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Methane is a major greenhouse gas and a key component of global biogeochemical cycles. Microbial methane often deviates from isotope and isotopolog equilibrium in surface environments but approaches equilibrium in deep subsurface sediments. The origin of this near-equilibrium isotopic signature in methane, whether directly produced by methanogens or achieved through anaerobic oxidation of methane (AOM), remains uncertain. Here, we show that, in the absence of AOM, microbial methane produced from deep-sea sediments exhibits isotopolog compositions approaching thermodynamic equilibrium due to energy limitation. In contrast, microbial methane from salt marsh and thermokarst lakes exhibits significant hydrogen and clumped isotopic disequilibrium due to high free-energy availability. We propose that clumped isotopologs of methane provide a proxy for characterizing the bioenergetics of environments for methane production. Together, these observations demonstrate methane clumped isotopes as a powerful tool to better understand the relation between methane metabolisms and the energy landscape in natural environments. 

Abstract. Despite long-standing interest in the biogeochemistry of the Santa Barbara Basin (SBB), there are no direct rate measurements of different nitrogen transformation processes. We investigated benthic nitrogen cycling using in situ incubations with 15NO3- addition and quantified the rates of total nitrate (NO3-) uptake, denitrification, anaerobic ammonia oxidation (anammox), N2O production, and dissimilatory nitrate reduction to ammonia (DNRA). Denitrification was the dominant NO3- reduction process, while anammox contributed 0 %–27 % to total NO3- reduction. DNRA accounted for less than half of NO3- reduction except at the deepest station at the center of the SBB where NO3- concentration was lowest. NO3- availability and sediment total organic carbon content appeared to be two key controls on the relative importance of DNRA. The increasing importance of fixed N retention via DNRA relative to fixed N loss as NO3- deficit intensifies suggests a negative feedback loop that potentially contributes to stabilizing the fixed N budget in the SBB. Nitrous oxide (N2O) production as a fraction of total NO3- reduction ranged from 0.2 % to 1.5 %, which was higher than previous reports from nearby borderland basins. A large fraction of NO3- uptake was unaccounted for by NO3- reduction processes, suggesting that intracellular storage may play an important role. Our results indicate that the SBB acts as a strong sink for fixed nitrogen and potentially a net source of N2O to the water column. 

ABSTRACT Marine macroalgae produce abundant and diverse polysaccharides, which contribute substantially to the organic matter exported to the deep ocean. Microbial degradation of these polysaccharides plays an important role in the turnover of macroalgal biomass. Various members of thePlanctomycetes-Verrucomicrobia-Chlamydia(PVC) superphylum are degraders of polysaccharides in widespread anoxic environments. In this study, we isolated a novel anaerobic bacterial strain NLcol2^Tfrom microbial mats on the surface of marine sediments offshore Santa Barbara, CA, USA. Based on 16S ribosomal RNA (rRNA) gene and phylogenomic analyses, strain NLcol2^Trepresents a novel species within thePontiellagenus in theKiritimatiellotaphylum (within the PVC superphylum). Strain NLcol2^Tis able to utilize various monosaccharides, disaccharides, and macroalgal polysaccharides such as agar and ɩ-carrageenan. A near-complete genome also revealed an extensive metabolic capacity for anaerobic degradation of sulfated polysaccharides, as evidenced by 202 carbohydrate-active enzymes (CAZymes) and 165 sulfatases. Additionally, its ability of nitrogen fixation was confirmed by nitrogenase activity detected during growth on nitrogen-free medium, and the presence of nitrogenases (nifDKH) encoded in the genome. Based on the physiological and genomic analyses, this strain represents a new species of bacteria that may play an important role in the degradation of macroalgal polysaccharides and with relevance to the biogeochemical cycling of carbon, sulfur, and nitrogen in marine environments. Strain NLcol2^T(= DSM 113125^T= MCCC 1K08672^T) is proposed to be the type strain of a novel species in thePontiellagenus, and the namePontiella agarivoranssp. nov. is proposed.IMPORTANCEGrowth and intentional burial of marine macroalgae is being considered as a carbon dioxide reduction strategy but elicits concerns as to the fate and impacts of this macroalgal carbon in the ocean. Diverse heterotrophic microbial communities in the ocean specialize in these complex polymers such as carrageenan and fucoidan, for example, members of theKiritimatiellotaphylum. However, only four type strains within the phylum have been cultivated and characterized to date, and there is limited knowledge about the metabolic capabilities and functional roles of related organisms in the environment. The new isolate strain NLcol2^Texpands the known substrate range of this phylum and further reveals the ability to fix nitrogen during anaerobic growth on macroalgal polysaccharides, thereby informing the issue of macroalgal carbon disposal. 

Abstract. 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 9.9 µM). 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. 

Abstract. The trace metal iron (Fe) is an essential micronutrient that controls phytoplankton productivity, which subsequently affects organic matter cycling with feedback on the cycling of macronutrients. Along the continental margin of the US West Coast, high benthic Fe release has been documented, in particular from deep anoxic basins in the Southern California Borderland. However, the influence of this Fe release on surface primary production remains poorly understood. In the present study from the Santa Barbara Basin, in situ benthic Fe fluxes were determined along a transect from shallow to deep sites in the basin. Fluxes ranged between 0.23 and 4.9 mmol m−2 d−1, representing some of the highest benthic Fe fluxes reported to date. To investigate the influence of benthic Fe release from the oxygen-deficient deep basin on surface phytoplankton production, we combined benthic flux measurements with numerical simulations using the Regional Ocean Modeling System coupled to the Biogeochemical Elemental Cycling (ROMS-BEC) model. For this purpose, we updated the model Fe flux parameterization to include the new benthic flux measurements from the Santa Barbara Basin. Our simulations suggest that benthic Fe fluxes enhance surface primary production, supporting a positive feedback on benthic Fe release by decreasing oxygen in bottom waters. However, a reduction in phytoplankton Fe limitation by enhanced benthic fluxes near the coast may be partially compensated for by increased nitrogen limitation further offshore, limiting the efficacy of this positive feedback. 

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. 

Fungi in terrestrial environments are known to play a key role in carbon and nitrogen biogeochemistry and exhibit high diversity. In contrast, the diversity and function of fungi in the ocean has remained underexplored and largely neglected. In the eastern tropical North Pacific oxygen minimum zone, we examined the fungal diversity by sequencing the internal transcribed spacer region 2 (ITS2) and mining a metagenome dataset collected from the same region. Additionally, we coupled 15N-tracer experiments with a selective inhibition method to determine the potential contribution of marine fungi to nitrous oxide (N2O) production. Fungal communities evaluated by ITS2 sequencing were dominated by the phyla Basidiomycota and Ascomycota at most depths. However, the metagenome dataset showed that about one third of the fungal community belong to early-diverging phyla. Fungal N2O production rates peaked at the oxic–anoxic interface of the water column, and when integrated from the oxycline to the top of the anoxic depths, fungi accounted for 18–22% of total N2O production. Our findings highlight the limitation of ITS-based methods typically used to investigate terrestrial fungal diversity and indicate that fungi may play an active role in marine nitrogen cycling.