Evidence of cryptic methane cycling and non-methanogenic methylamine consumption in the sulfate-reducing zone of sediment in the Santa Barbara Basin, California

Abstract

Abstract. The recently discovered cryptic methane cycle in the sulfate-reducing zone of marine and wetland sediment couples methylotrophic methanogenesis to anaerobic oxidation of methane (AOM). Here we present evidence of cryptic methane cycling activity within the upper regions of the sulfate-reducing zone, along a depth transect within the Santa Barbara Basin, off the coast of California, USA. The top 0–20 cm of sediment from each station was subjected to geochemical analyses and radiotracer incubations using 35S–SO42-, 14C–mono-methylamine, and 14C–CH4 to find evidence of cryptic methane cycling. Methane concentrations were consistently low (3 to 16 µM) across the depth transect, despite AOM rates increasing with decreasing water depth (from max 0.05 nmol cm−3 d−1 at the deepest station to max 1.8 nmol cm−3 d−1 at the shallowest station). Porewater sulfate concentrations remained high (23 to 29 mM), despite the detection of sulfate reduction activity from 35S–SO42- incubations with rates up to 134 nmol cm−3 d−1. Metabolomic analysis showed that substrates for methanogenesis (i.e., acetate, methanol and methylamines) were mostly below the detection limit in the porewater, but some samples from the 1–2 cm depth section showed non-quantifiable evidence of these substrates, indicating their rapid turnover. Estimated methanogenesis from mono-methylamine ranged from 0.2 to 0.5 nmol cm−3 d−1. Discrepancies between the rate constants (k) of methanogenesis (from 14C–mono-methylamine) and AOM (from either 14C–mono-methylamine-derived 14C–CH4 or from directly injected 14C–CH4) suggest the activity of a separate, concurrent metabolic process directly metabolizing mono-methylamine to inorganic carbon. We conclude that the results presented in this work show strong evidence of cryptic methane cycling occurring within the top 20 cm of sediment in the Santa Barbara Basin. The rapid cycling of carbon between methanogenesis and methanotropy likely prevents major build-up of methane in the sulfate-reducing zone. Furthermore, our data suggest that methylamine is utilized by both methanogenic archaea capable of methylotrophic methanogenesis and non-methanogenic microbial groups. We hypothesize that sulfate reduction is responsible for the additional methylamine turnover, but further investigation is needed to elucidate this metabolic activity.

Sulfide Toxicity as Key Control on Anaerobic Oxidation of Methane in Eutrophic Coastal Sediments

“…These are conditions that could favor methanogens at potentially lower abundances in top sediments to be more active than in deeper sediments, where they could be more abundant but have less substrate availability. Additionally, the observation that the highest potential methane production rates were measured in surface sediments concomitant with relatively high sulfate concentrations suggests cryptic methane cycling, in which methane is consumed as soon as it is produced within the SMTZ, detectable via radiotracer or stable isotope studies . Methanogenesis from noncompetitive substrates is supported by our data since genomic potential for methanol and methylamine-driven methanogenesis was identified in three out of four methanogen MAGs.…”

“…Additionally, the observation that the highest potential methane production rates were measured in surface sediments concomitant with relatively high sulfate concentrations suggests cryptic methane cycling, in which methane is consumed as soon as it is produced within the SMTZ, detectable via radiotracer or stable isotope studies. 73 Methanogenesis from noncompetitive substrates is supported by our data since genomic potential for methanol and methylamine-driven methanogenesis was identified in three out of four methanogen MAGs. This could partially fuel AOM in Site 5, where the ANME-2 MAG coverage was significant (3.85×) within the SMTZ.…”

Divergent Gut Microbiota: Archaeal and Bacterial Signatures Unveil Unique Patterns in Colombian Cyclists Compared to Weightlifters and Non‐Athletes

“…[ 60–62 ] While the metabolic function of these archaeal taxa remains poorly understood, they are commonly associated with methane production in the gut. [ 63,64 ] Our findings suggest an intriguing correlation between bacterial and archaeal members through correlation networks (Figure 6B), emphasizing the need for further exploration of potential correlations between endurance athletes and methane production. Methanogenic archaea are integral components of the human gut microbiota, playing a role in methane generation through anaerobic fermentation of organic compounds.…”

Spatial evidence of cryptic methane cycling and methylotrophic metabolisms along a land-ocean transect in a California coastal wetland

“…Although sulfate reduction outcompetes methanogenesis for hydrogen and acetate in the sulfate reduction zone above the SMTZ, methylated substrates such as methylsulfides, methanol and methylamines, are known to be non-competitive for methanogenesis of the methylotrophic pathways (Oremland and Taylor, 1978;Lovley and Klug, 1986;Maltby et al, 2016;Zhuang et al, 2016;Zhuang et al, 2018;Krause and Treude, 2021;Krause et al, 2023). Thus, methylotrophic methanogenesis activity has been shown to occur within the sulfate-reducing zone in various aquatic environments, including coastal wetlands (Oremland et al, 1982;Oremland and Polcin, 1982;Krause and Treude, 2021).…”

“…Thus, methylotrophic methanogenesis activity has been shown to occur within the sulfate-reducing zone in various aquatic environments, including coastal wetlands (Oremland et al, 1982;Oremland and Polcin, 1982;Krause and Treude, 2021). However, despite the methylotrophic methanogenesis activity, methane concentrations are by several orders of magnitude lower within the sulfate-reducing zone, above the SMTZ, compared to deeper sediments where sulfate is depleted (Barnes and Goldberg, 1976;Wehrmann et al, 2011;Beulig et al, 2018;Krause et al, 2023;Krause and Treude, 2021). This low level of methane is controlled by concurrent methylotrophic methanogenesis and AOM activity which is now referred as the cryptic methane cycle, and has been detected in the marine and coastal wetland sediment (Krause and Treude, 2021;Xiao et al, 2017;Xiao et al, 2018;Krause et al, 2023).…”