Niche Differentiation of Sulfate- and Iron-Dependent Anaerobic Methane Oxidation and Methylotrophic Methanogenesis in Deep Sea Methane Seeps

Abstract

Methane seeps are widespread seafloor ecosystems shaped by complex physicochemical-biological interactions over geological timescales, and seep microbiomes play a vital role in global biogeochemical cycling of key elements on Earth. However, the mechanisms underlying the coexistence of methane-cycling microbial communities remain largely elusive. Here, high-resolution sediment incubation experiments revealed a cryptic methane cycle in the South China Sea (SCS) methane seep ecosystem, showing the coexistence of sulfate (SO 4 2−)-or iron (Fe)-dependent anaerobic oxidation of methane (AOM) and methylotrophic methanogenesis. This previously unrecognized methane cycling is not discernible from geochemical profiles due to high net methane consumption. High-throughput sequencing and Catalyzed Reporter Deposition-Fluorescence in situ Hybridization (CARD-FISH) results suggested that anaerobic methane-oxidizing archaea (ANME)-2 and-3 coupled to sulfatereducing bacteria (SRB) carried out SO 4 2−-AOM, and alternative ANME-2 and-3 solely or coupled to iron-reducing bacteria (IRB) might participate in Fe-AOM in sulfate-depleted environments. This finding suggested that ANME could alter AOM metabolic pathways according to geochemical changes. Furthermore, the majority of methylotrophic methanogens belonged to Methanimicrococcus, and hydrogenotrophic and acetoclastic methanogens were likely inhibited by sulfate or iron respiration. Fe-AOM and methylotrophic methanogenesis are overlooked potential sources and sinks of methane in methane seep ecosystems, thus influencing methane budgets and even the global carbon budget in the ocean.

Anthropogenic and Environmental Constraints on the Microbial Methane Cycle in Coastal Sediments

“…Therefore, methylotrophic methanogenesis may be an important but previously overlooked methane source in coastal shallow sediments (Conrad, 2020), and trimethylamine, dimethylsulfide, and dimethylsulfoniopropionate may be more common methanogenic substrates in marine sediments than currently thought (Zhuang et al, 2017), especially under higher salinity. Methylotrophic methanogens can co-exist with acetogens, SRB and ANME in OMZ sediments (Bhattacharya et al, 2020) and deep sea methane seeps (Li et al, 2020;Xu et al, 2020), and methanogenesis in the sulfate-reducing zone has been identified in coastal sediments (Maltby et al, 2016). However, whether these microorganisms compete for the same substrates or exist in separate niches remains unclear.…”

Distinct Bottom-Water Bacterial Communities at Methane Seeps With Various Seepage Intensities in Haima, South China Sea

“…Although microbial community structures have been investigated at cold seeps in the SCS, nearly all the reports have focused on seepage-affected sediments (Lai et al, 2007;Zhang et al, 2012;Niu et al, 2017;Wu et al, 2018;Cui et al, 2019Cui et al, , 2020Zhuang et al, 2019;Li et al, 2020). Recently, Zhang et al (2020) investigate prokaryotes along the depth profile of the water column.…”

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 ,...…”

“…The least studied ANME group is ANME-3. ANME-3 has been found mainly in marine ecosystems, including submarine mud volcanoes, deep-marine seeps, shallow and coastal sediments [ 3 , 6 , 7 , 26 , 34 , 35 , 36 , 37 ]. There is a single study report on the detection of ANME-3 in basaltic and granitic rock samples from the deep terrestrial subsurface [ 38 ].…”

“…There are some indications that ANME-3 archaea could oxidize methane without a bacterial partner, probably due to direct electron transfer to Fe(III) or sulfate [ 35 , 36 ]. Nevertheless, the association of ANME-3 archaea with sulfate-reducing bacteria has also been demonstrated [ 37 ]. The reconstruction of the ANME-3 metabolism is hampered by the lack of the genomic data, which are still represented by only a small genome fragment in the fosmid library [ 39 ].…”