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

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Microbial Community Structure Along a Horizontal Oxygen Gradient in a Costa Rican Volcanic Influenced Acid Rock Drainage System See discussions, stats, and author profiles for this publication at: https://www.researchgate.net/publication/342362476 Microbial Community Structure Along a Horizontal Oxygen Gradient in a Costa Rican Volcanic Influenced Acid Rock Drainage System Article in Microbial Ecology · June 2020 DOI: 10.1007/s00248-020-01530-9 CITATIONS READS 0 91 9 authors, including: Alejandro Arce Rodríguez Fernando Puente-Sánchez Helmholtz Centre for Infection Research National Center for Biotechnology (CNB) 21 PUBLICATIONS 422 CITATIONS 51 PUBLICATIONS 271 CITATIONS SEE PROFILE SEE PROFILE Roberto Avendaño Eduardo Libby National Center for Biotechnological Innovations (CENIBiot) University of Costa Rica 11 PUBLICATIONS 72 CITATIONS 42 PUBLICATIONS 1,473 CITATIONS SEE PROFILE SEE PROFILE Some of the authors of this publication are also working on these related projects: Políticas de Ciencia, Tecnología e Innovación View project Biodiversity and Ecology of Aquatic Fungi and Oomycetes View project All content following this page was uploaded by Max Chavarría on 30 June 2020. The user has requested enhancement of the downloaded file. Microbial Ecology https://doi.org/10.1007/s00248-020-01530-9 ENVIRONMENTAL MICROBIOLOGY Microbial Community Structure Along a Horizontal Oxygen Gradient in a Costa Rican Volcanic Influenced Acid Rock Drainage System Alejandro Arce-Rodríguez1,2 & Fernando Puente-Sánchez3 & Roberto Avendaño4 & Eduardo Libby5 & Raúl Mora-Amador6,7 & Keilor Rojas-Jimenez8 & María Martínez9 & Dietmar H. Pieper1 & Max Chavarría4,5,10 Received: 27 June 2019 /Accepted: 17 May 2020 # Springer Science+Business Media, LLC, part of Springer Nature 2020 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 ~ 8–293gkg−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 distri- bution 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. Keywords Costa Rica . San Cayetano . Acid rock drainage . Microbial communities . Oxygen gradient Electronic supplementary material The online version of this article (https://doi.org/10.1007/s00248-020-01530-9) contains supplementary material, which is available to authorized users. * Max Chavarría 6 Escuela Centroamericana de Geología, Universidad de Costa Rica, [email protected] San José 11501-2060, Costa Rica 7 Laboratorio de Ecología Urbana, Universidad Estatal a Distancia, 1 Microbial Interactions and Processes Research Group, Helmholtz San José 11501-2060, Costa Rica Centre for Infection Research, 38124 Braunschweig, Germany 8 2 Present address: Department of Molecular Bacteriology, Helmholtz Escuela de Biología, Universidad de Costa Rica, San Centre for Infection Research, 38124 Braunschweig, Germany José 11501-2060, Costa Rica 3 Systems Biology Program, Centro Nacional de Biotecnología 9 Observatorio Vulcanológico y Sismológico de Costa Rica, (CNB-CSIC), C/Darwin 3, 28049 Madrid, Spain Universidad Nacional (OVSICORI-UNA), Heredia 2386-3000, 4 Centro Nacional de Innovaciones Biotecnológicas (CENIBiot), Costa Rica CeNAT-CONARE, San José 1174-1200, Costa Rica 10 Centro de Investigaciones en Productos Naturales (CIPRONA), 5 Escuela de Química, Universidad de Costa Rica, San Universidad de Costa Rica, Sede Central, San Pedro de Montes de José 11501-2060, Costa Rica Oca, San José 11501-2060, Costa Rica Arce-Rodríguez A. et al. Introduction Natural ARD environments are characterized by the pres- ence of iron- and sulfur-oxidizing bacteria. For example, in The study of acid rock drainage (ARD) sites has provided a the natural ARD formed in the Pastoruri Glacier area, the wealth of information about microbial populations adapted to presence of Acidithiobacillus, a sulfur- and iron-oxidizing ac- extreme acidic environments. Most of the known ARD eco- idophilic bacteria, was detected [6]. Dold et al. [7]reportedthe systems in the world have been caused by human activity, formation of an ARD system in the Antarctic landmass due to