Methylotrophic methanogenesis and potential methylated substrates in marine sediment

Methane is the simplest hydrocarbon and a potent greenhouse gas that plays important roles in atmospheric chemistry, the global carbon cycle, and the formation of gas hydrates in marine sediment. Microbial production of methane is the terminal step during the degradation of organic matter. It is generally thought that methane is predominantly produced from hydrogenotrophic and acetoclastic methanogenesis, while methylotrophic methanogenesis and its relative importance for methane production in marine sediments remain largely unconstrained. The main objective of this study is to constrain potential methylated substrates and methylotrophic methanogenic activities, and further evaluate the importance of methylotrophic methanogenesis in marine sediment. As the lack of knowledge on in situ concentrations of methylated compounds impedes our understanding on their quantitative contribution to methane production, the first step was to determine the concentrations and carbon isotopic composition of methylated compounds using newly-developed methods. Quantitative or isotopic analysis of methanol, trimethylamine (TMA) and dimethylsulfide (DMS) in marine sediment and pore waters were achieved using gas chromatographic approaches in combination with a range of pretreatment techniques. Using these protocols, the concentrations and distributions of methylated compounds were determined in a variety of marine sediments from Aarhus Bay in Denmark, Orca Basin in the Gulf of Mexico and Gulf of Lions in the northwestern Mediterranean Sea. To further constrain the importance of methylotrophic methanogenesis, two case studies combining the newly-developed methods as well as various biogeochemical analyses were performed in hypersaline sediment and estuarine sediment. In hypersaline sediment of Orca Basin, multiple lines of evidences from abundances of methanogenic substrates, carbon isotope systematics between methane and substrates, thermodynamic calculations, stable isotope tracer and radiotracer experiments as well as gene and lipid biomarkers collectively confirmed that methylotrophic methanogenesis was the dominant methanogenic pathway in Orca Basin sediments. Furthermore, the distribution of methanogenic substrates, activity and diversity were characterized to quantitatively estimate the relative importance of different methanogenic pathways in estuarine sediment of the northwestern Mediterranean Sea. The results showed that both methylotrophic and hydrogenotrophic methanogenesis contributed to the formation of methane in the sulfate reduction zone, with methylotrophic methanogenesis accounting for 13%-74% of the total methane production. In the sulfate-depleted sediments, hydrogenotrophic methanogenesis dominated methanogenic pathway (67%-97%), whereas acetoclastic methanogenesis contributed up to 31% of methane production in organic-rich sediment. In contrast, the contribution of methylotrophic methanogenesis to the total methanogenic activity was negligible in the methanogenic zone (< 1%). Collectively, new constraints from methylated compounds and the metabolic activities improve our quantitative understanding on methylotrophic methanogenesis in different marine sediment settings. The findings in this thesis provide more comprehensive insights into the relative importance of methylotrophic methanogenesis in marine sediment

Microbial communities under distinct thermal and geochemical regimes in axial and off-axis sediments of Guaymas Basin

© The Author(s), 2021. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Teske, A., Wegener, G., Chanton, J. P., White, D., MacGregor, B., Hoer, D., de Beer, D., Zhuang, G., Saxton, M. A., Joye, S. B., Lizarralde, D., Soule, S. A., & Ruff, S. E. Microbial communities under distinct thermal and geochemical regimes in axial and off-axis sediments of Guaymas Basin. Frontiers in Microbiology, 12, (2021): 633649, https://doi.org/10.3389/fmicb.2021.633649.Cold seeps and hydrothermal vents are seafloor habitats fueled by subsurface energy sources. Both habitat types coexist in Guaymas Basin in the Gulf of California, providing an opportunity to compare microbial communities with distinct physiologies adapted to different thermal regimes. Hydrothermally active sites in the southern Guaymas Basin axial valley, and cold seep sites at Octopus Mound, a carbonate mound with abundant methanotrophic cold seep fauna at the Central Seep location on the northern off-axis flanking regions, show consistent geochemical and microbial differences between hot, temperate, cold seep, and background sites. The changing microbial actors include autotrophic and heterotrophic bacterial and archaeal lineages that catalyze sulfur, nitrogen, and methane cycling, organic matter degradation, and hydrocarbon oxidation. Thermal, biogeochemical, and microbiological characteristics of the sampling locations indicate that sediment thermal regime and seep-derived or hydrothermal energy sources structure the microbial communities at the sediment surface.Research on Guaymas Basin in the Teske lab is supported by NSF Molecular and cellular Biology grant 1817381 “Collaborative Research: Next generation physiology: a systems-level understanding of microbes driving carbon cycling in marine sediments”. Sampling in Guaymas Basin was supported by collaborative NSF Biological Oceanography grants 1357238 and 1357360 “Collaborative Research: Microbial carbon cycling and its interaction with sulfur and nitrogen transformations in Guaymas Basin hydrothermal sediments” to AT and SJ, respectively. SER was supported by an AITF/Eyes High Postdoctoral Fellowship and start-up funds provided by the Marine Biological Laboratory

