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

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 ironoxidizers (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.

Rapid shift in microbial community structure in a neutral hydrothermal hot spring from Costa Rica

“…Interestingly, the absence of iron-oxidizing bacteria (see below) can be related to the neutral pH which favors its abiotic oxidation, thus reducing the availability of electron donors for this type of bacteria (Earhart 2009; Johnson et al 2012). This is one of the clearest differences in Bajo las Peñas compared to other hot springs that we have characterized in Costa Rica (Arce-Rodríguez et al 2019, 2020), whose physicochemical characteristics are typical of ARD or VARD environments (with acidic pH), where the presence of iron oxidizers is very common.…”

“…All these observations suggest that the sulfate source in Bajo las Peñas is different from Acid Rock Drainage (ARD) and Volcanic influenced Acid Rock Drainage (VARD) environments. We have described VARD ecosystems associated with nearby Irazu Volcano’s hydrothermal system (Arce-Rodríguez et al 2020) in which the sulfate and the acidity come from the volcano hydrothermal system rather than from biological oxidation of pyrite as in ARD systems (Amils et al 2002; Arce-Rodríguez et al 2017, 2019). However, they do not seem to influence Bajo las Peñas and instead, the likely sources of sulfate are anhydrite/gypsum dissolution perhaps aided by some acid rain as the area is downwind from active Turrialba Volcano (Porowski et al 2019).…”

Out of the blue: the independent activity of sulfur-oxidizers and diatoms mediate the sudden color shift of a tropical river

“…Based on these chemical and microbiological similarities, we hypothesize that Quebrada Agria is influenced by one or more upstream hydrothermal springs akin to the one described in Arce-Rodríguez et al ., 2019). Under this scenario, sulfide originating from hydrothermal fluids would be oxidized by microbial activity (Amils et al ., 2007; Arce-Rodríguez et al ., 2020), causing a decrease in pH and high sulfate concentrations observed near the ‘Teñidero’ site. The acidity of the water would in turn promote weathering and result in extensive mobilization of dissolved silicon and aluminum (Bigham & Nordstrom, 2000).…”

“…In Quebrada Agria, hydrothermal sulfide is oxidized by bacteria such as Sulfuriferula and Sulfurimonas resulting in an acidic fluid capable of mobilizing silicates and metals such as aluminum, as has been described for other ecosystems (Bigham & Nordstrom, 2000; Amils et al ., 2007; Arce-Rodríguez et al ., 2020). Meanwhile, the partitioning of silicon in Río Buenavista is controlled by diatoms, which are in turn the most likely source for the colloidal silica particles suspended in the stream.…”

Special Issue: Diversity of Extremophiles in Time and Space

“…Great changes have been observed in both geochemistry and microbiology due to seasonality in different parts of the planet [8,9]. In addition, within these ecosystems, drastic changes in physicochemical conditions are usually generated over small distances (e.g., oxygen content and temperature [10,11]) leading to the formation of micro-niches colonized by specialized microbial communities. With this fact in mind, this Special Issue, "Diversity of Extremophiles in Time and Space", presents a series of scientific articles dedicated to the study of extremophiles but focused on space-time variations in these extreme ecosystems.…”