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 (SO42–)- 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 sulfate-reducing bacteria (SRB) carried out SO42–-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.
Highlights
Methane seeps are methane-dependent chemosynthetic ecosystems (Paull et al, 1984) that occur widely in the marine environment, and are considered some of the richest benthic ecosystems on the seabed (Valentine, 2011)
The rapid decrease in sulfate concentration as well as increase in DIC and methane concentrations indicate that the Sulfate-methane transition zone (SMTZ) in Jiaolong methane seep area is shallow, within 6 cm below the sediment-water interface
We compared the archaeal and bacterial diversity of the Jiaolong methane seep with those of 23 globally distributed methane seeps, and found that the microbial richness of the Jiaolong methane seep was at a medium level
Summary
Methane seeps are methane-dependent chemosynthetic ecosystems (Paull et al, 1984) that occur widely in the marine environment, and are considered some of the richest benthic ecosystems on the seabed (Valentine, 2011). The produced methane continuously seeps or erupts from the sedimentary subsurface to the seabed in the form of methane-rich fluids, and more than 90% of the methane is consumed by anaerobic methane-oxidizing archaea (Valentine, 2011), forming an efficient methane biofilter that prevents its diffusion into the seawater. Previous studies believed that in the ocean, the majority of methane is oxidized anaerobically by anaerobic methaneoxidizing archaea (ANME) coupled with sulfate reduction (Boetius et al, 2000). Targeted enrichment with ferrihydrite provides strong evidence for AOM coupled with iron reduction, and ANME-1, Methanococcoides/ANME-3 (Beal et al, 2009), ANME-2a and -2c (Scheller et al, 2016), ANME2d (Methanoperedens nitroreducens) (Ettwig et al, 2016; Shen et al, 2019), Candidatus Methanoperedens ferrireducens (Cai et al, 2018), and Methanosarcina acetivorans (Yan et al, 2018) might be involved in Fe-AOM. Bar-Or et al (2017) highlighted the essential role of methanogens and methanotrophic bacteria in the process of Fe-AOM
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