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

Abstract

Mud volcanoes are prominent geological structures where fluids and gases from the deep subsurface are discharged along a fracture network in tectonically active regions. Microbial communities responsible for sulfur and methane cycling and organic transformation in terrestrial mud volcanoes remain poorly characterized. Using a metagenomics approach, we analyzed the microbial community of bubbling fluids retrieved from an active mud volcano in eastern Crimea. The microbial community was dominated by chemolithoautotrophic Campylobacterota and Gammaproteobacteria, which are capable of sulfur oxidation coupled to aerobic and anaerobic respiration. Methane oxidation could be enabled by aerobic Methylococcales bacteria and anaerobic methanotrophic archaea (ANME), while methanogens were nearly absent. The ANME community was dominated by a novel species of Ca. Methanoperedenaceae that lacked nitrate reductase and probably couple methane oxidation to the reduction of metal oxides. Analysis of two Ca. Bathyarchaeota genomes revealed the lack of mcr genes and predicted that they could grow on fatty acids, sugars, and proteinaceous substrates performing fermentation. Thermophilic sulfate reducers indigenous to the deep subsurface, Thermodesulfovibrionales (Nitrospirae) and Ca. Desulforudis (Firmicutes), were found in minor amounts. Overall, the results obtained suggest that reduced compounds delivered from the deep subsurface support the development of autotrophic microorganisms using various electron acceptors for respiration.

Diversity and Metabolic Potential of the Terrestrial Mud Volcano Microbial Community with a High Abundance of Archaea Mediating the Anaerobic Oxidation of Methane

“…The 16S rRNA gene phylogeny ( Supplementary Figure S1a ) demonstrates that this microorganism is closely related to ANME-3 archaea detected in Haakon Mosby mud volcano, deep-sea sediments of Monterey Canyon, and some other habitats [ 3 , 4 , 79 ]. The mcrA gene of KA19 ( Supplementary Figure S1b ) phylogenetically belongs to «group f» cluster previously found to be associated with ANME-3 microorganisms [ 4 , 5 , 6 , 7 , 8 , 9 , 10 , 11 , 12 , 13 , 14 , 15 , 16 , 17 , 18 , 19 , 20 , 21 , 22 , 23 , 24 , 25 , 26 , 27 , 28 , 29 , 30 , 31 , 32 , 33 , 34 , 35 , 36 , 37 , 38 , 39 , 40 , 41 , 42 , 43 , 44 , 45 , 46 , 47 , 48 , 49 , 50 , 51 ,...…”

“…Apparently in the members of Ca. Methanoperedenaceae, MHC are involved in the reduction of insoluble Fe(III) or Mn(IV) oxides [ 24 , 32 , 33 ]. The presence of MHC in ANME-3 has not been reported.…”

“…MAGs of Phaeovulum, Sulfurimonas, “Thiohalomonadaceae” and Trueperaceae encode complete or almost complete pathways for CO 2 fixation and are most likely autotrophic microorganisms. The presence of Sulfurimonas has been noted in TMVs [ 24 ]. Sulfurimonas crateris was isolated from Taman TMV in anoxic conditions; it can grow by oxidation of HS − , S 0 and S 2 O 3 2− coupled to denitrification [ 93 ].…”

“…Microorganisms of terrestrial mud volcanoes have been investigated to a relatively small extent, a number of TMVs located in the areas of mud volcanism in Romania, Italy, Azerbaijan, Taiwan, China, Trinidad and Russia were inspected in relation to microbial community composition and abundance [ 13 , 14 , 15 , 16 , 17 , 18 , 19 , 20 , 21 , 22 ]. Metagenomic approaches were applied to explore the prokaryotic diversity of TMV only recently [ 23 , 24 ].…”

Assessment of Temporal Effects of a Mud Volcanic Eruption on the Bacterial Community and Their Predicted Metabolic Functions in the Mud Volcanic Sites of Niaosong, Southern Taiwan

“…Currently, studying the microbial communities existing in mud volcanoes has received more attention due to their impact on the global methane cycle [4,5]. The mud volcanic fluids ejected from the reservoir may be geothermally heated; thus, the microorganisms with higher temperature and salinity tolerance can thrive better in these environments [4,6].…”