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Thermoplasmatales and sulfur-oxidizing bacteria dominate the microbial community at the surface water of a CO2-rich hydrothermal spring located in Tenorio Volcano National Park, Costa Rica

  • Alejandro Arce-Rodríguez
  • Fernando Puente-Sánchez
  • Roberto Avendaño
  • María Martínez-Cruz
  • J. Maarten de Moor
  • Dietmar H. Pieper
  • Max Chavarría
Original Paper

Abstract

Here we report the chemical and microbial characterization of the surface water of a CO2-rich hydrothermal vent known in Costa Rica as Borbollones, located at Tenorio Volcano National Park. The Borbollones showed a temperature surrounding 60 °C, a pH of 2.4 and the gas released has a composition of ~ 97% CO2, ~ 0.07% H2S, ~ 2.3% N2 and ~ 0.12% CH4. Other chemical species such as sulfate and iron were found at high levels with respect to typical fresh water bodies. Analysis by 16S rRNA gene metabarcoding revealed that in Borbollones predominates an archaeon from the order Thermoplasmatales and one bacterium from the genus Sulfurimonas. Other sulfur- (genera Thiomonas, Acidithiobacillus, Sulfuriferula, and Sulfuricurvum) and iron-oxidizing bacteria (genera Sideroxydans, Gallionella, and Ferrovum) were identified. Our results show that CO2-influenced surface water of Borbollones contains microorganisms that are usually found in acid rock drainage environments or sulfur-rich hydrothermal vents. To our knowledge, this is the first microbiological characterization of a CO2-dominated hydrothermal spring from Central America and expands our understanding of those extreme ecosystems.

Keywords

Borbollones Wet mofette CO2-rich thermal Archaea Sulfur-oxidizing bacteria Tenorio Volcano National Park 

Notes

Acknowledgements

We acknowledge the support during field work from the park rangers at Tenorio Volcano National Park and the SINAC administration. We also are grateful to Arnoldo Vargas for help in the design of some figures.

Author contributions

AA-R, FP-S, MC conceived and designed the experiments. AA-R, RA, MM-C, MdM performed the experiments. AA-R, FP-S, MC analyzed the data. DHP, MC contributed reagents or materials or analysis tools. AA-R, FP-S, DHP, MC wrote the paper. All authors reviewed and approved the final version of the manuscript.

Funding

The Vice-rectory of Research of Universidad de Costa Rica (809-B6-524), CENIBiot and by the ERC grant IPBSL (ERC250350-IPBSL) supported this research. Data Intensive Academic Grid, which is supported by the USA National Science Foundation (0959894) provided computational resources. F.P-S. is supported by the Spanish Economy and Competitiveness Ministry (MINECO) grant CTM2016-80095-C2-1-R. MMC acknowledges government funding from the Transitorio I of the National Law 8488 for Emergencies and Risk Prevention in Costa Rica. JMdM gratefully acknowledges support from the Deep Carbon Observatory Biology Meets Subduction project.

Compliance with ethical standards

Conflict of interest

The authors declare that there are no conflicts of interest.

Ethical approval

This study does not describe any experimental work related to human.

Supplementary material

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Supplementary material 1 (DOCX 23 kb)
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Supplementary material 2 (TIFF 12514 kb)
792_2018_1072_MOESM3_ESM.xlsx (39 kb)
Supplementary material 3 (XLSX 38 kb)

Supplementary material 4 (MOV 70971 kb)

