Microbial Community Structure Along a Horizontal Oxygen Gradient in a Costa Rican Volcanic Influenced Acid Rock Drainage System


We describe the geochemistry and microbial diversity of a pristine environment that resembles an acid rock drainage (ARD) but it is actually the result of hydrothermal and volcanic influences. We designate this environment, and other comparable sites, as volcanic influenced acid rock drainage (VARD) systems. The metal content and sulfuric acid in this ecosystem stem from the volcanic milieu and not from the product of pyrite oxidation. Based on the analysis of 16S rRNA gene amplicons, we report the microbial community structure in the pristine San Cayetano Costa Rican VARD environment (pH = 2.94–3.06, sulfate ~ 0.87–1.19 g L−1, iron ~ 35–61 mg L−1 (waters), and ~ 8–293 g kg−1 (sediments)). San Cayetano was found to be dominated by microorganisms involved in the geochemical cycling of iron, sulfur, and nitrogen; however, the identity and abundance of the species changed with the oxygen content (0.40–6.06 mg L−1) along the river course. The hypoxic source of San Cayetano is dominated by a putative anaerobic sulfate-reducing Deltaproteobacterium. Sulfur-oxidizing bacteria such as Acidithiobacillus or Sulfobacillus are found in smaller proportions with respect to typical ARD. In the oxic downstream, we identified aerobic iron-oxidizers (Leptospirillum, Acidithrix, Ferrovum) and heterotrophic bacteria (Burkholderiaceae bacterium, Trichococcus, Acidocella). Thermoplasmatales archaea closely related to environmental phylotypes found in other ARD niches were also observed throughout the entire ecosystem. Overall, our study shows the differences and similarities in the diversity and distribution of the microbial communities between an ARD and a VARD system at the source and along the oxygen gradient that establishes on the course of the river.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6


  1. 1.

    Baker BJ, Banfield JF (2003) Microbial communities in acid mine drainage. FEMS Microbiol Ecol 44:139–152

    CAS  Google Scholar 

  2. 2.

    Johnson DB, Bacelar-Nicolau P, Okibe N, Thomas A, Hallberg KB (2009) Ferrimicrobium acidiphilum gen. nov., sp. nov. and Ferrithrix thermotolerans gen. nov., sp. nov.: heterotrophic, iron-oxidizing, extremely acidophilic actinobacteria. Int J Syst Evol Microbiol 59:1082–1089

    CAS  PubMed  Google Scholar 

  3. 3.

    Sánchez-Andrea I, Rodríguez N, Amils R, Sanz JL (2011) Microbial diversity in anaerobic sediments at Río Tinto, a naturally acidic environment with a high heavy metal content. Appl Environ Microbiol 77:6085–6093

    PubMed  PubMed Central  Google Scholar 

  4. 4.

    Arce-Rodríguez A, Puente-Sánchez F, Avendaño R, Martínez-Cruz M, de Moor JM, Pieper DH, Chavarría M (2019) 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. Extremophiles 23:177–187

    PubMed  Google Scholar 

  5. 5.

    Gadanho M, Libkind D, Sampaio JP (2006) Yeast diversity in the extreme acidic environments of the Iberian Pyrite Belt. Microb Ecol 52:552–563

    PubMed  Google Scholar 

  6. 6.

    González-Toril E, Santofimia E, Blanco Y, López-Pamo E, Gómez MJ, Bobadilla M, Cruz R, Palomino EJ, Aguilera Á (2015) Pyrosequencing-based assessment of the microbial community structure of Pastoruri glacier area (Huascarán National Park, Perú), a natural extreme acidic environment. Microb Ecol 70:936–947

    PubMed  Google Scholar 

  7. 7.

    Dold B, Gonzalez-Toril E, Aguilera A, Lopez-Pamo E, Cisternas ME, Bucchi F, Amils R (2013) Acid rock drainage and rock weathering in Antarctica: important sources for iron cycling in the Southern Ocean. Environ Sci Technol 47:6129–6136

    CAS  PubMed  Google Scholar 

  8. 8.

