metagenomic analysis of healthy and white plague-affected Mussismilia braziliensis corals. Microb Ecol 65: 1076-1086.
13. Gradoville, M.R., White, A.E., Bo, D., Church, M.J., and Letelier, R.M. (2014) Diversity trumps acidification: lack of evidence for carbon dioxide enhancement of Trichodesmium community nitrogen or carbon fixation at Station ALOHA. Limnol Oceanogr 59: 645-659.
14. Graue, J., Engelen, B., and Cypionka, H. (2012) Degradation of cyanobacterial biomass in anoxic tidal-flat sediments: a microcosm study of metabolic processes and community changes. ISME J 6: 660-669.
15. Hall-Spencer, J.M., Rodolfo-Metalpa, R., Martin, S., Ransome, E., Fine, M., Turner, S.M., etal. (2008) Volcanic carbon dioxide vents show ecosystem effects of ocean acidification. Nature 454: 96-99.
16. Hamisi, M., Díez, B., Lyimo, T., Ininbergs, K., and Bergman, B. (2013) Epiphytic cyanobacteria of the seagrass Cymodocea rotundata: diversity, diel nifH expression and nitrogenase activity. Environ Microbiol Rep 5: 367-376.
17. Hoegh-Guldberg, O., Mumby, P.J., Hooten, A.J., Steneck, R.S., Greenfield, P., Gomez, E., etal. (2007) Coral reefs under rapid climate change and ocean acidification. Science 318: 1737-1742.
18. Hutchins, D.A., Fu, F.-X., Zhang, Y., Warner, M.E., Feng, Y., Portune, K., etal. (2007) CO2 control of Trichodesmium N2 fixation, photosynthesis, growth rates, and elemental ratios: Implications for past, present, and future ocean biogeochemistry. Limnol Oceanogr 52: 1293-1304.
19. Johnson, V.R., Brownlee, C., Rickaby, R.E.M., Graziano, M., Milazzo, M., and Hall-Spencer, J.M. (2011) Responses of marine benthic microalgae to elevated CO2. Mar Biol 160: 1813-1824.
20. Johnstone, I.M. (1979) Papua New Guinea seagrasses and aspects of the biology and growth of Enhalus acoroides (L.f.) Royle. Aquat Bot 7: 197-208.
21. Kerfahi, D., Hall-Spencer, J.M., Tripathi, B.M., Milazzo, M., Lee, J., and Adams, J.M. (2014) Shallow water marine sediment bacterial community shifts along a natural CO2 gradient in the Mediterranean sea off Vulcano, Italy. Microb Ecol 67: 819-828.
22. Koch, M., Bowes, G., Ross, C., and Zhang, X.-H. (2013) Climate change and ocean acidification effects on seagrasses and marine macroalgae. Glob Chang Biol 19: 103-132.
23. Li, S., Sun, L., Wu, H., Hu, Z., Liu, W., Li, Y., and Wen, X. (2012) The intestinal microbial diversity in mud crab (Scylla paramamosain) as determined by PCR-DGGE and clone library analysis. J Appl Microbiol 113: 1341-1351.
24. Lidbury, I., Johnson, V., Hall-Spencer, J.M., Munn, C.B., and Cunliffe, M. (2012) Community-level response of coastal microbial biofilms to ocean acidification in a natural carbon dioxide vent ecosystem. Mar Pollut Bull 64: 1063-1066.
25. Lomas, M., Hopkinson, B., Losh, J., Ryan, D., Shi, D., Xu, Y., and Morel, F. (2012) Effect of ocean acidification on cyanobacteria in the subtropical North Atlantic. Aquat Microb Ecol 66: 211-222.
26. Low-Décarie, E., Fussmann, G.F., and Bell, G. (2014) Aquatic primary production in a high-CO2 world. Trends Ecol Evol 29: 223-232.
27. Marhaeni, B., Radjasa, O.K., Khoeri, M.M., Sabdono, A., Bengen, D.G., and Sudoyo, H. (2011) Antifouling activity of bacterial symbionts of seagrasses against marine biofilm-forming bacteria. J Environ Prot (Irvine, . Calif). 02: 1245-1249.