References

  1. Akerman NH, Butterfield DA, Huber JA (2013) Phylogenetic diversity and functional gene patterns of sulfur-oxidizing subseafloor Epsilonproteobacteria in diffuse hydrothermal vent fluids. Front Microbiol 4:1–14.  https://doi.org/10.3389/fmicb.2013.00185 CrossRefGoogle Scholar
  2. Alvarado Induni G (2011) Los volcanes de Costa Rica: geología, historia, riqueza natural y su gente. Editorial Universidad Estatal a Distancia, San José, p 386Google Scholar
  3. Arce-Rodríguez A, Puente-Sánchez F, Avendaño R et al (2017) Pristine but metal-rich Río Sucio (Dirty River) is dominated by Gallionella and other iron-sulfur oxidizing microbes. Extremophiles 21:235–243.  https://doi.org/10.1007/s00792-016-0898-7 CrossRefGoogle Scholar
  4. Auernik KS, Cooper CR, Kelly RM (2008) life in hot acid: pathway analyses in extremely thermoacidophilic archaea. Curr Opin Biotechnol 19:445–453.  https://doi.org/10.1016/j.copbio.2008.08.001 CrossRefGoogle Scholar
  5. Barton LL, Fardeau ML, Fauque GD (2014) Hydrogen sulfide: a toxic gas produced by dissimilatory sulfate and sulfur reduction and consumed by microbial oxidation. Met Ions Life Sci 14:237–277.  https://doi.org/10.1007/978-94-017-9269-1_10 CrossRefGoogle Scholar
  6. Beaubien S, Ciotoli G, Coombs P et al (2008) The impact of a naturally occurring CO2 gas vent on the shallow ecosystem and soil chemistry of a Mediterranean pasture (Latera, Italy). Int J Greenh Gas Con 2:373–387.  https://doi.org/10.1016/j.ijggc.2008.03.005 CrossRefGoogle Scholar
  7. Beulig F, Heuer VB, Akob DM et al (2015) Carbon flow from volcanic CO2 into soil microbial communities of a wetland mofette. ISME J 9:746–759.  https://doi.org/10.1038/ismej.2014.148 CrossRefGoogle Scholar
  8. Bohorquez LC, Delgado-Serrano L, López G et al (2012) In-depth characterization via complementing culture-independent approaches of the microbial community in an acidic hot spring of the Colombian Andes. Microb Ecol 63:103–115.  https://doi.org/10.1007/s00248-011-9943-3 CrossRefGoogle Scholar
  9. Burbach K, Seifert J, Pieper DH, Camarinha-Silva A (2016) Evaluation of DNA extraction kits and phylogenetic diversity of the porcine gastrointestinal tract based on Illumina sequencing of two hypervariable regions. Microbiologyopen 5:70–82.  https://doi.org/10.1002/mbo3.312 CrossRefGoogle Scholar
  10. Camacho A (2009) Sulfur bacteria. Encyclopedia of Inland waters. Academic Press, Cambridge, pp 261–278.  https://doi.org/10.1016/b978-012370626-3.00128-9 CrossRefGoogle Scholar
  11. Camarinha-Silva A, Jáuregui R, Chaves-Moreno D et al (2014) Comparing the anterior nare bacterial community of two discrete human populations using Illumina amplicon sequencing. Environ Microbiol 16:2939–2952.  https://doi.org/10.1111/1462-2920.12362 CrossRefGoogle Scholar
  12. Capecchiacci F, Tassi F, Liegler A, Fentrees S, Deering C, Vaselli O, Martínez M, Taylor-Castillo W (2015) Geochemistry of water and gas discharges from the Tenorio volcanic system (Costa Rica). Book of abstracts Conference: Il Pianeta Dinamico: sviluppi e prospettive a 100 anni da Wegener. Firenze 2-4 Settembre 2015Google Scholar
  13. Castellón E, Martínez M, Madrigal-Carballo S et al (2013) Scattering of light by colloidal aluminosilicate particles produces the unusual sky-blue color of Río Celeste (Tenorio Volcano Complex, Costa Rica). PLoS One 8:e75165.  https://doi.org/10.1371/journal.pone.0075165 CrossRefGoogle Scholar
  14. de Moor JM, Fischer TP, Sharp ZD, Hilton DR, Barry PH, Mangasini F, Ramirez C (2013) Gas chemistry and nitrogen isotope compositions of cold mantle gases from Rungwe Volcanic Province, southern Tanzania. Chem Geol 339:30–42.  https://doi.org/10.1016/j.chemgeo.2012.08.004 CrossRefGoogle Scholar
  15. DeLong EF (1992) Archaea in coastal marine environments. Proc Natl Acad Sci USA 89:5685–5689.  https://doi.org/10.1073/pnas.89.12.5685 CrossRefGoogle Scholar
  16. Edgar RC, Haas BJ, Clemente JC et al (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200.  https://doi.org/10.1093/bioinformatics/btr381 CrossRefGoogle Scholar
  17. Frerichs J, Oppermann BI, Gwosdz S et al (2013) Microbial community changes at a terrestrial volcanic CO2 vent induced by soil acidification and anaerobic microhabitats within the soil column. FEMS Microbiol Ecol 84:60–74.  https://doi.org/10.1111/1574-6941.12040 CrossRefGoogle Scholar
  18. Giammanco S, Parello F, Gambardella B et al (2007) Focused and diffuse effluxes of CO2 from mud volcanoes and mofettes south of Mt. Etna (Italy). J Volcanol Geotherm Res 165:46–63.  https://doi.org/10.1016/j.jvolgeores.2007.04.010 CrossRefGoogle Scholar