Methylotropher Methanogenese und potentielle methylierte Substrate in marinen Sedimenten

Methane is the simplest hydrocarbon and a potent greenhouse gas that plays important roles in atmospheric chemistry, the global carbon cycle, and the formation of gas hydrates in marine sediment. Microbial production of methane is the terminal step during the degradation of organic matter. It is generally thought that methane is predominantly produced from hydrogenotrophic and acetoclastic methanogenesis, while methylotrophic methanogenesis and its relative importance for methane production in marine sediments remain largely unconstrained. The main objective of this study is to constrain potential methylated substrates and methylotrophic methanogenic activities, and further evaluate the importance of methylotrophic methanogenesis in marine sediment. As the lack of knowledge on in situ concentrations of methylated compounds impedes our understanding on their quantitative contribution to methane production, the first step was to determine the concentrations and carbon isotopic composition of methylated compounds using newly-developed methods. Quantitative or isotopic analysis of methanol, trimethylamine (TMA) and dimethylsulfide (DMS) in marine sediment and pore waters were achieved using gas chromatographic approaches in combination with a range of pretreatment techniques. Using these protocols, the concentrations and distributions of methylated compounds were determined in a variety of marine sediments from Aarhus Bay in Denmark, Orca Basin in the Gulf of Mexico and Gulf of Lions in the northwestern Mediterranean Sea. To further constrain the importance of methylotrophic methanogenesis, two case studies combining the newly-developed methods as well as various biogeochemical analyses were performed in hypersaline sediment and estuarine sediment. In hypersaline sediment of Orca Basin, multiple lines of evidences from abundances of methanogenic substrates, carbon isotope systematics between methane and substrates, thermodynamic calculations, stable isotope tracer and radiotracer experiments as well as gene and lipid biomarkers collectively confirmed that methylotrophic methanogenesis was the dominant methanogenic pathway in Orca Basin sediments. Furthermore, the distribution of methanogenic substrates, activity and diversity were characterized to quantitatively estimate the relative importance of different methanogenic pathways in estuarine sediment of the northwestern Mediterranean Sea. The results showed that both methylotrophic and hydrogenotrophic methanogenesis contributed to the formation of methane in the sulfate reduction zone, with methylotrophic methanogenesis accounting for 13%-74% of the total methane production. In the sulfate-depleted sediments, hydrogenotrophic methanogenesis dominated methanogenic pathway (67%-97%), whereas acetoclastic methanogenesis contributed up to 31% of methane production in organic-rich sediment. In contrast, the contribution of methylotrophic methanogenesis to the total methanogenic activity was negligible in the methanogenic zone (< 1%). Collectively, new constraints from methylated compounds and the metabolic activities improve our quantitative understanding on methylotrophic methanogenesis in different marine sediment settings. The findings in this thesis provide more comprehensive insights into the relative importance of methylotrophic methanogenesis in marine sediment

Microbial cell distribution in the Guaymas Basin subseafloor biosphere, a young marginal rift basin with rich organics and steep temperature gradient

