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Changes in prokaryotic community composition accompanying a pronounced temperature shift of a shallow marine thermal brine pool (Panarea Island, Italy)

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Abstract

Hot Lake is a recently described thermal brine pool off Panarea Island (Eolian Islands, Italy) where emitted fluids are highly saline and rich in CO2 and H2S. The prokaryotic community composition in surface sediment samples was analyzed by high-throughput Illumina sequencing targeting the V3 region of the 16S rRNA at two time points that differed mainly with respect to temperature conditions, high-temperature (94 °C, HT09) and low-temperature (28.5 °C, LT10). Bacterial richness and diversity were greater than those of Archaea under both temperature conditions. In contrast to Bacteria, diversity and evenness of Archaea greatly increased at LT10. While the phylogenetic analysis indicated the presence of members mostly affiliated with the same taxonomic groups, their relative abundances differed from HT09 to LT10, resulting in different bacterial and archaeal assemblages. Both HT09 and LT10 were dominated by members of the Epsilonproteobacteria. Within this subphylum, bacteria of the genus Sulfurimonas were most frequently detected at HT09, while Arcobacter prevailed at LT10. The abundance of other dominant taxonomic groups (≥1 % of Illumina reads) also correlated with temperature conditions. Members assigned to hyperthermophilic Euryarchaeota (Thermococci) or to thermophilic (Caldiserica) and thermoresistant (Firmicutes) bacterial taxa were dominant at HT09, while those related to non-thermophilic Bacteroidetes, Fusobacteria and Actinobacteria were dominant at LT10. Several, probably photosynthetic, members of the Alphaproteobacteria, Chlorobi, Cyanobacteria and Chloroflexi were recovered under both temperature conditions. The co-occurrence of photosynthetic and chemolithotrophic microorganisms represents a unique feature of shallow vents such as Hot Lake.

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References

  • Brinkhoff T, Muyzer G (1997) Increased species diversity and extended habitat range of sulfur-oxidizing Thiomicrospira spp. Appl Environ Microbiol 63:3789–3796

    PubMed Central  CAS  PubMed  Google Scholar 

  • Campbell BJ, Engel AS, Porter ML, Takai K (2006) The versatile epsilon-proteobacteria: key players in sulphidic habitats. Nat Rev Microbiol 4:458–468

    Article  CAS  PubMed  Google Scholar 

  • Campbell BJ, Polson SW, Zeigler Allen L, Williamson SJ, Lee CK, Wommack KE, Cary SC (2013) Diffuse flow environments within basalt- and sediment based hydrothermal vent ecosystems harbor specialized microbial communities. Front Microbiol 4:182. doi:10.3389/fmicb.2013.00182

    Article  PubMed Central  PubMed  Google Scholar 

  • Cole JR, Wang Q, Cardenas E, Fish J, Chai B, Farris RJ, Kulam-Syed-Mohideen AS, McGarrell DM, Marsh T, Garrity GM, Tiedje JM (2009) The ribosomal database project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res 37:D141–D145

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Dando P, Aliani S, Arab H, Bianchi C, Brehmer M, Cocito S, Fowler SW, Gundersen J, Hooper LE, Kolbl R, Kuever J, Linke P, Makropoulos KC, Meloni R, Miquel JC, Morri C, Muller S, Robinson C, Schlesner H, Sievert S, Stohr R, Stuben D, Thomm M, Varnavas SP, Ziebis W (2000) Hydrothermal studies in the Aegean Sea. Phys Chem Earth B Hydro Oceans Atmos 25:1–8. doi:10.1016/S1464-1909(99)00112-4

    Article  Google Scholar 

  • DasSarma S, Fleischmann EF (1995) Archaea: a laboratory manual. Halophiles. Cold Spring Harbour Laboratory Press, New York, pp 269–272

    Google Scholar 

  • Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics. doi:10.1093/bioinformatics/btq461

    PubMed  Google Scholar 

  • Flores GE, Shakya M, Meneghin J, Yang ZK, Seewald JS, Geoff Wheat C, Podar M, Reysenbach AL (2012) Inter-field variability in the microbial communities of hydrothermal vent deposits from a back-arc basin. Geobiology 10:333–346

    Article  CAS  PubMed  Google Scholar 

  • 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 16:105–117

    Article  Google Scholar 

  • Gugliandolo C, Italiano F, Maugeri TL (2006) The submarine hydrothermal system of Panarea (Southern Italy): biogeochemical processes at the thermal fluids-sea bottom interface. Ann Geophys 49:783–792

    Google Scholar 

  • Gugliandolo C, Lentini V, Spanò A, Maugeri TL (2012) New bacilli from shallow hydrothermal vents of Panarea Island (Italy) and their biotechnological potentialities. J Appl Microbiol 112:1102–1112

