Advertisement

Extremophiles

, Volume 13, Issue 1, pp 199–212 | Cite as

Bacterial and archaeal populations at two shallow hydrothermal vents off Panarea Island (Eolian Islands, Italy)

  • Teresa Luciana Maugeri
  • Valeria Lentini
  • Concetta Gugliandolo
  • Francesco Italiano
  • Sylvie Cousin
  • Erko Stackebrandt
Original Paper

Abstract

The aim of this study was to investigate the microbial community thriving at two shallow hydrothermal vents off Panarea Island (Italy). Physico-chemical characteristics of thermal waters were examined in order to establish the effect of the vents on biodiversity of both Bacteria and Archaea. Water and adjacent sediment samples were collected at different times from two vents, characterised by different depth and temperature, and analysed to evaluate total microbial abundances, sulphur-oxidising and thermophilic aerobic bacteria. Total microbial abundances were on average of the order of 105 cells ml−1, expressed as picoplanktonic size fraction. Picophytoplanktonic cells accounted for 0.77–3.83% of the total picoplanktonic cells. The contribution of bacterial and archaeal taxa to prokaryotic community diversity was investigated by PCR–DGGE fingerprinting method. The number of bands derived from bacterial DNA was highest in the DGGE profiles of water sample from the warmest and deepest site (site 2). In contrast, archaeal richness was highest in the water of the coldest and shallowest site (site 1). Sulphur-oxidising bacteria were detected by both culture-dependent and -independent methods. The primary production at the shallow hydrothermal system of Panarea is supported by a complex microbial community composed by phototrophs and chemolithotrophs.

Keywords

Archaea Bacteria Prokaryote community PCR–DGGE Shallow hydrothermal vents 

Notes

Acknowledgments

This study was partially supported by research grants (FIRB 2001) from Ministero Istruzione, Università e Ricerca (MIUR), Rome, Italy, and partially by research grants (2002 financing ORME024370) from the University of Messina, Italy. We would like to thank Evelyne Brambilla, DSMZ (Braunschweig, Germany) for her invaluable technical assistance.

