Microbial Ecology

, Volume 67, Issue 4, pp 819–828 | Cite as

Shallow Water Marine Sediment Bacterial Community Shifts Along a Natural CO2 Gradient in the Mediterranean Sea Off Vulcano, Italy

  • Dorsaf Kerfahi
  • Jason M. Hall-Spencer
  • Binu M. Tripathi
  • Marco Milazzo
  • Junghoon Lee
  • Jonathan M. Adams
Environmental Microbiology

Abstract

The effects of increasing atmospheric CO2 on ocean ecosystems are a major environmental concern, as rapid shoaling of the carbonate saturation horizon is exposing vast areas of marine sediments to corrosive waters worldwide. Natural CO2 gradients off Vulcano, Italy, have revealed profound ecosystem changes along rocky shore habitats as carbonate saturation levels decrease, but no investigations have yet been made of the sedimentary habitat. Here, we sampled the upper 2 cm of volcanic sand in three zones, ambient (median pCO2 419 μatm, minimum Ωarag 3.77), moderately CO2-enriched (median pCO2 592 μatm, minimum Ωarag 2.96), and highly CO2-enriched (median pCO2 1611 μatm, minimum Ωarag 0.35). We tested the hypothesis that increasing levels of seawater pCO2 would cause significant shifts in sediment bacterial community composition, as shown recently in epilithic biofilms at the study site. In this study, 454 pyrosequencing of the V1 to V3 region of the 16S rRNA gene revealed a shift in community composition with increasing pCO2. The relative abundances of most of the dominant genera were unaffected by the pCO2 gradient, although there were significant differences for some 5 % of the genera present (viz. Georgenia, Lutibacter, Photobacterium, Acinetobacter, and Paenibacillus), and Shannon Diversity was greatest in sediments subject to long-term acidification (>100 years). Overall, this supports the view that globally increased ocean pCO2 will be associated with changes in sediment bacterial community composition but that most of these organisms are resilient. However, further work is required to assess whether these results apply to other types of coastal sediments and whether the changes in relative abundance of bacterial taxa that we observed can significantly alter the biogeochemical functions of marine sediments.

Supplementary material

248_2014_368_MOESM1_ESM.docx (25 kb)
ESM 1(DOCX 25 kb)
248_2014_368_MOESM2_ESM.xlsx (91 kb)
ESM 2(XLSX 91 kb)

