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Archaea belonging to the phylum Bathyarchaeota are the predominant archaeal species in cold, anoxic marine sediments and additionally occur in a variety of habitats, both natural and man-made. Metagenomic and single-cell sequencing studies suggest that Bathyarchaeota may have a significant impact on the emissions of greenhouse gases into the atmosphere, either through direct production of methane or through the degradation of complex organic matter that can subsequently be converted into methane. This is especially relevant in permafrost regions where climate change leads to thawing of permafrost, making high amounts of stored carbon bioavailable. Here we present the analysis of nineteen draft genomes recovered from a sediment core metagenome of the Polar Fox Lagoon, a thermokarst lake located on the Bykovsky Peninsula in Siberia, Russia, which is connected to the brackish Tiksi Bay. We show that the Bathyarchaeota in this lake are predominantly peptide degraders, producing reduced ferredoxin from the fermentation of peptides, while degradation pathways for plant-derived polymers were found to be incomplete. Several genomes encoded the potential for acetogenesis through the Wood-Ljungdahl pathway, but methanogenesis was determined to be unlikely due to the lack of genes encoding the key enzyme in methanogenesis, methyl-CoM reductase. Many genomes lacked a clear pathway for recycling reduced ferredoxin. Hydrogen metabolism was also hardly found: one type 4e [NiFe] hydrogenase was annotated in a single MAG and no [FeFe] hydrogenases were detected. Little evidence was found for syntrophy through formate or direct interspecies electron transfer, leaving a significant gap in our understanding of the metabolism of these organisms.
The release of greenhouse gases from the large organic carbon stock in permafrost deposits in the circumarctic regions may accelerate global warming upon thaw. The extent of this positive climate feedback is thought to be largely controlled by the microbial degradability of the organic matter preserved in these sediments. In addition, weathering and oxidation processes may release inorganic carbon preserved in permafrost sediments as CO2, which is generally not accounted for. We used C-13 and C-14 analysis and isotopic mass balances to differentiate and quantify organic and inorganic carbon released as CO2 in the field from an active retrogressive thaw slump of Pleistocene-age Yedoma and during a 1.5-years incubation experiment. The results reveal that the dominant source of the CO2 released from freshly thawed Yedoma exposed as thaw mound is Pleistocene-age organic matter (48-80%) and to a lesser extent modern organic substrate (3-34%). A significant portion of the CO2 originated from inorganic carbon in the Yedoma (17-26%). The mixing of young, active layer material with Yedoma at a site on the slump floor led to the preferential mineralization of this young organic carbon source. Admixtures of younger organic substrates in the Yedoma thaw mound were small and thus rapidly consumed as shown by lower contributions to the CO2 produced during few weeks of aerobic incubation at 4 degrees C corresponding to approximately one thaw season. Future CO2 fluxes from the freshly thawed Yedoma will contain higher proportions of ancient inorganic (22%) and organic carbon (61-78%) as suggested by the results at the end, after 1.5 years of incubation. The increasing contribution of inorganic carbon during the incubation is favored by the accumulation of organic acids from microbial organic matter degradation resulting in lower pH values and, in consequence, in inorganic carbon dissolution. Because part of the inorganic carbon pool is assumed to be of pedogenic origin, these emissions would ultimately not alter carbon budgets. The results of this study highlight the preferential degradation of younger organic substrates in freshly thawed Yedoma, if available, and a substantial release of CO2 from inorganic sources.
Permafrost thaw subjects previously frozen soil organic carbon (SOC) to microbial degradation to the greenhouse gases carbon dioxide (CO2) and methane (CH4). Emission of these gases constitutes a positive feedback to climate warming. Among numerous uncertainties in estimating the strength of this permafrost carbon feedback (PCF), two are: (i) how mineralization of permafrost SOC thawed in saturated anaerobic conditions responds to changes in temperature and (ii) how microbial communities and temperature sensitivities change over time since thaw. To address these uncertainties, we utilized a thermokarst-lake sediment core as a natural chronosequence where SOC thawed and incubated in situ under saturated anaerobic conditions for up to 400 years following permafrost thaw. Initial microbial communities were characterized, and sediments were anaerobically incubated in the lab at four temperatures (0 °C, 3 °C, 10 °C, and 25 °C) bracketing those observed in the lake's talik. Net CH4 production in freshly-thawed sediments near the downward-expanding thaw boundary at the base of the talik were most sensitive to warming at the lower incubation temperatures (0 °C to 3 °C), while the overlying sediments which had been thawed for centuries had initial low abundant methanogenic communities (< 0.02%) and did not experience statistically significant increases in net CH4 production potentials until higher incubation temperatures (10 °C to 25 °C). We propose these observed differences in temperature sensitivities are due to differences in SOM quality and functional microbial community composition that evolve over time; however further research is necessary to better constrain the roles of these factors in determining temperature controls on anaerobic C mineralization.