    González-Toril E, Llobet-Brossa E, Casamayor EO et al (2003) Microbial ecology of an extreme acidic environment, the Tinto River. Appl Environ Microbiol 69:4853–4865

    PubMed  PubMed Central  Google Scholar 

  9. 9.

    López-Archilla AI, Gérard E, Moreira D et al (2004) Macrofilamentous microbial communities in the metal-rich and acidic river Tinto Spain. FEMS Microbiol Lett 235:221–228

    Google Scholar 

  10. 10.

    García-Moyano A, González-Toril E, Aguilera Á, Amils R (2012) Comparative microbial ecology study of the sediments and the water column of the Río Tinto, an extreme acidic environment. FEMS Microbiol Ecol 81:303–314

    PubMed  Google Scholar 

  11. 11.

    Sánchez-Andrea I, Knittel K, Amann R, Amils R, Sanz JL (2012) Quantification of Tinto River sediment microbial communities: importance of sulfate-reducing bacteria and their role in attenuating acid mine drainage. Appl Environ Microbiol 78:4638–4645

    PubMed  PubMed Central  Google Scholar 

  12. 12.

    Fernández-Remolar DC, Rodriguez N, Gomez F (2003) Geological record of an acidic environment driven by iron hydrochemistry: the Tinto River system. J Geophys Res 108:5080

    Google Scholar 

  13. 13.

    Amils R, Fernández-Remolar D, the IPBSL Team (2014) Río Tinto: a geochemical and mineralogical terrestrial analogue of Mars. Life 4:511–534

    CAS  PubMed  PubMed Central  Google Scholar 

  14. 14.

    Arce-Rodríguez A, Puente-Sánchez F, Avendaño R, Libby E, Rojas L, Cambronero JC, Pieper DH, Timmis KN, Chavarría M (2017) Pristine but metal-rich Río Sucio (Dirty River) is dominated by Gallionella and other iron-sulfur oxidizing microbes. Extremophiles 21:235–243

    PubMed  Google Scholar 

  15. 15.

    Urbieta M, Porati G, Segretín A, González-Toril E, Giaveno M, Donati E (2015) Copahue geothermal system: a volcanic environment with rich extreme prokaryotic biodiversity. Microorganisms 3:344–363

    CAS  PubMed  PubMed Central  Google Scholar 

  16. 16.

    Johnson DB, Okibe N, Roberto FF (2003) Novel thermos-acidophilic bacteria isolated from geothermal sites in Yellowstone National Park: physiological and phylogenetic characteristics. Arch Microbiol 180:60–68

    CAS  PubMed  Google Scholar 

  17. 17.

    Melton ED, Swanner ED, Behrens S, Schmidt C, Kappler A (2014) The interplay of microbially mediated and abiotic reactions in the biogeochemical Fe cycle. Nat Rev Microbiol 12:797–808

    CAS  PubMed  Google Scholar 

  18. 18.

    Castellón E, Martínez M, Madrigal-Carballo S, Arias ML, Vargas WE, Chavarría M (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

    PubMed  PubMed Central  Google Scholar 

  19. 19.

    González-Toril E, Aguilera A, Rodriguez N, Fernández-Remolar D, Gómez F, Diaz E, García-Moyano A, Sanz JL, Amils R (2010) Microbial ecology of Río Tinto, a natural extreme acidic environment of biohydrometallurgical interest. Hydrometallurgy 104:329–333

    Google Scholar 

  20. 20.

    Bohorquez LC, Delgado-Serrano L, López G, Osorio-Forero C, Klepac-Ceraj V, Kolter R, Junca H, Baena S, Zambrano MM (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

    PubMed  Google Scholar 

  21. 21.

    Camarinha-Silva A, Jáuregui R, Chaves-Moreno D, Oxley APA, Schaumburg F, Becker K, Wos-Oxley ML, Pieper DH (2014) Comparing the anterior nare bacterial community of two discrete human populations using Illumina amplicon sequencing. Environ Microbiol 16:2939–2952

    CAS  PubMed  Google Scholar 

  22. 22.