References

  1. 1.
    Widdicombe S, Spicer JI, Kitidis V (2011) Effects of ocean acidifi cation on sediment fauna. In: Gattuso JP, Hansson L (eds) Ocean acidification. Oxford University Press, Oxford, pp 176–191Google Scholar
  2. 2.
    Munn CB (2011) Marine microbiology: ecology and applications, 2nd edn. Garland Science, New YorkGoogle Scholar
  3. 3.
    Caldeira K, Wickett ME (2003) Anthropogenic carbon and ocean pH. Nature 425(6956):365–365CrossRefPubMedGoogle Scholar
  4. 4.
    Olafsson J, Olafsdottir SR, Benoit-Cattin A, Danielsen M, Arnarson TS, Takahashi T (2009) Rate of Iceland Sea acidification from time series measurements. Biogeosciences 6(11):2661–2668CrossRefGoogle Scholar
  5. 5.
    Liu JW, Weinbauer MG, Maier C, Dai MH, Gattuso JP (2010) Effect of ocean acidification on microbial diversity and on microbe-driven biogeochemistry and ecosystem functioning. Aquat Microb Ecol 61(3):291–305. doi:10.3354/Ame01446 CrossRefGoogle Scholar
  6. 6.
    Allgaier M, Riebesell U, Vogt M, Thyrhaug R, Grossart HP (2008) Coupling of heterotrophic bacteria to phytoplankton bloom development at different pCO2 levels: a mesocosm study. Biogeosciences 5(4):1007–1022. doi:10.5194/bg-5-1007-2008 CrossRefGoogle Scholar
  7. 7.
    Newbold LK, Oliver AE, Booth T, Tiwari B, DeSantis T, Maguire M, Andersen G, van der Gast CJ, Whiteley AS (2012) The response of marine picoplankton to ocean acidification. Environ Microbiol 14(9):2293–2307CrossRefPubMedGoogle Scholar
  8. 8.
    Ray JL, Topper B, An S, Silyakova A, Spindelbock J, Thyrhaug R, DuBow MS, Thingstad TF, Sandaa RA (2012) Effect of increased pCO2 on bacterial assemblage shifts in response to glucose addition in Fram Strait seawater mesocosms. Fems Microbiol Ecol 82(3):713–723. doi:10.1111/j.1574-6941.2012.01443.x CrossRefPubMedGoogle Scholar
  9. 9.
    Lindh MV, Riemann L, Baltar F, Romero-Oliva C, Salomon PS, Graneli E, Pinhassi J (2013) Consequences of increased temperature and acidification on bacterioplankton community composition during a mesocosm spring bloom in the Baltic Sea. Environ Microbiol Rep 5(2):252–262. doi:10.1111/1758-2229.12009 CrossRefPubMedGoogle Scholar
  10. 10.
    Sperling M, Piontek J, Gerdts G, Wichels A, Schunck H, Roy AS, La Roche J, Gilbert J, Nissimov JI, Bittner L, Romac S, Riebesell U, Engel A (2013) Effect of elevated CO2 on the dynamics of particle-attached and free-living bacterioplankton communities in an Arctic fjord. Biogeosciences 10(1):181–191. doi:10.5194/bg-10-181-2013 CrossRefGoogle Scholar
  11. 11.
    Roy AS, Gibbons SM, Schunck H, Owens S, Caporaso JG, Sperling M, Nissimov JI, Romac S, Bittner L, Muhling M, Riebesell U, LaRoche J, Gilbert JA (2013) Ocean acidification shows negligible impacts on high-latitude bacterial community structure in coastal pelagic mesocosms. Biogeosciences 10(1):555–566. doi:10.5194/bg-10-555-2013 CrossRefGoogle Scholar
  12. 12.
    Krause E, Wichels A, Gimenez L, Lunau M, Schilhabel MB, Gerdts G (2012) Small changes in pH have direct effects on marine bacterial community composition: a microcosm approach. Plos One 7 (10)Google Scholar
  13. 13.
    Kroeker KJ, Micheli F, Gambi MC (2013) Ocean acidification causes ecosystem shifts via altered competitive interactions. Nat Clim Change 3(2):156–159. doi:10.1038/Nclimate1680 CrossRefGoogle Scholar
  14. 14.