28. Martin, S., Rodolfo-Metalpa, R., Ransome, E., Rowley, S., Buia, M.-C., Gattuso, J.-P., and Hall-Spencer, J. (2008) Effects of naturally acidified seawater on seagrass calcareous epibionts. Biol Lett 4: 689-692.
29. Medina-Pons, F.J., Terrados, J., López-López, A., Yarza, P., and Rosselló-Móra, R. (2009) Evaluation of the 18S rRNA clone library approach to study the diversity of the macroeukaryotic leaf-epiphytic community of the seagrass Posidonia oceanica (L.) Delile. Mar Biol 156: 1963-1976.
30. Meron, D., Atias, E., Iasur Kruh, L., Elifantz, H., Minz, D., Fine, M., and Banin, E. (2011) The impact of reduced pH on the microbial community of the coral Acropora eurystoma. ISME J 5: 51-60.
31. Michael, T.S., Shin, H.W., Hanna, R., and Spafford, D.C. (2008) A review of epiphyte community development: surface interactions and settlement on seagrass. J Environ Biol 29: 629-638.
32. Morrow, K.M., Moss, A.G., Chadwick, N.E., and Liles, M.R. (2012) Bacterial associates of two Caribbean coral species reveal species-specific distribution and geographic variability. Appl Environ Microbiol 78: 6438-6449.
33. Morrow, K.M., Bourne, D.G., Humphrey, C., Botté, E.S., Laffy, P., Zaneveld, J., etal. (2014) Natural volcanic CO2 seeps reveal future trajectories for host-microbial associations in corals and sponges. ISME J. 2: 1-15.
34. Mouchka, M.E., Hewson, I., and Harvell, C.D. (2010) Coral-associated bacterial assemblages: current knowledge and the potential for climate-driven impacts. Integr Comp Biol 50: 662-674.
35. Orth, R.J., Carruthers, T.J.B., Dennison, W.C., Duarte, C.M., Fourqurean, J.W., Heck, K.L., Jr, etal. (2006) A global crisis for seagrass ecosystems. Bioscience 56: 987-996.
36. Paerl, H.W., and Huisman, J. (2009) Climate change: a catalyst for global expansion of harmful cyanobacterial blooms. Environ Microbiol Rep 1: 27-37.
37. Quast, C., Pruesse, E., Yilmaz, P., Gerken, J., Schweer, T., Yarza, P., etal. (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41: D590-D596.
38. Ragazzola, F., Foster, L.C., Form, A.U., Büscher, J., Hansteen, T.H., and Fietzke, J. (2013) Phenotypic plasticity of coralline algae in a high CO2 world. Ecol Evol 3: 3436-3446.
39. Ramette, A. (2009) Quantitative community fingerprinting methods for estimating the abundance of operational taxonomic units in natural microbial communities. Appl Environ Microbiol 75: 2495-2505.
40. Raulf, F.F., Fabricius, K.E., Uthicke, S., de Beer, D., Abed, R.M.M., and Ramette, A. (2015) Changes in microbial communities in coastal sediments along natural CO2 gradients at a volcanic vent in Papua New Guinea. Environ Microbiol doi:10.1111/1462-2920.12729.
41. Ries, J.B. (2011) Skeletal mineralogy in a high-CO2 world. J Exp Mar Bio Ecol 403: 54-64.
42. Rungrassamee, W., Klanchui, A., Maibunkaew, S., Chaiyapechara, S., Jiravanichpaisal, P., and Karoonuthaisiri, N. (2014) Characterization of intestinal bacteria in wild and domesticated adult black tiger shrimp (Penaeus monodon). PLoS ONE 9: e91853.