    Schulz C, Schütte K, Koch N, Vilchez-Vargas R, Wos-Oxley ML, Oxley APA, Vital M, Malfertheiner P, Pieper DH (2018) The active bacterial assemblages of the upper GI tract in individuals with and without Helicobacter infection. Gut 67:216–225

    CAS  PubMed  Google Scholar 

  23. 23.

    Cole JR, Wang Q, Fish JA et al (2014) Ribosomal database project: data and tools for high throughput rRNA analysis. Nucleic Acids Res 42:633–642

    Google Scholar 

  24. 24.

    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

    CAS  PubMed  PubMed Central  Google Scholar 

  25. 25.

    Yilmaz P, Parfrey LW, Yarza P, Gerken J, Pruesse E, Quast C, Schweer T, Peplies J, Ludwig W, Glöckner FO (2014) The SILVA and “All-Species Living Tree Project (LTP)” taxonomic frameworks. Nucleic Acids Res. 42:D643–D648

    CAS  PubMed  Google Scholar 

  26. 26.

    Pruesse E, Peplies J, Glöckner FO (2012) SINA: accurate high-throughput multiple sequence alignment of ribosomal RNA genes. Bioinformatics 28:1823–1829

    CAS  PubMed  PubMed Central  Google Scholar 

  27. 27.

    Pruesse E, Quast C, Knittel K, Fuchs BM, Ludwig W, Peplies J, Glockner FO (2007) SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res 35:7188–7196

    CAS  PubMed  PubMed Central  Google Scholar 

  28. 28.

    Yarza P, Yilmaz P, Pruesse E, Glöckner FO, Ludwig W, Schleifer KH, Whitman WB, Euzéby J, Amann R, Rosselló-Móra R (2014) Uniting the classification of cultured and uncultured bacteria and archaea using 16S rRNA gene sequences. Nat Rev Microbiol 12:635–645

    CAS  PubMed  Google Scholar 

  29. 29.

    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 25:3389–3402

    CAS  PubMed  PubMed Central  Google Scholar 

  30. 30.

    Core Team R (2017) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria http://www.R-project.org/

    Google Scholar 

  31. 31.

    Oksanen J, Blanchet FG, Friendly M, et al (2017) Vegan: Community Ecology Package. R package Version 2.4–3. https://CRAN.R project.org/package=vegan

  32. 32.

    La Gaceta (2017) Decreto N° 33903-MINAE-S El Presidente de la República El Ministro de Ambiente y Energía y la Ministra de Salud. N° 178

  33. 33.

    Vaselli O, Tassi F, Duarte E, Fernandez E, Poreda RJ, Huertas AD (2010) Evolution of fluid geochemistry at the Turrialba volcano (Costa Rica) from 1998 to 2008. Bull Volcanol 72:397–410

    Google Scholar 

  34. 34.

    Alvarado GE, Vega AE (2013) The Cervantes lava flow geomorphology, Irazú volcano (Costa Rica): description of the Central America’s greater lava flow field. Rev Geol Amer Central 48:99–118

    Google Scholar 

  35. 35.

    Ruprecht P, Plank T (2013) Feeding andesitic eruptions with a high-speed connection from the mantle. Nature 500:68–72

    CAS  PubMed  Google Scholar 

  36. 36.

    Piazza AD, Vona A, Mollo S et al (2019) Unsteady magma discharge during the “El Retiro” subplinian eruption (Turrialba volcano, Costa Rica): insights from textural and petrological analyses. J Volcanol Geotherm Res 371:101–115

    Google Scholar 

  37. 37.

    Kusakabe M, Komoda Y, Takano B, Abiko T (2000) Sulfur isotopic effects in the disproportionation reaction of sulfur dioxide in hydrothermal fluids: implications for the δ34S variations of dissolved bisulfate and elemental sulfur from active crater lakes. J Volcanol Geotherm Res 97:287–307

    CAS  Google Scholar 

  38. 38.

