Microbial Community Composition and Functional Capacity in a Terrestrial Ferruginous, Sulfate-Depleted Mud Volcano

Abstract

Terrestrial mud volcanoes (MVs) are an important natural source of methane emission. The role of microbial processes in methane cycling and organic transformation in such environments remains largely unexplored. In this study, we aim to uncover functional potentials and community assemblages across geochemical transitions in a ferruginous, sulfate-depleted MV of eastern Taiwan. Geochemical profiles combined with 16S rRNA gene abundances indicated that anaerobic oxidation of methane (AOM) mediated by ANME-2a group coincided with iron/manganese reduction by Desulfuromonadales at shallow depths deprived of sulfate. The activity of AOM was stimulated either by methane alone or by methane and a range of electron acceptors, such as sulfate, ferrihydrite, and artificial humic acid. Metagenomic analyses revealed that functional genes for AOM and metal reduction were more abundant at shallow intervals. In particular, genes encoding pili expression and electron transport through multi-heme cytochromes were prevalent, suggesting potential intercellular interactions for electron transport involved in AOM. For comparison, genes responsible for methanogenesis and degradation of chitin and plant-derived molecules were more abundant at depth. The gene distribution combined with the enhanced proportions of 16S rRNA genes related to methanogens and heterotrophs, and geochemical characteristics suggest that particulate organic matter was degraded into various organic entities that could further fuel in situ methanogenesis. Finally, genes responsible for aerobic methane oxidation were more abundant in the bubbling pool and near-surface sediments. These methane oxidizers account for the ultimate attenuation of methane discharge into the atmosphere. Overall, our results demonstrated that various community members were compartmentalized into stratified niches along geochemical gradients. These community members form a metabolic network that cascades the carbon transformation from the upstream degradation of recalcitrant organic carbon with fermentative production of labile organic entities and methane to downstream methane oxidation and metal reduction near the surface. Such a metabolic architecture enables effective methane removal under ferruginous, sulfate-depleted conditions in terrestrial MVs.

Rates and Microbial Players of Iron-Driven Anaerobic Oxidation of Methane in Methanic Marine Sediments

“…Their increase (ca. 5%) in relative 16S rRNA gene sequence abundance over 250 days is in tandem with the observed iron reduction detected by measuring dissolved iron over time (Supplementary Figure S8), and thus, they might serve as potential iron oxide-reducing partner bacteria in AOM (Chang et al, 2012;Tu et al, 2017). Besides the Desulfuromonadales, unclassified Gammaproteobacteria were highly stimulated compared to day 0 across all incubations in both geochemical zones (Supplementary Figure S9).…”

“…In terrestrial mud volcanoes where Fe-AOM is also suggested to occur, high correlation between gene copies of Desulfuromonadales and ANME-2a was taken as indication for ANME-2a to oxidize methane with Desulfuromonadales as iron oxide reducing partners (Chang et al, 2012;Tu et al, 2017). While dissimilatory iron oxide reducers (e.g., Desulfuromonadales) have not been clearly shown to act as partners for ANMEs, the increased relative abundance of Desulfuromonadales 16S rRNA genes (Figure 5B) cannot be ignored.…”

“…In addition to sulfate-coupled AOM (S-AOM), the role of other electron acceptors as additional sinks for methane in marine sediments is not fully established. Metal oxides such as those of iron and manganese have been suggested to serve as additional electron acceptors in AOM (Beal et al, 2009) in a number of terrestrial, coastal and marine environments (Sivan et al, 2011;Chang et al, 2012;Wankel et al, 2012;Segarra et al, 2013;Riedinger et al, 2014;Treude et al, 2014;Egger et al, 2015Egger et al, , 2016aEgger et al, ,b, 2017Oni et al, 2015;Ettwig et al, 2016;Rooze et al, 2016;Scheller et al, 2016;Bar-Or et al, 2017;Martinez-Cruz et al, 2017;Tu et al, 2017;Cai et al, 2018). To date, only few highly enriched cultures from freshwater sediments exist, in which Candidatus 'Methanoperedens nitroreducens' and Ca.…”

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

“…Although these primers have been reported to be less efficient in generating archaeal amplicons (Parada et al 2016), they were used to facilitate the comparison with other studies. The schemes and reagents for PCR and downstream processing of amplicons were the same as those described in Tu et al (2017).…”

Geological degassing enhances microbial metabolism in the continental subsurface

“…At hydrothermal vents, chemolithoautotrophs initiate the microbial trophic network and proliferate at high rates leading to high microbial cell numbers 1 . While volcanic sites and hydrothermal vent fields have been studied fairly thoroughly regarding their microbiome and the microbial activity 25,26,27,28,29 , little is known about deep subsurface ecosystems with low temperatures but heavy impact from gases released from the mantle.…”