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

  • Environmental Microbiology
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Abstract

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.

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Acknowledgments

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.

Funding

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.

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Author notes

  1. Alejandro Arce-Rodríguez

    Present address: Department of Molecular Bacteriology, Helmholtz Centre for Infection Research, 38124, Braunschweig, Germany

Authors and Affiliations

  1. Microbial Interactions and Processes Research Group, Helmholtz Centre for Infection Research, 38124, Braunschweig, Germany

    Alejandro Arce-Rodríguez & Dietmar H. Pieper

  2. Systems Biology Program, Centro Nacional de Biotecnología (CNB-CSIC), C/Darwin 3, 28049, Madrid, Spain

    Fernando Puente-Sánchez

  3. Centro Nacional de Innovaciones Biotecnológicas (CENIBiot), CeNAT-CONARE, San José, 1174-1200, Costa Rica

    Roberto Avendaño & Max Chavarría

  4. Escuela de Química, Universidad de Costa Rica, San José, 11501-2060, Costa Rica

    Eduardo Libby & Max Chavarría

  5. Escuela Centroamericana de Geología, Universidad de Costa Rica, San José, 11501-2060, Costa Rica

    Raúl Mora-Amador

  6. Laboratorio de Ecología Urbana, Universidad Estatal a Distancia, San José, 11501-2060, Costa Rica

    Raúl Mora-Amador

  7. Escuela de Biología, Universidad de Costa Rica, San José, 11501-2060, Costa Rica

    Keilor Rojas-Jimenez

  8. Observatorio Vulcanológico y Sismológico de Costa Rica, Universidad Nacional (OVSICORI-UNA), Heredia, 2386-3000, Costa Rica

    María Martínez

  9. Centro de Investigaciones en Productos Naturales (CIPRONA), Universidad de Costa Rica, Sede Central, San Pedro de Montes de Oca, San José, 11501-2060, Costa Rica

    Max Chavarría

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  1. Alejandro Arce-Rodríguez
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Correspondence to Max Chavarría.

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(XLSX 488 kb)

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)

High resolution image (TIF 19081 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)

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)

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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 80, 793–808 (2020). https://doi.org/10.1007/s00248-020-01530-9

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  • DOI: https://doi.org/10.1007/s00248-020-01530-9

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