    Reagan M, Duarte E, Soto, et al (2006) The eruptive history of Turrialba volcano, Costa Rica, and potential hazards from future eruptions In Rose WI, Bluth GJS, Carr MJ et al Volcanic Hazards in Central América: Geological Society of America Special Paper 412, 235–257

  39. 39.

    Marcucci EC, Hynek BM (2014) Laboratory simulations of acid-sulfate weathering under volcanic hydrothermal conditions: implications for early Mars. J Geophys Res 119:679–703

    CAS  Google Scholar 

  40. 40.

    Zimbelman DR, Rye RO, Breit GN (2005) Origin of secondary sulfate minerals on active andesitic stratovolcanoes. Chem Geol 215:37–60

    CAS  Google Scholar 

  41. 41.

    Winch S, Mills HJ, Kostka JE, Fortin D, Lean DRS (2009) Identification of sulfate-reducing bacteria in methylmercury-contaminated mine tailings by analysis of SSU rRNA genes. FEMS Micro Ecol 68:94–107

    CAS  Google Scholar 

  42. 42.

    Johnson DB, Joulian C, D’Hugues P et al (2008) Sulfobacillus benefaciens sp. nov., an acidophilic facultative anaerobic Firmicute isolated from mineral bioleaching operations. Extremophiles 12:789–798

    CAS  PubMed  Google Scholar 

  43. 43.

    Watling HR, Perrot FA, Shiers DW (2008) Comparison of selected characteristics of Sulfobacillus species and review of their occurrence in acidic and bioleaching environments. Hydrometallurgy 93:57–65

    CAS  Google Scholar 

  44. 44.

    Norris PR, Clark DA, Owen JP, Waterhouse S (1996) Characteristics of Sulfobacillus acidophilus sp. nov. and other moderately thermophilic mineral-sulphide-oxidizing bacteria. Microbiology 142:775–783

    CAS  PubMed  PubMed Central  Google Scholar 

  45. 45.

    Pina PS, Oliveira VA, Cruz FLS, Leão VA (2010) Kinetics of ferrous iron oxidation by Sulfobacillus thermosulfidooxidans. Biochem Eng J 51:194–197

    CAS  Google Scholar 

  46. 46.

    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 56:1620–1626

    CAS  PubMed  PubMed Central  Google Scholar 

  47. 47.

    Pronk JT, Johnson DB (1992) Oxidation and reduction of iron by acidophilic bacteria. Geomicrobiol J 10:79

    Google Scholar 

  48. 48.

    Menzel P, Gudbergsdóttir SR, Rike AG, Lin L, Zhang Q, Contursi P, Moracci M, Kristjansson JK, Bolduc B, Gavrilov S, Ravin N, Mardanov A, Bonch-Osmolovskaya E, Young M, Krogh A, Peng X (2015) Comparative metagenomics of eight geographically remote terrestrial hot springs. Microb Ecol 70:411–424

    PubMed  Google Scholar 

  49. 49.

    Kojima H, Watanabe M, Fukui M (2017) Sulfuritortus calidifontis gen. Nov., sp. nov., a sulfur oxidizer isolated from a hot spring microbial mat. Int J Syst Evol Microbiol 67:1355–1358

    CAS  PubMed  Google Scholar 

  50. 50.

    Boden R, Hutt LP, Rae AW (2017) Reclassification of Thiobacillus aquaesulis (Wood & Kelly, 1995) as Annwoodia aquaesulis gen. nov., comb. nov., transfer of Thiobacillus (Beijerinck, 1904) from the Hydrogenophilales to the Nitrosomonadales, proposal of Hydrogenophilalia class. nov. within the ‘Proteobacteria’, and four new families within the orders Nitrosomonadales and Rhodocyclales. Int J Syst Evol Microbiol 67:1191–1205

    CAS  PubMed  Google Scholar 

  51. 51.