&lt;p&gt;Guaymas Basin is a young marginal rift basin in the Gulf of California characterized by active seafloor spreading and rapid sediment deposition, including organic-rich sediments derived from highly productive overlying waters and terrigenous sediments from nearby continental margins. The combination of active seafloor spreading and rapid sedimentation within a narrow basin results in a dynamic environment where linked physical, chemical, and biological processes regulate the cycling of sedimentary carbon and other elements. This continuum of interrelating processes from magma to microbe motivated International Ocean Discovery Program Expedition 385 and is reflected in its title, &amp;#8220;Guaymas Basin Tectonics and Biosphere.&amp;#8221;&lt;/p&gt;&lt;p&gt;During IODP Expedition 385, organic-rich sediments with sill intrusions on the flanking regions and in the northern axial graben of Guaymas Basin (in eight sites) were drilled and core samples were recovered. Those cored samples were examined for their microbial cell abundance in a highly sensitive manner by density-gradient cell separation at the super clean room of Kochi Core Center, Japan, followed by direct counting on fluorescence microscopy. Cell abundance in surficial seafloor sediment (~10&lt;sup&gt;9&lt;/sup&gt; cells/cm&lt;sup&gt;3&lt;/sup&gt;) was roughly 1000 times higher than the bottom seawater (~10&lt;sup&gt;6&lt;/sup&gt; cells/cm&lt;sup&gt;3&lt;/sup&gt;) and gradually decreased with increasing depth and temperature. In contrast to the cell abundance profile observed at Nankai Trough (IODP Exp. 370), the gradual decrease of cell abundance was observed up to around 75&amp;#186;C, and we detected microbial cells even at hot horizons above 100&amp;#186;C.&lt;/p&gt;&lt;p&gt;We will present the overview of the microbial cell distribution in the Guaymas Basin and discuss its relation to the current and past environmental conditions, e.g., temperature and sill-intrusion, etc.&lt;/p&gt

Heat flow and thermal regime in the Guaymas Basin, Gulf of California: Estimates of conductive and advective heat transport

International audienc

Heat flow and thermal regime in the Guaymas Basin, Gulf of California: Estimates of conductive and advective heat transport

International audienc

Heat flow and thermal regime in the Guaymas Basin, Gulf of California: Estimates of conductive and advective heat transport

International audienc

Biological Sulfate Reduction in Deep Subseafloor Sediment of Guaymas Basin

Auteurs : IODP Exp. 385 Shipboard Scientific PartySulfate reduction is the quantitatively most important process to degrade organic matter in anoxic marine sediment and has been studied intensively in a variety of settings. Guaymas Basin, a young marginal ocean basin, offers the unique opportunity to study sulfate reduction in an environment characterized by organic-rich sediment, high sedimentation rates, and high geothermal gradients (100–958°C km −1 ). We measured sulfate reduction rates (SRR) in samples taken during the International Ocean Discovery Program (IODP) Expedition 385 using incubation experiments with radiolabeled 35 SO 4 2− carried out at in situ pressure and temperature. The highest SRR (387 nmol cm −3 d −1 ) was recorded in near-surface sediments from Site U1548C, which had the steepest geothermal gradient (958°C km −1 ). At this site, SRR were generally over an order of magnitude higher than at similar depths at other sites (e.g., 387–157 nmol cm −3 d −1 at 1.9 mbsf from Site U1548C vs. 46–1.0 nmol cm −3 d −1 at 2.1 mbsf from Site U1552B). Site U1546D is characterized by a sill intrusion, but it had already reached thermal equilibrium and SRR were in the same range as nearby Site U1545C, which is minimally affected by sills. The wide temperature range observed at each drill site suggests major shifts in microbial community composition with very different temperature optima but awaits confirmation by molecular biological analyses. At the transition between the mesophilic and thermophilic range around 40°C–60°C, sulfate-reducing activity appears to be decreased, particularly in more oligotrophic settings, but shows a slight recovery at higher temperatures

Carbon released by sill intrusion into young sediments measured through scientific drilling

International audienceThe intrusion of igneous sills into organic-rich sediments accompanies the emplacement of igneous provinces, continental rifting, and sedimented seafloor spreading. Heat from intruding sills in these settings alters sedimentary organic carbon, releasing methane and other gasses. Recent studies hypothesize that carbon released by this mechanism impacts global climate, particularly during large igneous province emplacements. However, the direct impacts of sill intrusion, including carbon release, remain insufficiently quantified. Here, we present results from International Ocean Discovery Program (IODP) Expedition 385 comparing drill-core and wireline measurements from correlative sedimentary strata at adjacent sites cored in Guaymas Basin, Gulf of California, one altered by a recently intruded sill and one unaffected. We estimate 3.30 Mt of carbon were released due to this sill intrusion, representing an order of magnitude less carbon than inferences from outcrops and modeling would predict. This attenuated carbon release can be attributed to shallow intrusion and the high heat capacity of young, high-porosity sediments. Shallow intrusion also impacts sub-seafloor carbon cycling by disrupting advective fluxes, and it compacts underlying sediments, increasing potential carbon release in response to subsequent intrusions