References

  1. Alain K, Zbinden M, Le Bris N, Lesongeur F, Querellou J, Gaill F, Cambon-Bonavita MA (2004) Early steps in microbial colonization processes at deep-sea hydrothermal vents. Environ Microbiol 6:227–241PubMedCrossRefGoogle Scholar
  2. Alexander B, Andersen JH, Cox RP, Imhoff JF (2002) Phylogeny of green sulphur bacteria on the basis of gene sequences of 16S rRNA and of the Fenna-Matthews-Olson protein. Arch Microbiol 178:131–140PubMedCrossRefGoogle Scholar
  3. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402PubMedCrossRefGoogle Scholar
  4. Amann RI, Ludwig W, Schleifer K (1995) Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol Rev 59:143–169PubMedGoogle Scholar
  5. Amend JP, Rogers KL, Shock EL, Gurrieri S, Inguaggiato S (2003a) Energetics of chemolithoautotrophy in the hydrothermal system of Vulcano Island, Southern Italy. Geobiology 1:37–58CrossRefGoogle Scholar
  6. Amend JP, Meyer-Dombard DR, Sheth SN, Zolotova N, Amend AC (2003b) Palaeococcus helgesonii sp. nov., a facultatively anaerobic, hyperthermophilic archaeon from a geothermal well on Vulcano Island, Italy. Arch Microbiol 179:394–401PubMedGoogle Scholar
  7. American Public Health Association (1969) Standard methods for the examination of water and wastewater, including bottom sediments and sludge. American Public Health Association, Washington DC, pp 604–609Google Scholar
  8. Caccamo D, Gugliandolo C, Stackebrandt E, Maugeri TL (2000) Bacillus vulcani sp. nov., a novel thermophilic species isolated from a shallow marine hydrothermal vent. Int J Syst Evol Microbiol 50:2009–2012PubMedGoogle Scholar
  9. Caccamo D, Maugeri TL, Gugliandolo C (2001) Identification of thermophilic and marine bacilli from shallow thermal vents by restriction analysis of their amplified 16S rDNA. J Appl Microbiol 91:520–524PubMedCrossRefGoogle Scholar
  10. Campbell BJ, Engel AS, Porter ML, Takai K (2006) The versatile epsilon-proteobacteria: key players in sulphidic habitats. Nat Rev Microbiol 4:458–468PubMedCrossRefGoogle Scholar
  11. Capaccioni B, Tassi F, Vaselli O, Tedesco D, Poreda R (2007) Submarine gas burst at Panarea Island, southern Italy, on 3 November 2002: a magmatic versus hydrothermal episode. J Geophys Res 112:B05201. doi: 10.1029/2006JB004359 CrossRefGoogle Scholar
  12. Capasso G, Inguaggiato S (1998) A simple method for the determination of dissolved gases in natural waters. An application to thermal waters from Vulcano island. Appl Geochem 13(5):631–642CrossRefGoogle Scholar
  13. Caracausi A, Ditta M, Italiano F, Longo M, Nuccio PM, Paonita A, Rizzo A (2005) Changes in fluid geochemistry and physico-chemical conditions of geothermal systems caused by magmatic input: the recent abrupt outgassing off the island of Panarea (Aeolian Islands, Italy). Geochem Cosmochim Acta 69:3045–3059CrossRefGoogle Scholar
  14. Casamayor EO, Schäfer H, Bañeras L, Pedrós-Alió C, Muyzer G (2000) Identification of and spatio-temporal difference between microbial assemblages from two neighboring sulphur lakes: comparison by microscopy and denaturing gradient gel electrophoresis. Appl Environ Microbiol 66:499–508PubMedCrossRefGoogle Scholar
  15. Corre E, Reysenbach AL, Prieur D (2001) Epsilon-proteobacterial diversity from a deep-sea hydrothermal vent on the Mid-Atlantic Ridge. FEMS Microbiol Lett 205:329–335PubMedGoogle Scholar
  16. Ehrhardt CJ, Haymon RM, Lamontagne MG, Holden PA (2007) Evidence for hydrothermal Archaea within the basaltic flanks of the East Pacific Rise. Environ Microbiol 9:900–912PubMedCrossRefGoogle Scholar
  17. Ferris MJ, Muyzer G, Ward DM (1996) Denaturing gradient gel electrophoresis profiles of 16S rRNA-defined populations inhabiting a hot spring microbial mat community. Appl Environ Microbiol 62:340–346PubMedGoogle Scholar