    Auernik KS, Cooper CR, Kelly RM (2008) Life in hot acid: pathway analyses in extremely thermoacidophilic archaea. Curr Opin Biotechnol 19:445–453

    CAS  PubMed  PubMed Central  Google Scholar 

  52. 52.

    Golyshina OV, Lünsdorf H, Kublanov IV, Goldenstein NI, Hinrichs KU, Golyshin PN (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

    CAS  PubMed  PubMed Central  Google Scholar 

  53. 53.

    Yasuda M, Oyaizu H, Yamagishi A, Oshima T (1995) Morphological variation of new Thermoplasma acidophilum isolates from Japanese hot springs. Appl Environ Microbiol 61:3482–3485

    CAS  PubMed  PubMed Central  Google Scholar 

  54. 54.

    Segerer A, Langworthy TA, Stetter KO (1988) Thermoplasma acidophilum and Thermoplasma volcanium sp. nov. from Solfatara fields. Syst Appl Microbiol 10:161–171

    Google Scholar 

  55. 55.

    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

    CAS  PubMed  Google Scholar 

  56. 56.

    Schleper C, Puehler G, Holz I, Gambacorta A, Janekovic D, Santarius U, Klenk HP, Zillig W (1995) Picrophilus gen. nov., fam. nov.: a novel aerobic, heterotrophic, thermoacidophilic genus and family comprising archaea capable of growth around pH 0. J Bacteriol 177:7050–7059

    CAS  PubMed  PubMed Central  Google Scholar 

  57. 57.

    Serour E, Antranikian G (2002) Novel thermoactive glucoamylases from thermoacidophilic archea Thermoplasma acidophilum, Picrophilus torridus and Picrophilus oshimae. Antonie Van Leeuwenhoek 81:73–83

    CAS  PubMed  Google Scholar 

  58. 58.

    Grégoire P, Bohli M, Cayol JL et al (2011) Caldilinea tarbellica sp. nov., a filamentous, thermophilic, anaerobic bacterium isolated from a deep hot aquifer in the Aquitaine Basin. Int J Syst Evol Microbiol 61:1436–1441

    PubMed  Google Scholar 

  59. 59.

    Sekiguchi Y, Yamada T, Hanada S et al (2003) Anaerolinea thermophila gen. Nov., sp. nov. and Caldilinea aerophila gen. nov., sp. nov., novel filamentous thermophiles that represent a previously uncultured lineage of the domain bacteria at the subphylum level. Int J Syst Evol Microbiol 53:1843–1851

    CAS  PubMed  Google Scholar 

  60. 60.

    Yamada T, Sekiguchi Y, Imachi H et al (2005) Diversity, localization, and physiological properties of filamentous microbes belonging to Chloroflexi subphylum I in mesophilic and thermophilic methanogenic sludge granules. Microbiology 71:7493–7503

    CAS  Google Scholar 

  61. 61.

    Coates JD, Ellis DJ, Gaw CV et al (1999) Geothrix fermentans gen. nov., sp. nov., a novel Fe(III)-reducing bacterium from a hydrocarbon-contaminated aquifer. Int J Syst Bacteriol 49:1615–1622

    CAS  PubMed  Google Scholar 

  62. 62.

    Fütterer O, Angelov A, Liesegang H, Gottschalk G, Schleper C, Schepers B, Dock C, Antranikian G, Liebl W (2004) Genome sequence of Picrophilus torridus and its implications for life around pH 0. Proc Natl Acad Sci 101:9091–9096

    PubMed  Google Scholar 

  63. 63.

    Lang SQ, Butterfield DA, Lilley MD, Paul Johnson H, Hedges JI (2006) Dissolved organic carbon in ridge-axis and ridge-flank hydrothermal systems. Geochim Cosmochim Acta 70:3830–3842

    CAS  Google Scholar 

  64. 64.