    Fabricius KE, Langdon C, Uthicke S, Humphrey C, Noonan S, Death G, Okazaki R, Muehllehner N, Glas MS, Lough JM (2011) Losers and winners in coral reefs acclimatized to elevated carbon dioxide concentrations. Nat Clim Change 1(3):165–169. doi:10.1038/Nclimate1122 CrossRefGoogle Scholar
  15. 15.
    Rodolfo-Metalpa R, Houlbreque F, Tambutte E, Boisson F, Baggini C, Patti FP, Jeffree R, Fine M, Foggo A, Gattuso JP, Hall-Spencer JM (2011) Coral and mollusc resistance to ocean acidification adversely affected by warming. Nat Clim Change 1(6):308–312CrossRefGoogle Scholar
  16. 16.
    Kitidis V, Laverock B, McNeill LC, Beesley A, Cummings D, Tait K, Osborn MA, Widdicombe S (2011) Impact of ocean acidification on benthic and water column ammonia oxidation. Geophys Res Lett 38:Artn L21603. doi:10.1029/2011gl049095 CrossRefGoogle Scholar
  17. 17.
    Ghosh A, Dey N, Bera A, Tiwari A, Sathyaniranjan K, Chakrabarti K, Chattopadhyay D (2010) Culture independent molecular analysis of bacterial communities in the mangrove sediment of Sundarban, India. Saline Syst 6(1):1. doi:10.1186/1746-1448-6-1 PubMedCentralCrossRefPubMedGoogle Scholar
  18. 18.
    Hongxiang X, Min W, Xiaogu W, Junyi Y, Chunsheng W (2008) Bacterial diversity in deep-sea sediment from northeastern Pacific Ocean. Acta Ecol Sin 28(2):479–485. doi:10.1016/S1872-2032(08)60026-8 CrossRefGoogle Scholar
  19. 19.
    Hendriks IE, Duarte CM, Alvarez M (2010) Vulnerability of marine biodiversity to ocean acidification: a meta-analysis. Estuar Coast Shelf Sci 86(2):157–164CrossRefGoogle Scholar
  20. 20.
    Johnson VR, Brownlee C, Rickaby REM, Graziano M, Milazzo M, Hall-Spencer JM (2011) Responses of marine benthic microalgae to elevated CO2. Mar Biol:1–12. doi:10.1007/s00227-011-1840-2
  21. 21.
    Lidbury I, Johnson V, Hall-Spencer JM, Munn CB, Cunliffe M (2012) Community-level response of coastal microbial biofilms to ocean acidification in a natural carbon dioxide vent ecosystem. Mar Pollut Bull 64(5):1063–1066. doi:10.1016/j.marpolbul.2012.02.011 CrossRefPubMedGoogle Scholar
  22. 22.
    Boatta F, D’Alessandro W, Gagliano AL, Liotta M, Milazzo M, Rodolfo-Metalpa R, Hall-Spencer JM, Parello F (2013) Geochemical survey of Levante Bay, Vulcano Island (Italy), a natural laboratory for the study of ocean acidification. Mar Pollut Bull: 485–494. doi:10.1016/j.marpolbul.2013.01.029
  23. 23.
    Kerrison P, Hall-Spencer JM, Suggett DJ, Hepburn LJ, Steinke M (2011) Assessment of pH variability at a coastal CO2 vent for ocean acidification studies. Estuar Coast Shelf Sci 94(2):129–137. doi:10.1016/j.ecss.2011.05.025 CrossRefGoogle Scholar
  24. 24.
    Unno T, Jang J, Han D, Kim JH, Sadowsky MJ, Kim OS, Chun J, Hur HG (2010) Use of barcoded pyrosequencing and shared OTUs to determine sources of fecal bacteria in watersheds. Environ Sci Technol 44(20):7777–7782. doi:10.1021/Es101500z CrossRefPubMedGoogle Scholar
  25. 25.
    Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microb 75(23):7537–7541. doi:10.1128/Aem.01541-09 CrossRefGoogle Scholar
  26. 26.
    Huse SM, Welch DM, Morrison HG, Sogin ML (2010) Ironing out the wrinkles in the rare biosphere through improved OTU clustering. Environ Microbiol 12(7):1889–1898. doi:10.1111/j.1462-2920.2010.02193.x PubMedCentralCrossRefPubMedGoogle Scholar
  27. 27.
    Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27(16):2194–2200. doi:10.1093/bioinformatics/btr381 PubMedCentralCrossRefPubMedGoogle Scholar
  28. 28.
    Price MN, Dehal PS, Arkin AP (2010) FastTree 2—approximately maximum-likelihood trees for large alignments. Plos One 5(3):Artn E9490. doi:10.1371/Journal.Pone.0009490 CrossRefGoogle Scholar