  18. Fiala G, Stetter KO (1986) Pyrococcus furiosus sp. nov. represents a novel genus of marine heterotrophic archaebacteria growing optimally at 100°C. Arch Microbiol 145:56–61CrossRefGoogle Scholar
  19. Garrity GM, Bell JA, Lilburn T (2005) Order V. Thiotrichales ord. nov. In: Brenner DJ, Krieg NR, Staley JT, Garrity GM (eds) Bergey’s manual of systematic bacteriology, (The Proteobacteria), part B (The Gammaproteobacteria), New York, Springer, p 131Google Scholar
  20. Glissman K, Chin KJ, Casper P, Conrad R (2004) Methanogenic pathway and archaeal community structure in the sediment of eutrophic Lake Dagow: effect of temperature. Microb Ecol 48:389–399PubMedCrossRefGoogle Scholar
  21. Graff A, Stubner S (2003) Isolation and molecular characterization of thiosulphate-oxidizing bacteria from an Italian rice field soil. Syst Appl Microbiol 26:445–452PubMedCrossRefGoogle Scholar
  22. Gugliandolo C, Maugeri TL (1998) Temporal variations in heterotrophic mesophilic bacteria from a marine shallow hydrothermal vent off the Island of Vulcano (Eolian Islands, Italy). Microb Ecol 36:13–22PubMedCrossRefGoogle Scholar
  23. Gugliandolo C, Italiano F, Maugeri TL, Inguaggiato S, Caccamo D, Amend JP (1999) Submarine hydrothermal vents of the Eolian Islands: relationship between microbial communities and thermal fluids. Geomicrobiol J 16:105–117CrossRefGoogle Scholar
  24. Gugliandolo C, Maugeri TL, Caccamo D, Stackebrandt E (2003) Bacillus aeolius sp. nov. a novel thermophilic, halophilic marine Bacillus species from Eolian Islands (Italy). Syst Appl Microbiol 26:172–176PubMedCrossRefGoogle Scholar
  25. Hafenbradl D, Keller M, Dirmeier R, Rachel R, Roßnagel P, Burggraf S, Huber H, Stetter KO (1996) Ferroglobus placidus gen. nov., a novel hyperthermophilic archaeum that oxidizes Fe2+ at neutral pH under anoxic conditions. Arch Microbiol 166:308–314PubMedCrossRefGoogle Scholar
  26. Heising S, Richter L, Ludwig W, Schink B (1999) Chlorobium ferrooxidans sp. nov., a phototrophic green sulphur bacterium that oxidizes ferrous iron in coculture with a ‘Geospirillum’ sp. strain. Arch Microbiol 172:116–124PubMedCrossRefGoogle Scholar
  27. Hirayama H, Sunamura M, Takai K, Nunoura T, Noguchi T, Oida H, Furushima Y, Yamamoto H, Oomori T, Horikoshi K (2007) Culture-dependent and -independent characterization of microbial communities associated with a shallow submarine hydrothermal system occurring within a Coral Reef off Taketomi Island, Japan. Appl Environ Microbiol 73:764–7656CrossRefGoogle Scholar
  28. Huber H, Stetter KO (1989) Thiobacillus prosperus sp. nov., represents a new group of halotolerant metal-mobilizing bacteria isolated from a marine geothermal field. Arch Microbiol 151:479–485CrossRefGoogle Scholar
  29. Huber R, Langworthy TA, König H, Thomm M, Woese CR, Sleytr UB, Stetter KO (1986) Thermotoga maritima sp. nov. represents a new genus of unique extremely thermophilic eubacteria growing up to 90°C. Arch Microbiol 144:324–333CrossRefGoogle Scholar
  30. Italiano F, Nuccio PM (1991) Geochemical investigations of submarine volcanic exhalations to the East of Panarea, Eolian Islands, Italy. J Volcanol Geotherm Res 46:125–141CrossRefGoogle Scholar
  31. Kielak A, Pijl AS, van Veen JA, Kowalchuk GA (2008) Differences in vegetation composition and plant species identity lead to only minor changes in soil-borne microbial communities in a former arable field. FEMS Microbiol Ecol 63:372–382PubMedCrossRefGoogle Scholar
  32. Kodama Y, Watanabe K (2003) Isolation and characterization of a sulphur-oxidizing chemolithotroph growing on crude oil under anaerobic conditions. Appl Environ Microbiol 69:107–112PubMedCrossRefGoogle Scholar
  33. Lane DJ (1991) 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M, Wiley J, Sons LDT (eds) Nucleic acid techniques in bacterial systematics. West Sussex, UK, pp 115–175Google Scholar
