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Abstract
Biomineralized ferric oxide microbial mats are ubiquitous features on Earth, are common in hot springs of Yellowstone National Park (YNP, WY, USA), and form due to direct interaction between microbial and physicochemical processes. The overall goal of this study was to determine the contribution of different community members to the assembly and succession of acidic high-temperature Fe(III)-oxide mat ecosystems. Spatial and temporal changes in Fe(III)-oxide accretion and the abundance of relevant community members were monitored over 70 days using sterile glass microscope slides incubated in the outflow channels of two acidic geothermal springs (pH = 3–3.5; temperature = 68–75°C) in YNP. Hydrogenobaculum spp. were the most abundant taxon identified during early successional stages (4–40 days), and have been shown to oxidize arsenite, sulfide, and hydrogen coupled to oxygen reduction. Iron-oxidizing populations of Metallosphaera yellowstonensis were detected within 4 days, and reached steady-state levels within 14–30 days, corresponding to visible Fe(III)-oxide accretion. Heterotrophic archaea colonized near 30 days, and emerged as the dominant functional guild after 70 days and in mature Fe(III)-oxide mats (1–2 cm thick). First-order rate constants of Fe(III)-oxide accretion ranged from 0.046 to 0.05 day−1, and in situ microelectrode measurements showed that the oxidation of Fe(II) is limited by the diffusion of O2 into the Fe(III)-oxide mat. The formation of microterracettes also implicated O2 as a major variable controlling microbial growth and subsequent mat morphology. The assembly and succession of Fe(III)-oxide mat communities follows a repeatable pattern of colonization by lithoautotrophic organisms, and the subsequent growth of diverse organoheterotrophs. The unique geochemical signatures and micromorphology of extant biomineralized Fe(III)-oxide mats are also useful for understanding other Fe(II)-oxidizing systems.
Highlights
Microbial mat communities are ubiquitous geobiological features in contemporary and past environments on Earth, are often stratified due to gradients in key geochemical constituents, and often leave biological signatures preserved in the rock record
The primary objectives of the current study were to (i) determine the spatiotemporal dynamics of key community members involved in Fe(III)-oxide mat assembly in acidic geothermal springs of Norris Geyser Basin (YNP), (ii) quantify the amount of Fe(III)-oxides accreted and oxygen consumed in situ as a function of time, (iii) monitor temporal changes in community composition using 16S rRNA gene sequencing, and (iv) integrate laboratory measurements and field observations across different scales to develop a conceptual model of Fe(III)-oxide assembly and succession
Coccus-shaped archaea were identified at early time points using both scanning electron microscopy (SEM) and fluorescence in situ hybridization (FISH) (Figure 3), but were considerably less abundant than Hydrogenobaculum spp. (Figures 2, 3)
Summary
Microbial mat communities are ubiquitous geobiological features (e.g., stromatolites; Riding, 1999) in contemporary and past environments on Earth, are often stratified due to gradients in key geochemical constituents (e.g., oxygen; de Beer et al, 1994; Bernstein et al, 2013), and often leave biological signatures (biomarkers) preserved in the rock record (e.g., lipids; Peters and Moldowan, 1993). Biogeochemical stratification of microbial mats may produce distinct morphological features that can be preserved (e.g., iron formations and marine carbonates), and provide insights into past geochemical and hydrodynamic conditions (e.g., Kappler and Straub, 2005; Fouke, 2011). Understanding mechanisms of assembly and succession in modern-day mat communities provides clues regarding past environmental conditions and biogeophysical controls that lead to the biomineralization of specific solid phases (Reid et al, 2000; Fouke, 2011). Microorganisms may gain energy via the oxidation of Fe(II) to Fe(III) under aerobic or anaerobic conditions, which usually results in the precipitation of insoluble solid-phase Fe(III)-oxides (Konhauser, 1998, 2006; Kappler and Straub, 2005; Ehrlich and Newman, 2009; Emerson, 2012). Low pH (
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