especially mining processes [1–5]. ARD environments the activity of psychrophilic acid mine drainage microorgan- resulting from the exposure of metallic sulfide ores to the isms found in cold climates, specifically Acidithiobacillus atmosphere due to mining activities are referred to as acid ferrivorans,andThiobacillus plumbophilus. Similarly, studies mine drainage (AMD) sites, while the term ARD is usually of ARD-like environments at Yellowstone National Park [16] reserved for systems that are naturally originated. The anthro- and active volcanoes like Copahue in the Andes [15] have pogenic influence modifies the geology, hydrology, and biol- shown many parallels to ARD sites where iron- and sulfur- ogy of the AMD, making it difficult to pinpoint the inherent oxidizing microorganisms also predominated. geochemical and natural microbiological conditions of these The iron cycle is one of the most important biochemical sites. It is therefore interesting from an ecological and evolu- processes that take place in these environments where micro- tionary point of view to study ARD ecosystems without an- organisms in oxic niches can oxidize ferrous iron with oxygen thropogenic influence. Unfortunately, there are far less studies to generate metabolic energy. Microorganisms can also reduce on the geochemistry and microbiology of pristine natural ferric iron (or its minerals) to ferrous iron using organic matter ARD systems, for example, the Pastoruri Glacier area in [17]. At the origin of ARD’s like the Tinto river, dominant Huascarán National Park (Perú) [6], the Antarctic landmass organisms such as Acidithiobacillus and Leptospirillum act as [7], and the Tinto river (in Spanish Río Tinto), located at the primary producers obtaining energy from aerobic Fe(II) oxi- Iberian Pyrite Belt (IPB) of Spain [8–11]. In the latter case, dation to Fe(III) complex oxides [10]. However, once anaer- although the river and its source are located on a site that has obic conditions are established in the sediments (or in deep, been mined for thousands of years [12, 13], it has been pro- unmixed water), those same oxides can be used as electron posed that the conditions of extreme acidity and heavy metal acceptors for reduced organic matter or other electron sources pollution along the river are due to natural processes that were by Acidiphilium, Acidimicrobium, Ferrimicrobium,and operative before mining activities began [12, 13]. With the Ferroplasma [10], completing the iron cycle. notable exception of the Tinto river, access to such remote Being part of the Pacific Ring of Fire, Costa Rica’svolca- locations hampers their study. noes have plenty of acidic volcanic lakes and rivers amenable Besides these natural ARD sites, which are clearly as- for study [18]. In the country, multiple extreme environments sociated with the oxidation of sulfide minerals (mostly py- with different physicochemical characteristics can be found, rite), there are terrestrial acidic waters associated with hy- which fortunately do not have anthropogenic influence [4, 14, drothermal springs or volcanic activity where H2Soxida- 18]. Our group’s first incursion into these local ARD-like sites tion or SO2 reaction with water produce sulfuric acid and was the study of the mineral-laden Sucio river (in Spanish Río whose geochemistry resemble ARD or AMD sites. These Sucio due to abundant yellowish schwertmannite precipita- ARD-like environments share most of their natural compo- tion). Here, we found a striking abundance of Gallionella sition (low pH, high sulfate, and presence of metals such as (44%) and Ferrovaceae (33%) species [14]. Our result com- iron) with that of ARD sites and are of interest because pares well with studies in the Tinto river where 80% of the they can be unequivocally assigned to natural causes [14, water column’s bacterial species corresponds to only three 15]. In order to differentiate these locations from the ARD bacterial genera: Leptospirillum, Acidithiobacillus,and sites, we refer to these sites as volcanic acid rock drainage Acidiphilium, all involved
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