  29. 29.
    Oksanen J, Kindt R, Legendre P, O’Hara B, Stevens MHH, Oksanen MJ, Suggests M (2007) The vegan package. Community ecology package Disponível em: http://www.R-project.org Acesso em 10 (01):2008
  30. 30.
    Simmons S, Norris PR (2002) Acidophiles of saline water at thermal vents of Vulcano, Italy. Extremophiles 6(3):201–207. doi:10.1007/s007920100242 CrossRefPubMedGoogle Scholar
  31. 31.
    Rusch A, Amend JP (2008) Functional characterization of the microbial community in geothermally heated marine sediments. Microb Ecol 55(4):723–736. doi:10.1007/s00248-007-9315-1 CrossRefPubMedGoogle Scholar
  32. 32.
    Inagaki F, Suzuki M, Takai K, Oida H, Sakamoto T, Aoki K, Nealson KH, Horikoshi K (2003) Microbial communities associated with geological horizons in coastal subseafloor sediments from the Sea of Okhotsk. Appl Environ Microbiol 69(12):7224–7235PubMedCentralCrossRefPubMedGoogle Scholar
  33. 33.
    Bowman JP, McCuaig RD (2003) Biodiversity, community structural shifts, and biogeography of prokaryotes within Antarctic continental shelf sediment. Appl Environ Microb 69(5):2463–2483CrossRefGoogle Scholar
  34. 34.
    Ravenschlag K, Sahm K, Amann R (2001) Quantitative molecular analysis of the microbial community in marine arctic sediments (Svalbard). Appl Environ Microbiol 67(1):387–395. doi:10.1128/AEM.67.1.387-395.2001 PubMedCentralCrossRefPubMedGoogle Scholar
  35. 35.
    Li WJ, Xu P, Schumann P, Zhang YQ, Pukall R, Xu LH, Stackebrandt E, Jiang CL (2007) Georgenia ruanii sp. nov., a novel actinobacterium isolated from forest soil in Yunnan (China), and emended description of the genus Georgenia. Int J Syst Evol Micr 57:1424–1428. doi:10.1099/ijs.0.64749-0 CrossRefGoogle Scholar
  36. 36.
    Altenburger P, Kämpfer P, Schumann P, Vybiral D, Lubitz W, Busse HJ (2002) Georgenia muralis gen. nov., sp. nov., a novel actinobacterium isolated from a medieval wall painting. Int J Syst Evol Micr 52(Pt 3):875–881Google Scholar
  37. 37.
    Park S, Kang SJ, Oh TK, Yoon JH (2010) Lutibacter maritimus sp. nov., isolated from a tidal flat sediment. Int J Syst Evol Micr 60:610–614. doi:10.1099/Ijs.0.012401-0 CrossRefGoogle Scholar
  38. 38.
    Choi DH, Cho BC (2006) Lutibacter litoralis gen. nov., sp. nov., a marine bacterium of the family Flavobacteriaceae isolated from tidal flat sediment. Int J Syst Evol Micr 56:771–776. doi:10.1099/ijs.0.64146-0 CrossRefGoogle Scholar
  39. 39.
    Farmer JJ III, Hickman-Brenner FW (2006) The genera vibrio and photobacterium. In: Dworkin M, Falkow S, Rosenberg E, Schleifer K-H, Stackebrandt E (eds) The prokaryotes. Springer, New York, pp 508–563CrossRefGoogle Scholar
  40. 40.
    Nogi Y, Masui N, Kato C (1998) Photobacterium profundum sp. nov., a new, moderately barophilic bacterial species isolated from a deep-sea sediment. Extremophiles 2(1):1–7. doi:10.1007/s007920050036 CrossRefPubMedGoogle Scholar
  41. 41.
    Wagner M, Erhart R, Manz W, Amann R, Lemmer H, Wedi D, Schleifer KH (1994) Development of an rRNA-targeted oligonucleotide probe specific for the genus Acinetobacter and its application for in situ monitoring in activated sludge. Appl Environ Microbiol 60(3):792–800PubMedCentralPubMedGoogle Scholar
  42. 42.