    Article  CAS  PubMed  Google Scholar 

  • Hansen MC, Tolker-Neilson T, Givskov M, Molin S (1998) Biased 16S rDNA PCR amplification caused by interference from DNA flanking template region. FEMS Microbiol Ecol 26:141–149

    Article  CAS  Google Scholar 

  • 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 73:7642–7656

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Huang C-I, Schubotz F, Price R, Amend J, Bach W, Meyerdierks A, Amann R (2010) Geomicrobiological study at shallow-sea hydrothermal vent site, Hot Lake, Lago Caldo, Panarea, Italy. 2th International Workshop on Research in Shallow Marine and Fresh Water Systems, Milazzo, Italy, Abstract p 37, 3–10 October 2010

  • Huber JA, Mark Welch DB, Morrison HG, Huse SM, Neal PR, Butterfield DA, Sogin ML (2007) Microbial population structures in the deep marine biosphere. Science 318:97–100

    Article  CAS  PubMed  Google Scholar 

  • Huber JA, Cantin HV, Huse SM, Welch DB, Sogin ML, Butterfield DA (2010) Isolated communities of Epsilonproteobacteria in hydrothermal vent fluids of the Mariana Arc seamounts. FEMS Microbiol Ecol 73:538–549

    CAS  PubMed  Google Scholar 

  • Inagaki F, Takai K, Kobayashi H, Nealson KH, Horikoshi K (2003) Sulfurimonas autotrophica gen. nov., sp. nov., a novel sulfur-oxidizing epsilon-proteobacterium isolated from hydrothermal sediments in the Mid-Okinawa Trough. Int J Syst Evol Microbiol 53:1801–1805

    Article  CAS  PubMed  Google Scholar 

  • Inagaki F, Takai K, Nealson KH, Horikoshi K (2004) Sulfurovum lithotrophicum gen. nov., sp. nov., a novel sulfur-oxidizing chemolithoautotroph within the epsilon-proteobacteria isolated from Okinawa Trough hydrothermal sediments. Int J Syst Evol Microbiol 54:1477–1482

    Article  CAS  PubMed  Google Scholar 

  • Italiano F (2009) Hydrothermal fluids vented at shallow depths at the Aeolian islands: relationships with volcanic and geothermal systems. Procs. Int. Workshop Research in shallow marine and fresh water systems, Freiberg, pp 55–60, 14–16 May 2009

  • Italiano F, Nuccio PM (1991) Geochemical investigations of submarine volcanic exhalations to the East of Panarea, Eolian Islands, Italy. J Volcanol Geotherm Res 46:125–141

    Article  CAS  Google Scholar 

  • Kerfahi D, Hall-Spencer JM, Tripathi BM, Milazzo M, Lee J, Adams JM (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

    Article  CAS  PubMed  Google Scholar 

  • Lentini V, Gugliandolo C, Bunk B, Overmann J, Maugeri TL (2014) Diversity of prokaryotic community at a shallow marine hydrothermal site elucidated by Illumina sequencing technology. Curr Microbiol 69:457–466

    Article  CAS  PubMed  Google Scholar 

  • 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 55:626–639

    Article  CAS  PubMed  Google Scholar 

  • 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, Trieste Lint 11, p 199–205

  • Maugeri TL, Gugliandolo C, Caccamo D, Stackebrandt E (2001) A polyphasic taxonomic study of thermophilic bacilli from shallow, marine vents. Syst Appl Microbiol 24:451–468

    Article  Google Scholar 

  • Maugeri TL, Gugliandolo C, Caccamo D, Stackebrandt E (2002) Three novel halotolerant and thermophilic Geobacillus strains from shallow marine vents. Syst Appl Microbiol 25:450–455

    Article  CAS  PubMed  Google Scholar 

  • Maugeri TL, Lentini V, Gugliandolo C, Italiano F, Cousin S, Stackebrandt E (2009) Bacterial and archaeal populations at two shallow hydrothermal vents off Panarea Island (Eolian Islands, Italy). Extremophiles 13:199–212

    Article  CAS  PubMed  Google Scholar 

  • Maugeri TL, Lentini V, Gugliandolo C, Italiano F, Cousin S, Stackebrandt E (2010) Microbial diversity at a hot shallow thermal vent in the Southern Tyrrhenian Sea (Italy). Geomicrobiol J 27:1–11

    Article  Google Scholar 

  • Maugeri TL, Lentini V, Spanò A, Gugliandolo C (2013a) Abundance and diversity of picocyanobacteria in shallow hydrothermal vents of Panarea Island (Italy). Geomicrobiol J 30:93–99