    Justice NB, Norman A, Brown CT, Singh A, Thomas BC, Banfield JF (2014) Comparison of environmental and isolate Sulfobacillus genomes reveals diverse carbon, sulfur, nitrogen, and hydrogen metabolisms. BMC Genomics 15:1107

    PubMed  PubMed Central  Google Scholar 

  65. 65.

    Gale NL, Beck JV (1967) Evidence for the Calvin cycle and hexose monophosphate pathway in Thiobacillus ferrooxidans. J Bacteriol 94:1052–1059

    CAS  PubMed  PubMed Central  Google Scholar 

  66. 66.

    Brysch K, Schneider C, Fuchs G, Widdel F (1987) Lithoautotrophic growth of sulfate-reducing bacteria, and description of Desulfobacterium autotrophicum gen. nov., sp. nov. Arch Microbiol 148:264–274

    CAS  Google Scholar 

  67. 67.

    Golyshina OV, Kublanov IV, Tran H, Korzhenkov AA, Lünsdorf H, Nechitaylo TY, Gavrilov SN, Toshchakov SV, Golyshin PN (2016) Biology of archaea from a novel family Cuniculiplasmataceae (Thermoplasmata) ubiquitous in hyper acidic environments. Sci Rep 6:39034

    CAS  PubMed  PubMed Central  Google Scholar 

  68. 68.

    Hedrich S, Johnson DB (2013) Aerobic and anaerobic oxidation of hydrogen by acidophilic bacteria. FEMS Microbiol Lett 349:40–45

    CAS  PubMed  Google Scholar 

  69. 69.

    Brandis A, Thauer RK (1981) Growth of Desulfovibrio species on hydrogen and sulphate as sole energy source. Microbiology 126:249–252

    CAS  Google Scholar 

  70. 70.

    Melián GV, Galindo I, Pérez NM, Hernández PA, Fernández M, Ramírez C, Mora R, Alvarado GE (2007) Diffuse emission of hydrogen from Poás Volcano, Costa Rica. América Central Pure Appl Geophys 164:2465–2487

    Google Scholar 

  71. 71.

    Weiss JV, Rentz JA, Plaia T, Neubauer SC, Merrill-Floyd M, Lilburn T, Bradburne C, Megonigal JP, Emerson D (2007) Characterization of neutrophilic Fe(II)-oxidizing bacteria isolated from the rhizosphere of wetland plants and description of Ferritrophicum radicicola gen. nov. sp. nov., and Sideroxydans paludicola sp. nov. Geomicrobiol J 24:559–570

    CAS  Google Scholar 

  72. 72.

    Compant S, Nowak J, Coenye T, Clément C, Ait Barka E (2008) Diversity and occurrence of Burkholderia spp. in the natural environment. FEMS Microbiol Rev 32:607–626

    CAS  PubMed  Google Scholar 

  73. 73.

    Mesa V, Gallego JLR, González-Gil R, Lauga B, Sánchez J, Méndez-García C, Peláez AI (2017) Bacterial, archaeal, and eukaryotic diversity across distinct microhabitats in an acid mine drainage. Front Microbiol 8:1756

    PubMed  PubMed Central  Google Scholar 

  74. 74.

    Goltsman DSA, Dasari M, Thomas BC, Shah MB, VerBerkmoes NC, Hettich RL, Banfield JF (2013) New group in the Leptospirillum clade: cultivation-independent community genomics, proteomics, and transcriptomics of the new species “Leptospirillum Group IV UBA BS.”. Appl Environ Microbiol 79:5384–5393

    CAS  PubMed  PubMed Central  Google Scholar 

  75. 75.

    Sand W, Rohde K, Sobotke B, Zenneck C (1992) Evaluation of Leptospirillum ferrooxidans for leaching. Appl Environ Microbiol 58:85–92

    CAS  PubMed  PubMed Central  Google Scholar 

  76. 76.

