Steep redox gradient and biogeochemical cycling driven by deeply sourced fluids and gases in a terrestrial mud volcano

Abstract

Mud volcanoes provide an accessible channel through which deep subsurface environments can be observed. The manner in which deeply sourced materials shape biogeochemical processes and microbial communities in such geological features remains largely unknown. This study characterized redox transitions, biogeochemical fluxes and microbial communities for samples collected from a methane-rich mud volcano in southwestern Taiwan. Our results indicated that oxygen penetration was confined within the upper 4 mm of fluids/muds and counteracted by the oxidation of pyrite, dissolved sulfide, methane and organic matter at various degrees. Beneath the oxic zone, anaerobic sulfur oxidation, sulfate reduction, anaerobic methanotrophy and methanogenesis were compartmentalized into different depths in the pool periphery, forming a metabolic network that efficiently cycles methane and sulfur. Community members affiliated with various Proteobacteria capable of aerobic oxidation of sulfur, methane and methyl compounds were more abundant in the anoxic zone with diminished sulfate and high methane. These findings suggest either the requirement of alternative electron acceptors or a persistent population that once flourished in the oxic zone. Overall, this study demonstrates the distribution pattern for a suite of oxidative and reductive metabolic reactions along a steep redox gradient imposed by deep fluids in a mud volcano ecosystem.

Sulfur and Methane-Oxidizing Microbial Community in a Terrestrial Mud Volcano Revealed by Metagenomics

“…In some mud volcanoes, such interactions could lead to geochemical and metabolic stratification forming the upper sulfate-rich oxic and lower methane-rich anoxic zones, harboring distinct bacterial and archaeal communities [ 14 ]. For example, in a methane-rich mud volcano in southwestern Taiwan, oxygen penetration was limited to the upper 4 mm layer of the fluids and counteracted by the oxidation of sulfide, methane, and organic matter [ 16 ]. However, in the mud volcano we studied, the active release of gases and bubbling created conditions for mud mixing in the crater, at least at the depth from which the samples have been acquired (10–20 cm).…”

“…Microbial communities associated with mud volcanoes located at the seafloor have been extensively studied [ 7 , 8 , 9 , 10 , 11 , 12 ]. More limited number of studies has focused on microbial communities in terrestrial mud volcanoes [ 13 , 14 , 15 , 16 , 17 , 18 , 19 ]. These studies revealed that archaeal communities are mostly composed of methanogens and anaerobic methanotrophs (ANME), while bacterial communities are more diverse and consist of members of various phyla.…”

“…These studies revealed that archaeal communities are mostly composed of methanogens and anaerobic methanotrophs (ANME), while bacterial communities are more diverse and consist of members of various phyla. Among them, sulfate-reducing bacteria, presumably originating from deep subsurface fluids, were found at various terrestrial mud volcano sites [ 14 , 16 , 17 , 18 , 20 ]. Sulfate-reducers can form syntrophic consortia with anaerobic methanotrophic archaea (ANME) performing anaerobic oxidation of methane (AOM) [ 8 , 21 ].…”

Stochastic process determines the spatial variations in microbial community inhabiting terrestrial mud volcanoes across the Eurasian continent

“…For a geographic scale larger than tens of kilometers, dispersal through groundwater transport would be essentially absent. This limitation, combined with enormous oxidative power driven by the atmospheric oxygen (Lin et al, 2018) renders the terrestrial MVs ideal for investigating whether any biogeographic pattern imposed by geographic isolation and environmental contexts emerges. In addition to various spatial scales, environmental and redox contexts vary substantially along a vertical scale.…”

Deep-Sourced Fluids From a Convergent Margin Host Distinct Subseafloor Microbial Communities That Change Upon Mud Flow Expulsion

“…In flows aged 1–2 years from the Håkon Mosby MV (Barents Sea), communities dominated by aerobic methanotrophic bacteria were identified as an initial successional stage (Ruff et al, 2018). Diffusion of electron acceptors, such as oxygen and sulfate, into fresh flows can be inhibited by upward transport of MV-derived mud breccia and reduced fluids (Niemann et al, 2006), but nevertheless is understood to drive a suite of redox-stratified microbial metabolisms that occur with increasing depth: aerobic oxidation of sulfide, sulfate reduction, anaerobic methane oxidation (AOM), and methanogenesis (Lin et al, 2018). Whether microbial communities across active MVs respond similarly to fluid expulsion is not known, given the considerable heterogeneity of fluid sources and compositions (Mazzini and Etiope, 2017).…”