ALBERT

Description: 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.

Description: The Santa Barbara Basin naturally experiences transient deoxygenation due to its unique geological setting in the southern California Borderland and seasonal changes in ocean currents. Long-term measurements of the basin showed that anoxic events and subsequent nitrate exhaustion in the bottom waters have been occurring more frequently and lasting longer over the past decade. One characteristic of the Santa Barbara Basin is the seasonal development of extensive mats of benthic nitrate-reducing sulfur-oxidizing bacteria, which are found at the sediment-water interface when the basin's bottom waters reach anoxia but still provide some nitrate. To assess the mat's impact on the benthic and pelagic redox environment, we collected biogeochemical sediment and benthic flux data in November 2019, after anoxia developed in the deepest waters of the basin and dissolved nitrate was depleted (down to 9.9μM). We found that the development of mats was associated with a shift from denitrification to dissimilatory nitrate reduction to ammonium. The zone of sulfate reduction appeared near the sediment-water interface in sediment hosting these ephemeral white mats. We found that an exhaustion of iron oxides in the surface sediment was an additional prerequisite for mat proliferation. Our research further suggests that cycles of deoxygenation and reoxygenation of the benthic environment result in extremely high benthic fluxes of dissolved iron from the basin's sediment. This work expands our understanding of nitrate-reducing sulfur-oxidizing mats and their role in sustaining and potentially expanding marine anoxia.