    Heyndrickx M, Vandemeulebroecke K, Hoste B, Janssen P, Kersters K, De Vos P, Logan NA, Ali N, Berkeley RC (1996) Reclassification of Paenibacillus (formerly Bacillus) pulvifaciens (Nakamura 1984) Ash et al. 1994, a later subjective synonym of Paenibacillus (formerly Bacillus) larvae (White 1906) Ash et al. 1994, as a subspecies of P. larvae, with emended descriptions of P. larvae as P. larvae subsp. larvae and P. larvae subsp. pulvifaciens. Int J Sys Bacteriol 46(1):270–279CrossRefGoogle Scholar
  43. 43.
    Dias BB, Hart B, Smart CW, Hall-Spencer JM (2010) Modern seawater acidification: the response of foraminifera to high-CO2 conditions in the Mediterranean Sea. J Geol Soc London 167(5):843–846. doi:10.1144/0016-76492010-050 CrossRefGoogle Scholar
  44. 44.
    Uthicke S, Momigliano P, Fabricius KE (2013) High risk of extinction of benthic foraminifera in this century due to ocean acidification. Sci Rep 3:1769. doi:10.1038/srep01769 PubMedCentralCrossRefGoogle Scholar
  45. 45.
    Pettit LR, Hart MB, Medina-Sanchez AN, Smart CW, Rodolfo-Metalpa R, Hall-Spencer JM, Prol-Ledesma RM (2013) Benthic foraminifera show some resilience to ocean acidification in the northern Gulf of California, Mexico. Mar Pollut Bull: 452–462. doi:10.1016/j.marpolbul.2013.02.011
  46. 46.
    Moy AD, Howard WR, Bray SG, Trull TW (2009) Reduced calcification in modern Southern Ocean planktonic foraminifera. Nat Geosci 2(4):276–280CrossRefGoogle Scholar
  47. 47.
    Meron D, Buia MC, Fine M, Banin E (2013) Changes in microbial communities associated with the sea anemone Anemonia viridis in a natural pH gradient. Microb Ecol 65(2):269–276. doi:10.1007/s00248-012-0127-6 CrossRefPubMedGoogle Scholar
  48. 48.
    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 6(9):1775–1785PubMedCentralCrossRefPubMedGoogle Scholar
  49. 49.
    Shannon CE, Weaver W (1948) A mathematical theory of communication. vol 27. American Telephone and Telegraph CompanyGoogle Scholar
  50. 50.
    Piontek J, Lunau M, Handel N, Borchard C, Wurst M, Engel A (2010) Acidification increases microbial polysaccharide degradation in the ocean. Biogeosciences 7(5):1615–1624. doi:10.5194/bg-7-1615-2010 CrossRefGoogle Scholar
  51. 51.
    Fierer N, Bradford MA, Jackson RB (2007) Toward an ecological classification of soil bacteria. Ecology 88(6):1354–1364CrossRefPubMedGoogle Scholar
  52. 52.
    Tripathi BM, Kim M, Singh D, Lee-Cruz L, Lai-Hoe A, Ainuddin AN, Go R, Rahim RA, Husni MH, Chun J, Adams JM (2012) Tropical soil bacterial communities in Malaysia: pH dominates in the equatorial tropics too. Microb Ecol 64(2):474–484. doi:10.1007/s00248-012-0028-8 CrossRefPubMedGoogle Scholar
  53. 53.
    Chapin FS, Walker BH, Hobbs RJ, Hooper DU, Lawton JH, Sala OE, Tilman D (1997) Biotic control over the functioning of ecosystems. Science 277(5325):500–504. doi:10.1126/science.277.5325.500 CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  • Dorsaf Kerfahi
    • 1
    • 4
  • Jason M. Hall-Spencer
    • 2
  • Binu M. Tripathi
    • 1
  • Marco Milazzo
    • 3
  • Junghoon Lee
    • 5
  • Jonathan M. Adams
    • 1
  1. 1.Department of Biological SciencesSeoul National UniversityGwanak-GuRepublic of Korea
  2. 2.Marine Biology and Ecology Research CentrePlymouth UniversityPlymouthUK
  3. 3.Dipartimento di Scienze della Terra e del MareUniversity of PalermoPalermoItaly
  4. 4.School of Chemical and Biological EngineeringSeoul National UniversityGwanak-GuRepublic of Korea
  5. 5.School of Mechanical and Aerospace EngineeringSeoul National UniversityGwanak-GuRepublic of Korea

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