    Issotta F, Galleguillos PA, Moya-Beltrán A et al (2016) Draft genome sequence of chloride-tolerant Leptospirillum ferriphilum Sp-Cl from industrial bioleaching operations in Northern Chile. Stand Genomic Sci 11:1–7

    Google Scholar 

  77. 77.

    Jones RM, Johnson DB (2015) Acidithrix ferrooxidans gen. nov., sp. nov.; a filamentous and obligately heterotrophic, acidophilic member of the Actinobacteria that catalyzes dissimilatory oxido-reduction of iron. Res Microbiol 166:111–120

    CAS  PubMed  Google Scholar 

  78. 78.

    Ziegler S, Waidner B, Itoh T, Schumann P, Spring S, Gescher J (2013) Metallibacterium scheffleri gen. nov., sp. nov., an alkalinizing gammaproteobacterium isolated from an acidic biofilm. Int J Syst Evol Microbiol 63:1499–1504

    PubMed  Google Scholar 

  79. 79.

    Itoh T, Yamanoi K, Kudo T, Ohkuma M, Takashina T (2011) Aciditerrimonas ferrireducens gen. nov., sp. nov., an iron-reducing thermoacidophilic actinobacterium isolated from a solfataric field. Int J Syst Evol Microbiol 61:1281–1285

    PubMed  Google Scholar 

  80. 80.

    Selenska-Pobell S (2002) Chapter 8 diversity and activity of bacteria in uranium waste piles. Radioactivity in the environment 2:225–254

    CAS  Google Scholar 

  81. 81.

    Aguilera A, Manrubia SC, Gómez F et al (2006) Eukaryotic community distribution and its relationship to water physicochemical parameters in an extreme acidic environment, Río Tinto (Southwestern Spain). Appl Environ Microbiol 72:5325–5330

    CAS  PubMed  PubMed Central  Google Scholar 

Download references


We thank Carlos Rodriguez of Centro de Investigación en Contaminación Ambiental (CICA-UCR) for the help with the chemical analysis. We also are grateful to Solange Voysest for help with the design of some figures.


This work was supported by The Vice-rectory of Research of Universidad de Costa Rica (project number VI 809-B6-524), the Costa Rican Ministry of Science, Technology and Telecommunication (MICITT) and Federal Ministry of Education and Research (BMBF) (project VolcanZyme contract No FI-255B-17), and the ERC grant IPBSL (ERC250350-IPBSL). MM acknowledges government funding from the Transitorio I of the National Law 8488 for Emergencies and Risk Prevention in Costa Rica. F.P-S. is supported by grant IJC2018-035180-I from the Spanish Ministry of Science and Innovation.

Author information



Corresponding author

Correspondence to Max Chavarría.

Electronic Supplementary Material

Figure S1.

Alpha-diversity estimations of San Cayetano samples. Richness indicate that 63% of the samples presented richness values higher than 500 OTUs, and that 88% of the samples presented values of the Shannon index greater than 3. (PNG 3585 kb)

Figure S2.

Canonical coordination analysis (CCA) of the microbial communities in San Cayetano river. Vector fitting of environmental variables was performed to the CCA ordination. The direction and length of the vectors are determined by the envfit function in the vegan package. Only vectors with a p-value < 0.05 are shown. (PNG 2690 kb)


Rising of the San Cayetano river. The river is born in a rocky area where water emerges from the depths. (MOV 22362 kb)


(XLSX 488 kb)

High resolution image (TIF 19081 kb)

High resolution image (TIF 14313 kb)

Video S1.

Rising of the San Cayetano river. The river is born in a rocky area where water emerges from the depths. (MOV 22362 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Arce-Rodríguez, A., Puente-Sánchez, F., Avendaño, R. et al. Microbial Community Structure Along a Horizontal Oxygen Gradient in a Costa Rican Volcanic Influenced Acid Rock Drainage System. Microb Ecol (2020). https://doi.org/10.1007/s00248-020-01530-9

Download citation


  • Costa Rica
  • San Cayetano
  • Acid rock drainage
  • Microbial communities
  • Oxygen gradient