    Article  CAS  Google Scholar 

  • Maugeri TL, Gugliandolo C, Lentini V (2013b) Diversity of prokaryotes at a shallow submarine vent by high-throughput Illumina sequencing. Atti della Accademia Peloritana dei Pericolanti Classe di Scienze Fisiche, Matematiche e Naturali ISSN 1825–1242. doi:10.1478/AAPP.912A1

  • Meyer JL, Akerman NH, Proskurowski G, Huber JA (2013) Microbiological characterization of post-eruption “snowblower” vents at Axial Seamount. Front Microbiol, Juan de Fuca Ridge. doi:10.3389/fmicb.2013.00153

    Google Scholar 

  • Price RE, Lesniewski R, Nitzsche KS, Meyerdierks A, Saltikov C, Pichler T, Amend JP (2013) Archaeal and bacterial diversity in an arsenic-rich shallow sea hydrothermal system undergoing phase separation. Front Microbiol. doi:10.3389/fmicb.2013.00158

    Google Scholar 

  • Reysenbach AL, Gotz D, Yernool D (2002) Microbial diversity of marine and terrestrial thermal springs. In: Staley JT, Reysenbach AL (eds) Biodiversity of microbial life. Wiley, New York, pp 345–421

    Google Scholar 

  • 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 Microbiol 75:7537–7541

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sieland R, Steinbrückner D, Hamel M, Merkel B, Schipek M (2009) Geochemical investigations and gas quantification of submarine fluid discharges in the hydrothermal system of Panarea (Aeolian Islands, Italy). FOG–Freiberg Online. Geology 22:87–93

    Google Scholar 

  • 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 66:3102–3109

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Steinbrückner D (2009) Quantification of submarine degassing of Panarea Volcano in the Aeolian archipelago, Italy. FOG–Freiberg Online. Geology 23:1–113

    Google Scholar 

  • Takai K, Hirayama H, Nakagawa T, Suzuki Y, Nealson KH, Horikoshi K (2005) Lebetimonas acidiphila gen. nov., sp. nov., a novel thermophilic, acidophilic, hydrogen-oxidizing chemolithoautotroph within the ‘Epsilonproteobacteria’, isolated from a deep-sea hydrothermal fumarole in the Mariana Arc. Int J Syst Evol Microbiol 55:183–189

    Article  CAS  PubMed  Google Scholar 

  • Tarasov VG (2006) Effects of shallow-water hydrothermal venting on biological communities of coastal marine ecosystems of the Western Pacific. Adv Mar Biol 50:267–421

    Article  CAS  PubMed  Google Scholar 

  • Tarasov VG, Gebruk AV, Mironov AN, Moskalev LI (2005) Deep-sea and shallow-water hydrothermal vent communities: two different phenomena? Chem Geol 224:5–39

    Article  CAS  Google Scholar 

  • Tassi F, Capaccioni B, Caramanna G, Cinti D, Montegrossi G, Pizzino L, Quattrocchi F, Vaselli O (2009) Low-pH waters discharging from submarine vents at Panarea Island (Aeolian Islands, southern Italy) after the 2002 gas blast: origin of hydrothermal fluids and implications for volcanic surveillance. Appl Geochem 24:246–254

    Article  CAS  Google Scholar 

  • Thornburg CC, Zabriskie TM, McPhail KL (2010) Deep-sea hydrothermal vents: potential hot spots for natural products discovery? J Nat Prod 73:489–499

    Article  CAS  PubMed  Google Scholar 

  • Wang QG, Garrity M, Tiedje JM, Cole JR (2007) Naïve Bayesian Classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wirsen CO, Sievert SM, Cavanaugh CM, Molyneaux SJ, Ahmad A, Taylor LT, DeLong EF, Taylor CD (2002) Characterization of an autotrophic sulfide-oxidizing marine Arcobacter sp. that produces filamentous sulfur. Appl Environ Microbiol 68:316–325

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zinger L, Amaral-Zettler LA, Fuhrman JA, Horner-Devine MC, Huse SM, Welch DBM, Martiny JBH, Sogin M, Boetius A, Ramette A (2011) Global patterns of bacterial beta-diversity in seafloor and seawater ecosystems. PLoS One 6(9):e24570. doi:10.1371/journal.pone.0024570

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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Correspondence to Concetta Gugliandolo.

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Communicated by A. Oren.

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Gugliandolo, C., Lentini, V., Bunk, B. et al. Changes in prokaryotic community composition accompanying a pronounced temperature shift of a shallow marine thermal brine pool (Panarea Island, Italy). Extremophiles 19, 547–559 (2015). https://doi.org/10.1007/s00792-015-0737-2

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