  34. Manini E, Luna GM, Corinaldesi C, Zeppilli D, Bortoluzzi G, Caramanna G, Raffa F, Danovaro R (2008) Prokaryote diversity and virus abundance in shallow hydrothermal vents of the Mediterranean Sea (Panarea Island) and the Pacific Ocean (North Sulawesi-Indonesia). Microb Ecol 55:626–639PubMedCrossRefGoogle Scholar
  35. Maugeri TL, Acosta Pomar MLC, Bruni V (1990) Picoplancton. In: Innamorati M, Ferrari I, Marino D, Ribera D’Alcalà M (eds) Metodi per lo studio del plancton marino. Nova Thalassia Lint Trieste, Italy, pp 199–205Google Scholar
  36. Maugeri TL, Gugliandolo C, Caccamo D, Stackebrandt E (2001) A polyphasic taxonomic study of thermophilic bacilli from shallow, marine vents. Syst Appl Microbiol 24:572–587PubMedCrossRefGoogle Scholar
  37. Maugeri TL, Gugliandolo C, Caccamo D, Stackebrandt E (2002) Three novel halotolerant and thermophilic Geobacillus strains from shallow marine vents. Syst Appl Microbiol 25:450–455PubMedCrossRefGoogle Scholar
  38. Miller TR, Franklin MP, Halden RU (2007) Bacterial community analysis of shallow groundwater undergoing sequential anaerobic and aerobic chloroethane biotransformation. FEMS Microbiol Ecol 60:299–311PubMedCrossRefGoogle Scholar
  39. Mills HJ, Martinez RJ, Story S, Sobecky PA (2005) Characterization of microbial community structure in Gulf of Mexico gas hydrates: comparative analysis of DNA- and RNA-derived clone libraries. Appl Environ Microbiol 71:3235–3247PubMedCrossRefGoogle Scholar
  40. Muyzer G (1999) DGGE/TGGE a method for identifying genes from natural ecosystems. Curr Opin Microbiol 2:317–322PubMedCrossRefGoogle Scholar
  41. Muyzer G, De Waal EC, Uitterlinden AG (1993) Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction amplified genes coding for 16S rRNA. Appl Environ Microbiol 59:695–700PubMedGoogle Scholar
  42. Muyzer G, Hottenträger S, Teske A, Wawer C (1996) Denaturing gradient gel electrophoresis of PCR-amplified 16S rDNA—A new molecular approach to analyse the genetic diversity of mixed microbial communities. In: Akkermans ADL, van Elsas JD, de Bruijn FJ (eds) Molecular microbial ecology manual. Kluwer Academic Publishers, Dordrecht, pp 1–23Google Scholar
  43. Nakagawa S, Takai K, Inagaki F, Chiba H, Ishibashi J, Kataoka S, Hirayama H, Nunoura T, Horikoshi K, Sako Y (2005) Variability in microbial community and venting chemistry in a sediment-hosted backarc hydrothermal system: impacts of subseafloor phase-separation. FEMS Microbiol Ecol 54:141–155PubMedCrossRefGoogle Scholar
  44. Page A, Juniper SK, Olagnon M, Alain K, Desrosiers G, Querellou J, Cambon-Bonavita MA (2004) Microbial diversity associated with a Paralvinella sulfincola tube and the adjacent substratum on an active deep-sea vent chimney. Geobiology 2:225–238CrossRefGoogle Scholar
  45. Raskin L, Stromley JM, Rittmann BE, Stahl DA (1994) Group specific 16S rRNA hybridization probes to describe natural communities of methanogens. Appl Environ Microbiol 60:1232–1240PubMedGoogle Scholar
  46. Rogers KL, Amend JP (2005) Archaeal diversity and geochemical energy yields in a geothermal well on Vulcano Island, Italy. Geobiology 3:319–332CrossRefGoogle Scholar
  47. Rusch A, Amend JP (2004) Order-specific 16S rRNA-targeted oligonucleotide probes for (hyper) thermophilic archaea and bacteria. Extremophiles 8:357–366PubMedCrossRefGoogle Scholar
  48. Rusch A, Walpersdorf E, deBeer D, Gurrieri S, Amend JP (2005) Microbial communities near the oxic/anoxic interface in the hydrothermal system of Vulcano Island, Italy. Chem Geol 224:169–182CrossRefGoogle Scholar
  49. Sievert SM, Brinkhoff T, Muyzer G, Ziebis W, Kuever J (1999) Spatial heterogeneity of bacterial populations along an environmental gradient at a shallow submarine hydrothermal vent near Milos Island (Greece). Appl Environ Microbiol 65:3834–3842PubMedGoogle Scholar