  19. Giggenbach WF, Gougel R (1989) Method for the collection and analysis of geothermal and volcanic water and gas samples. Chem Div Report No 2387, New Zealand DSIRGoogle Scholar
  20. Golyshina OV, Lünsdorf H, Kublanov IV et al (2016) The novel extremely acidophilic, cell-wall-deficient archaeon Cuniculiplasma divulgatum gen. nov., sp. nov. represents a new family, Cuniculiplasmataceae fam. nov., of the order Thermoplasmatales. Int J Syst Evol Microbiol 66:332–340.  https://doi.org/10.1099/ijsem.0.000725 CrossRefGoogle Scholar
  21. He Z, Xiao S, Xie X et al (2007) Molecular diversity of microbial community in acid mine drainages of Yunfu sulfide mine. Extremophiles 11:305–314.  https://doi.org/10.1007/s00792-006-0044-z CrossRefGoogle Scholar
  22. Huber H, Stetter KO (2006) Thermoplasmatales. In: Dworkin M, Falkow S, Rosenberg E, Schleifer K-H, Stackebrandt E (eds) The prokaryotes. Springer, New York, pp 101–112CrossRefGoogle Scholar
  23. Huber JA, Butter DA, Baross JA (2003) Bacterial diversity in a subsea floor habitat following a deep-sea volcanic eruption. FEMS Microbiol Ecol 43:393–409.  https://doi.org/10.1111/j.1574-6941.2003.tb01080.x CrossRefGoogle Scholar
  24. Inagaki F, Takai K, Kobayashi H et al (2003) Sulfurimonas autotrophica gen. nov., sp. nov., a novel sulfur-oxidizing ε-proteobacterium isolated from hydrothermal sediments in the Mid-Okinawa Trough. Int J Syst Evol Microbiol 53:1801–1805.  https://doi.org/10.1099/ijs.0.02682-0 CrossRefGoogle Scholar
  25. Itoh T, Yoshikawa N, Takashina T (2007) Thermogymnomonas acidicola gen. nov., sp. nov., a novel thermoacidophilic, cell wall-less archaeon in order Thermoplasmatales, isolated from a solfataric soil in Hakone, Japan. Int J Syst Evol Microbiol 57:2557–2561.  https://doi.org/10.1099/ijs.0.65203-0 CrossRefGoogle Scholar
  26. Jiang L, Zheng Y, Chen J et al (2011) Stratification of archaeal communities in shallow sediments of the Pearl River Estuary, Southern China. Antonie Van Leeuwenhoek 99:739–751.  https://doi.org/10.1007/s10482-011-9548-3 CrossRefGoogle Scholar
  27. Jones DS, Kohl C, Grettenberger C et al (2015) Geochemical niches of iron-oxidizing acidophiles in acidic coal mine drainage. Appl Environ Microbiol 81:1242–1250.  https://doi.org/10.1128/AEM.02919-14 CrossRefGoogle Scholar
  28. Kämpf H, Bräuer K, Schumann J et al (2013) CO2 discharge in an active, non-volcanic continental rift area (Czech Republic): characterisation (δ13C,3He/4He) and quantification of diffuse and vent CO2 emissions. Chem Geol 339:71–83.  https://doi.org/10.1016/j.chemgeo.2012.08.005 CrossRefGoogle Scholar
  29. Kozich JJ, Westcott SL, Baxter NT et al (2013) Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the miseq illumina sequencing platform. Appl Environ Microbiol 79:5112–5120.  https://doi.org/10.1128/AEM.01043-13 CrossRefGoogle Scholar
  30. Krauze P, Kämpf H, Horn F et al (2017) Microbiological and geochemical survey of CO2-dominated mofette and mineral waters of the Cheb Basin, Czech Republic. Front Microbiol 8:2446.  https://doi.org/10.3389/fmicb.2017.02446 CrossRefGoogle Scholar
  31. Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874.  https://doi.org/10.1093/molbev/msw054 CrossRefGoogle Scholar
  32. Labrenz M, Grote J, Mammitzsch K et al (2013) Sulfurimonas gotlandica sp. nov., a chemoautotrophic and psychrotolerant epsilonproteobacterium isolated from a pelagic redoxcline, and an emended description of the genus Sulfurimonas. Int J Syst Evol Microbiol 63:4141–4148.  https://doi.org/10.1099/ijs.0.048827-0 CrossRefGoogle Scholar
  33. Luton PE, Wayne JM, Sharp RJ, Riley PW (2002) The mcrA gene as an alternative to 16S rRNA in the phylogenetic analysis of methanogen populations in landfill. Microbiology 148:3521–3530.  https://doi.org/10.1099/00221287-148-11-3521 CrossRefGoogle Scholar
  34. Oppermann BI, Michaelis W, Blumenberg M et al (2010) Soil microbial community changes as a result of long-term exposure to a natural CO2 vent. Geochim Cosmochim Acta 74:2697–2716.  https://doi.org/10.1016/j.gca.2010.02.006 CrossRefGoogle Scholar
  35. Paul K, Nonoh JO, Mikulski L, Brune A (2012) “Methanoplasmatales” Thermoplasmatales-related archaea in termite guts and other environments, are the seventh order of methanogens. Appl Environ Microbiol 78:8245–8253.  https://doi.org/10.1128/AEM.02193-12 CrossRefGoogle Scholar
  36. Pauwels H, Fouillac C, Goff F, Vuataz FD (1997) The isotopic and chemical composition of CO2-rich thermal waters in the mont-dore region (Massif-Central, France). Appl Geochemistry 12:411–427.  https://doi.org/10.1016/S0883-2927(97)00010-3 CrossRefGoogle Scholar
  37. Pronk JT, De Bruyn JC, Bos P, Kuenen JG (1992) Anaerobic growth of Thiobacillus ferrooxidans. Appl Environ Microbiol 58:2227–2230Google Scholar
