Carbonate-hosted microbial communities are prolific and pervasive methane oxidizers at geologically diverse marine methane seep sites

Abstract

At marine methane seeps, vast quantities of methane move through the shallow subseafloor, where it is largely consumed by microbial communities. This process plays an important role in global methane dynamics, but we have yet to identify all of the methane sinks in the deep sea. Here, we conducted a continental-scale survey of seven geologically diverse seafloor seeps and found that carbonate rocks from all sites host methane-oxidizing microbial communities with substantial methanotrophic potential. In laboratory-based mesocosm incubations, chimney-like carbonates from the newly described Point Dume seep off the coast of Southern California exhibited the highest rates of anaerobic methane oxidation measured to date. After a thorough analysis of physicochemical, electrical, and biological factors, we attribute this substantial metabolic activity largely to higher cell density, mineral composition, kinetic parameters including an elevated Vmax, and the presence of specific microbial lineages. Our data also suggest that other features, such as electrical conductance, rock particle size, and microbial community alpha diversity, may influence a sample’s methanotrophic potential, but these factors did not demonstrate clear patterns with respect to methane oxidation rates. Based on the apparent pervasiveness within seep carbonates of microbial communities capable of performing anaerobic oxidation of methane, as well as the frequent occurrence of carbonates at seeps, we suggest that rock-hosted methanotrophy may be an important contributor to marine methane consumption.

Impact of Concurrent aerobic–anaerobic Methanotrophy on Methane Emission from Marine Sediments in Gas Hydrate Area

“…Because this K m value is higher than the dissolved methane concentration of 0.34 mM in the incubations and that of 2.0 mM in average in situ , the AOM rates in this study would not attain a maximum ( V max ) and depend on the dissolved methane concentration. Following the Michaelis–Menten equation, , the in situ AOM rates were calculated to be 71 ± 6 nmol –1 mL –1 d –1 (upper sediments) and 2.5 ± 0.4 nmol –1 mL –1 d –1 (lower sediments) based on the in situ methane concentration (Table S8). For aerobic methane oxidation, the reported K m values (<100 μM) were much lower than the methane concentrations in this study.…”

“…We used the methane oxidation potentials and in situ vertical distributions of the active methanotroph species to model the methane consumption processes of the inside microbial mat sediments. The Michaelis−Menten constants (K m ) for AOM were reported ranging between 1.1 and 37 mM, while a recent study by Marlow et al used the conservative value of 5.65 mM 50 to normalize the AOM rates at different methane concentrations assessed so far. Although it is preferential that the K m value is determined on a site-by-site basis for accurate AOM rate estimation at the specific situation, normalizing by the conservative K m is also effective for the direct comparison among the rates measured in earlier studies.…”

Significance of anaerobic oxidation of methane (AOM) in mitigating methane emission from major natural and anthropogenic sources: a review of AOM rates in recent publications

“…This trend for AOM rates, albeit weak, is consonant with the observed increased methane oxidation rates at higher methane partial pressures. 8,158,180 Regarding the fractional turnover per unit time, K (per day), those of aerobic (median ¼ 0.0025 per day, Q1-Q3: 0.00035-0.022 per day) and anoxic methanotrophs (median ¼ 0.00091 per day, Q1-Q3: 0.0003-0.011 per day) are not signicantly different (Mann-Whitney U-test, p ¼ 0.07, Fig. 7B).…”

“…For instance, a substantial difference between measured AOM rates at ambient pressure and estimated/measured values from deep water sites or ocean bottoms has been reported. 8,158,180 Specifically, the incubation of the Eckernförde Bay sediment at 10.1 MPa of methane atmosphere enriched ANME-2a/b/c and SRB, yielding an AOM rate of 0.046 μmol CO 2 cm −3 d −1 , a few times higher than that at ambient pressure. 181 Similarly, incubations simulating the in situ pressure in the deep sea with sediments collected from a cold seep in the Gulf of Mexico and a hydrothermal site in the Guaymas Basin yielded 50 mM of dissolved methane, which supported AOM at 3.6–4.8 μmol CH 4 cm −3 d −1 .…”

“…7). [150][151][152][153][154][155][156][157][158][159][160][161][162][163][164][165][166][167] Sulfate-AOM is the dominant methane oxidation pathway because sulfate is the major reactive anion in seawater. Recent data suggest that iron/ manganese oxides are only responsible for approximately 2-3% of the methane oxidized around and below the sulfatemethane transition zones (SMTZ), 165 where the sulfate-driven AOM is usually detected.…”