  50. Sievert SM, Kuever J, Muyzer G (2000) Identification of 16S ribosomal DNA-defined bacterial populations at a shallow submarine hydrothermal vent near Milos Island (Greece). Appl Environ Microbiol 66:3102–3109PubMedCrossRefGoogle Scholar
  51. Sievert SM, Scott KM, Klotz MG, Chain PS, Hauser LJ, Hemp J, Hugler M, Land M, Lapidus A, Larimer FW, Lucas S, Malfatti SA, Meyer F, Paulsen IT, Ren Q, Simon J (2008) Genome of the epsilonproteobacterial chemolithoautotroph Sulfurimonas denitrificans. Appl Environ Microbiol 74:1145–1156PubMedCrossRefGoogle Scholar
  52. Skoog A, Vlahos P, Rogers KL, Amend JP (2007) Concentrations, distributions, and energy yields of dissolved neutrals aldoles in a shallow hydrothermal vent system of Vulcano, Italy. Org Geochem 38:1416–1430CrossRefGoogle Scholar
  53. Stahl DA, Amann RI (1991) Development and application of nucleic acid probes. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. Wiley, New York, pp 205–248Google Scholar
  54. Stetter KO (1988) Archaeoglobus fulgidus gen. nov., sp. nov. a new taxon of extremely thermophilic Archaebacteria. Syst Appl Microbiol 10:172–173Google Scholar
  55. Stetter KO, König H, Stackebrandt E (1983) Pyrodictium gen. nov., a new genus of submarine disc-shaped sulfur reducing Archaebacteria growing optimally at 105°C. Syst Appl Microbiol 4:535–551Google Scholar
  56. Sugisaki R, Taki K (1987) Simplified analysis of He, Ne and Ar dissolved in natural waters. Chem J 21:21–23Google Scholar
  57. Suzuki MT, Beja O, Taylor LT, Delong EF (2001) Phylogenetic analysis of ribosomal RNA operons from uncultivated coastal marine bacterioplankton. Environ Microbiol 3:323–331PubMedCrossRefGoogle Scholar
  58. Svensson E, Skoog A, Amend JP (2004) Concentration and distribution of dissolved amino acids in a shallow hydrothermal system, Vulcano Island (Italy). Org Geochem 35:1001–1014CrossRefGoogle Scholar
  59. Takai K, Suzuki M, Nakagawa S, Miyazaki M, Suzuki Y, Inagaki F, Horikoshi K (2006) Sulfurimonas paralvinellae sp. nov., a novel mesophilic, hydrogen- and sulfur-oxidizing chemolithoautotroph within the Epsilonproteobacteria isolated from a deep-sea hydrothermal vent polychaete nest, reclassification of Thiomicrospira denitrificans as Sulfurimonas denitrificans comb. nov. and emended description of the genus Sulfurimonas. Int J Syst Evol Microbiol 56:1725–1733PubMedCrossRefGoogle Scholar
  60. Tuttle JH, Jannasch HW (1972) Occurrence and types of Thiobacillus-like Bacteria in the sea. Limnol Oceanogr 32:591–607Google Scholar
  61. Van der Gucht K, Sabbe K, De Meester L, Vloemans N, Zwart G, Gillis M, Vyverman W (2001) Contrasting bacterioplankton community composition and seasonal dynamics in two neighbouring hypertrophic freshwater lakes. Environ Microbiol 3:680–690CrossRefGoogle Scholar
  62. Zaballos M, Lopez-Lopez A, Ovreas L, Galan Bartual S, D’Auria G, Alba JC, Legault B, Pushker R, Daae FL, Rodriguez-Valera F (2006) Comparison of prokaryotic diversity at offshore oceanic locations reveals a different microbiota in the Mediterranean Sea. FEMS Microbiol Ecol 56:389–405PubMedCrossRefGoogle Scholar
  63. Zhang G, Niu F, Ma X, Liu W, Dong M, Feng H, An L, Cheng G (2007) Phylogenetic diversity of bacteria isolates from the Qinghai-Tibet Plateau permafrost region. Can J Microbiol 53:1000–1010PubMedCrossRefGoogle Scholar

Copyright information

© Springer 2008

Authors and Affiliations

  • Teresa Luciana Maugeri
    • 1
  • Valeria Lentini
    • 1
  • Concetta Gugliandolo
    • 1
  • Francesco Italiano
    • 2
  • Sylvie Cousin
    • 3
  • Erko Stackebrandt
    • 3
  1. 1.Dipartimento di Biologia Animale ed Ecologia MarinaUniversità di MessinaMessinaItaly
  2. 2.Istituto Nazionale di Geofisica e VulcanologiaPalermoItaly
  3. 3.Deutsche Sammlung von Mikroorganismen und Zellkulturen GmbHBraunschweigGermany

Personalised recommendations