  38. Pruesse E, Peplies J, Glöckner FO (2012) SINA: accurate high-throughput multiple sequence alignment of ribosomal RNA genes. Bioinformatics 28:1823–1829.  https://doi.org/10.1093/bioinformatics/bts252 CrossRefGoogle Scholar
  39. Puente-Sánchez F, Aguirre J, Parro V (2016) A novel conceptual approach to read-filtering in high-throughput amplicon sequencing studies. Nucleic Acids Res 44:e40.  https://doi.org/10.1093/nar/gkv1113 CrossRefGoogle Scholar
  40. Quast C, Pruesse E, Yilmaz P et al (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41:D590–D596.  https://doi.org/10.1093/nar/gks1219 CrossRefGoogle Scholar
  41. Reysenbach A, Longnecker K, Kirshtein J (2000) Novel bacterial and archaeal lineages from an in situ growth chamber deployed at a mid-atlantic ridge hydrothermal vent. Appl Environ Microbiol 66:3798–3806.  https://doi.org/10.1128/AEM.66.9.3798-3806.2000 CrossRefGoogle Scholar
  42. Sáenz de Miera LE, Arroyo P, de Luis Calabuig E et al (2014) High-throughput sequencing of 16S RNA genes of soil bacterial communities from a naturally occurring CO2 gas vent. Int J Greenh Gas Control 29:176–184.  https://doi.org/10.1016/J.IJGGC.2014.08.014 CrossRefGoogle Scholar
  43. Sánchez-Andrea I, Rojas-Ojeda P, Amils R, Sanz JL (2012) Screening of anaerobic activities in sediments of an acidic environment: tinto River. Extremophiles 16:829–839.  https://doi.org/10.1007/s00792-012-0478-4 CrossRefGoogle Scholar
  44. Schleper C, Pühler G, Klenk P, Zillig W (1996) Picrophilus oshimae and Picrophilus tomdus fam. nov., gen. nov., sp. nov., Two species of hyperacidophilic, thermophilic, heterotrophic, aerobic archaea. Int J Syst Evol Microbiol 46:814–816.  https://doi.org/10.1099/00207713-46-3-814 Google Scholar
  45. Schloss PD, Westcott SL, Ryabin T et al (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541.  https://doi.org/10.1128/AEM.01541-09 CrossRefGoogle Scholar
  46. Segerer A, Langworthy TA, Stetter KO (1988) Thermoplasma acidophilum and Thermoplasma volcanium sp. nov. from solfatara fields. Syst Appl Microbiol 10:161–171.  https://doi.org/10.1016/S0723-2020(88)80031-6 CrossRefGoogle Scholar
  47. Serour E, Antranikian G (2002) Novel thermoactive glucoamylases from the thermoacidophilic archaea Thermoplasma acidophilumPicrophilus torridus and Picrophilus oshimae. Antonie Van Leeuwenhoek 81:73–83.  https://doi.org/10.1023/A:1020525525490 CrossRefGoogle Scholar
  48. Šibanc N, Dumbrell AJ, Mandić-Mulec I, Maček I (2014) Impacts of naturally elevated soil CO2 concentrations on communities of soil archaea and bacteria. Soil Biol Biochem 68:348–356.  https://doi.org/10.1016/j.soilbio.2013.10.018 CrossRefGoogle Scholar
  49. Sievert SM, Scott KM, Klotz MG et al (2008) Genome of the epsilonproteobacterial chemolithoautotroph Sulfurimonas denitrificans. Appl Environ Microbiol 74:1145–1156.  https://doi.org/10.1128/AEM.01844-07 CrossRefGoogle Scholar
  50. Suzuki I, Takeuchi TL, Yuthasastrakosol TD, Oh JK (1990) Ferrous iron and sulfur oxidation and ferric iron reduction activities of Thiobacillus ferrooxidans are affected by growth on ferrous iron, sulfur, or a sulfide ore. Appl Environ Microbiol 56:1620–1626Google Scholar
  51. Takai K, Horikoshi K (1999) Genetic diversity of archaea in deep-sea hydrothermal vent environments. Genetics 152:1285–1297.  https://doi.org/10.1016/s0723-2020(87)80053-x Google Scholar
  52. Timmer-ten Hoor A (1975) A new type of thiosulphate oxidizing, nitrate reducing microorganism: Thiomicrospira denitrificans sp. nov. Netherlands J Sea Res 9:344–350.  https://doi.org/10.1016/0077-7579(75)90008-3 CrossRefGoogle Scholar
  53. Valdés J, Pedroso I, Quatrini R et al (2008) Acidithiobacillus ferrooxidans metabolism: from genome sequence to industrial applications. BMC Genomics 9:597.  https://doi.org/10.1186/1471-2164-9-597 CrossRefGoogle Scholar
  54. Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267.  https://doi.org/10.1128/AEM.00062-07 CrossRefGoogle Scholar
  55. Yasuda M, Oyaizu H, Yamagishi A, Oshima T (1995) Morphological variation of new Thermoplasma acidophilum isolates from Japanese hot springs. Appl Environ Microbiol 61:3482–3485Google Scholar
  56. Zhang M, Zhang T, Shao MF, Fang HHP (2009) Autotrophic denitrification in nitrate-induced marine sediment remediation and Sulfurimonas denitrificans-like bacteria. Chemosphere 76:677–682.  https://doi.org/10.1016/j.chemosphere.2009.03.066 CrossRefGoogle Scholar
  57. Zhou H, Li J, Peng X et al (2009) Microbial diversity of a sulfide black smoker in main endeavour hydrothermal vent field, Juan de Fuca Ridge. J Microbiol 47:235–247.  https://doi.org/10.1007/s12275-008-0311-z CrossRefGoogle Scholar

