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

  • Environmental Microbiology
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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.

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References

  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 176–191

    Google Scholar 

  2. Munn CB (2011) Marine microbiology: ecology and applications, 2nd edn. Garland Science, New York

    Google Scholar 

  3. Caldeira K, Wickett ME (2003) Anthropogenic carbon and ocean pH. Nature 425(6956):365–365

    Article  CAS  PubMed  Google Scholar 

  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):2661–2668

    Article  CAS  Google Scholar 

  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

    Article  Google Scholar 

  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

    Article  CAS  Google Scholar 

  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):2293–2307

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  Google Scholar 

  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

    Article  Google Scholar 

  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)

  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

    Article  CAS  Google Scholar 

  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

    Article  CAS  Google Scholar 

  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):308–312

    Article  CAS  Google Scholar 

  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

    Article  Google Scholar 

  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

    Article  PubMed Central  PubMed  Google Scholar 

  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

    Article  Google Scholar 

  19. Hendriks IE, Duarte CM, Alvarez M (2010) Vulnerability of marine biodiversity to ocean acidification: a meta-analysis. Estuar Coast Shelf Sci 86(2):157–164

    Article  CAS  Google Scholar 

  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. 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

    Article  CAS  PubMed  Google Scholar 

  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. 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

    Article  CAS  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  Google Scholar 

  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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  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

    Article  Google Scholar 

  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. Simmons S, Norris PR (2002) Acidophiles of saline water at thermal vents of Vulcano, Italy. Extremophiles 6(3):201–207. doi:10.1007/s007920100242

    Article  CAS  PubMed  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  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):7224–7235

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  33. Bowman JP, McCuaig RD (2003) Biodiversity, community structural shifts, and biogeography of prokaryotes within Antarctic continental shelf sediment. Appl Environ Microb 69(5):2463–2483

    Article  CAS  Google Scholar 

  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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  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

    Article  Google Scholar 

  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):875–881

    CAS  Google Scholar 

  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

    Article  CAS  Google Scholar 

  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

    Article  CAS  Google Scholar 

  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 508–563

    Chapter  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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):792–800

    PubMed Central  CAS  PubMed  Google Scholar 

  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):270–279

    Article  CAS  Google Scholar 

  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

    Article  CAS  Google Scholar 

  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

    Article  PubMed Central  Google Scholar 

  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. Moy AD, Howard WR, Bray SG, Trull TW (2009) Reduced calcification in modern Southern Ocean planktonic foraminifera. Nat Geosci 2(4):276–280

    Article  CAS  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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):1775–1785

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  49. Shannon CE, Weaver W (1948) A mathematical theory of communication. vol 27. American Telephone and Telegraph Company

  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

    Article  CAS  Google Scholar 

  51. Fierer N, Bradford MA, Jackson RB (2007) Toward an ecological classification of soil bacteria. Ecology 88(6):1354–1364

    Article  PubMed  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  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

    Article  CAS  Google Scholar 

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Acknowledgments

This work was partly supported by a grant from the National Research Foundation (NRF) grant funded by the Korean government, Ministry of Education, Science and Technology (MEST) (NRF-2013-031400). This work was also partly supported by the Global Frontier Project, Centre of Integrated Smart Sensors funded by Ministry of Education Science and Technology, Korea (2012M3A6A6054201). DK is supported by the Korean Government Scholarship Program, Ministry of Education, Science, and Technology, South Korea. This work contributes to the EU FP7 project “Mediterranean Sea Acidification under a changing climate” (grant agreement no. 265103), with additional funding from Save Our Seas Foundation.

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Authors and Affiliations

  1. Department of Biological Sciences, Seoul National University, Gwanak-Gu, Seoul, 151-747, Republic of Korea

    Dorsaf Kerfahi, Binu M. Tripathi & Jonathan M. Adams

  2. Marine Biology and Ecology Research Centre, Plymouth University, Plymouth, PL4 8AA, UK

    Jason M. Hall-Spencer

  3. Dipartimento di Scienze della Terra e del Mare, University of Palermo, via Archirafi 28, 90123, Palermo, Italy

    Marco Milazzo

  4. School of Chemical and Biological Engineering, Seoul National University, Gwanak-Gu, Seoul, 151-747, Republic of Korea

    Dorsaf Kerfahi

  5. School of Mechanical and Aerospace Engineering, Seoul National University, Gwanak-Gu, Seoul, 151-747, Republic of Korea

    Junghoon Lee

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  1. Dorsaf Kerfahi
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  4. Marco Milazzo
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Correspondence to Junghoon Lee or Jonathan M. Adams.

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Kerfahi, D., Hall-Spencer, J.M., Tripathi, B.M. et al. Shallow Water Marine Sediment Bacterial Community Shifts Along a Natural CO2 Gradient in the Mediterranean Sea Off Vulcano, Italy. Microb Ecol 67, 819–828 (2014). https://doi.org/10.1007/s00248-014-0368-7

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