43. Russell, B.D., Connell, S.D., Findlay, H.S., Tait, K., Widdicombe, S., and Mieszkowska, N. (2013) Ocean acidification and rising temperatures may increase biofilm primary productivity but decrease grazer consumption. Philos Trans R Soc Lond B Biol Sci 368(1627):20120438. doi: 10.1098/rstb.2012.0438
44. Sand-Jensen, K. (1977) Effect of epiphytes on eelgrass photosynthesis. Aquat Bot 3: 55-63.
45. Sawall, Y., Richter, C., and Ramette, A. (2012) Effects of eutrophication, seasonality and macrofouling on the diversity of bacterial biofilms in equatorial coral reefs. PLoS ONE 7: e39951.
46. Singh, S.P., and Singh, P. (2014) Effect of CO2 concentration on algal growth: a review. Renew Sustain Energy Rev 38: 172-179.
47. Smith, A.M., Sutherland, J.E., Kregting, L., Farr, T.J., and Winter, D.J. (2012) Phylomineralogy of the coralline red algae: correlation of skeletal mineralogy with molecular phylogeny. Phytochemistry 81: 97-108.
48. Steele, J.A., Countway, P.D., Xia, L., Vigil, P.D., Beman, J.M., Kim, D.Y., etal. (2011) Marine bacterial, archaeal and protistan association networks reveal ecological linkages. ISME J 5: 1414-1425.
49. Sweet, M.J., Bythell, J.C., and Nugues, M.M. (2013) Algae as reservoirs for coral pathogens. PLoS ONE 8: e69717.
50. Teeling, H., Fuchs, B.M., Becher, D., Klockow, C., Gardebrecht, A., Bennke, C.M., etal. (2012) Substrate-controlled succession of marine bacterioplankton populations induced by a phytoplankton bloom. Science 336: 608-611.
51. Thompson, F.L., Barash, Y., Sawabe, T., Sharon, G., Swings, J., and Rosenberg, E. (2006) Thalassomonas loyana sp. nov., a causative agent of the white plague-like disease of corals on the Eilat coral reef. Int J Syst Evol Microbiol 56: 365-368.
52. Uku, J., Björk, M., Bergman, B., and Díez, B. (2007) Characterization and comparison of prokaryotic epiphytes associated with three East African seagrasses. J Phycol 43: 768-779.
53. Vega Thurber, R., Willner-Hall, D., Rodriguez-Mueller, B., Desnues, C., Edwards, R.A., Angly, F., etal. (2009) Metagenomic analysis of stressed coral holobionts. Environ Microbiol 11: 2148-2163.
54. Vizzini, S., Di Leonardo, R., Costa, V., Tramati, C.D., Luzzu, F., and Mazzola, A. (2013) Trace element bias in the use of CO2-vents as analogues for low-pH environments: implications for contamination levels in acidified oceans. Estuar Coast Shelf Sci 134: 19-30.
55. Wahl, M. (1989) Marine epibiosis. I. Fouling and antifouling: some basic aspects. Mar Ecol Prog Ser 58: 175-189.
56. Webster, N.S., Uthicke, S., Botté, E.S., Flores, F., and Negri, A.P. (2013) Ocean acidification reduces induction of coral settlement by crustose coralline algae. Glob Chang Biol 19: 303-315.
57. Weidner, S., Arnold, W., Stackebrandt, E., and Pu, A. (2000) Phylogenetic analysis of bacterial communities associated with leaves of the seagrass Halophila stipulacea by a culture-independent small-subunit rRNA gene approach. Microb Ecol 39: 22-31.
58. Witt, V., Wild, C., Anthony, K.R.N., Diaz-Pulido, G., and Uthicke, S. (2011) Effects of ocean acidification on microbial community composition of, and oxygen fluxes through, biofilms from the Great Barrier Reef. Environ Microbiol 13: 2976-2989.
59. Wolf, C., Frickenhaus, S., Kilias, E.S., Peeken, I., and Metfies, K. (2013) Regional variability in eukaryotic protist communities in the Amundsen Sea. Antarct Sci 11: 1-11.
60. Yamamuro, M., Umezawa, Y., and Koike, I. (2004) Internal variations in nutrient concentrations and the C and N stable isotope ratios in leaves of the seagrass Enhalus acoroides. Aquat Bot 79: 95-102.