Copyright information

© Springer Japan KK, part of Springer Nature 2019

Authors and Affiliations

  • Alejandro Arce-Rodríguez
    • 1
    • 2
    • 8
  • Fernando Puente-Sánchez
    • 3
  • Roberto Avendaño
    • 4
  • María Martínez-Cruz
    • 5
  • J. Maarten de Moor
    • 5
  • Dietmar H. Pieper
    • 2
  • Max Chavarría
    • 4
    • 6
    • 7
  1. 1.Institute of MicrobiologyTechnical University of BraunschweigBrunswickGermany
  2. 2.Microbial Interactions and Processes Research GroupHelmholtz Centre for Infection ResearchBrunswickGermany
  3. 3.Systems Biology ProgramCentro Nacional de Biotecnología (CNB-CSIC)MadridSpain
  4. 4.Centro Nacional de Innovaciones Biotecnológicas (CENIBiot)San JoséCosta Rica
  5. 5.Observatorio Vulcanológico y Sismológico de Costa Rica, Universidad Nacional (OVSICORI-UNA)HerediaCosta Rica
  6. 6.Escuela de QuímicaUniversidad de Costa Rica, Sede CentralSan JoséCosta Rica
  7. 7.Centro de Investigaciones en Productos Naturales (CIPRONA)Universidad de Costa Rica, Sede CentralSan JoséCosta Rica
  8. 8.Molecular Bacteriology Research GroupHelmholtz Centre for Infection ResearchBrunswickGermany

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