Sulfate deprivation triggers high methane production in a disturbed and rewetted coastal peatland
(2019)
In natural coastal wetlands, high supplies of marine sulfate suppress methanogenesis. Coastal wetlands are, however, often subject to disturbance by diking and drainage for agricultural use and can turn to potent methane sources when rewetted for remediation. This suggests that preceding land use measures can suspend the sulfate-related methane suppressing mechanisms. Here, we unravel the hydrological relocation and biogeochemical S and C transformation processes that induced high methane emissions in a disturbed and rewetted peatland despite former brackish impact. The underlying processes were investigated along a transect of increasing distance to the coastline using a combination of concentration patterns, stable isotope partitioning, and analysis of the microbial community structure. We found that diking and freshwater rewetting caused a distinct freshening and an efficient depletion of the brackish sulfate reservoir by dissimilatory sulfate reduction (DSR). Despite some legacy effects of brackish impact expressed as high amounts of sedimentary S and elevated electrical conductivities, contemporary metabolic processes operated mainly under sulfate-limited conditions. This opened up favorable conditions for the establishment of a prospering methanogenic community in the top 30-40 cm of peat, the structure and physiology of which resemble those of terrestrial organic-rich environments. Locally, high amounts of sulfate persisted in deeper peat layers through the inhibition of DSR, probably by competitive electron acceptors of terrestrial origin, for example Fe(III). However, as sulfate occurred only in peat layers below 30-40 cm, it did not interfere with high methane emissions on an ecosystem scale. Our results indicate that the climate effect of disturbed and remediated coastal wetlands cannot simply be derived by analogy with their natural counterparts. From a greenhouse gas perspective, the re-exposure of diked wetlands to natural coastal dynamics would literally open up the floodgates for a replenishment of the marine sulfate pool and therefore constitute an efficient measure to reduce methane emissions.
The rewetting of drained peatlands alters peat geochemistry and often leads to sustained elevated methane emission. Although this methane is produced entirely by microbial activity, the distribution and abundance of methane-cycling microbes in rewetted peatlands, especially in fens, is rarely described. In this study, we compare the community composition and abundance of methane-cycling microbes in relation to peat porewater geochemistry in two rewetted fens in northeastern Germany, a coastal brackish fen and a freshwater riparian fen, with known high methane fluxes. We utilized 16S rRNA high-throughput sequencing and quantitative polymerase chain reaction (qPCR) on 16S rRNA, mcrA, and pmoA genes to determine microbial community composition and the abundance of total bacteria, methanogens, and methanotrophs. Electrical conductivity (EC) was more than 3 times higher in the coastal fen than in the riparian fen, averaging 5.3 and 1.5 mS cm(-1), respectively. Porewater concentrations of terminal electron acceptors (TEAs) varied within and among the fens. This was also reflected in similarly high intra- and inter-site variations of microbial community composition. Despite these differences in environmental conditions and electron acceptor availability, we found a low abundance of methanotrophs and a high abundance of methanogens, represented in particular by Methanosaetaceae, in both fens. This suggests that rapid (re) establishment of methanogens and slow (re) establishment of methanotrophs contributes to prolonged increased methane emissions following rewetting.
Permafrost thaw subjects previously frozen organic carbon (OC) to microbial decomposition, generating the greenhouse gases (GHG) carbon dioxide (CO2) and methane (CH4) and fueling a positive climate feedback. Over one quarter of permafrost OC is stored in deep, ice-rich Pleistocene-aged yedoma permafrost deposits. We used a combination of anaerobic incubations, microbial sequencing, and ultrahigh-resolution mass spectrometry to show yedoma OC biolability increases with depth along a 12-m yedoma profile. In incubations at 3 degrees C and 13 degrees C, GHG production per unit OC at 12-versus 1.3-m depth was 4.6 and 20.5 times greater, respectively. Bacterial diversity decreased with depth and we detected methanogens at all our sampled depths, suggesting that in situ microbial communities are equipped to metabolize thawed OC into CH4. We concurrently observed an increase in the relative abundance of reduced, saturated OC compounds, which corresponded to high proportions of C mineralization and positively correlated with anaerobic GHG production potentials and higher proportions of OC being mineralized as CH4. Taking into account the higher global warming potential (GWP) of CH4 compared to CO2, thawed yedoma sediments in our study had 2 times higher GWP at 12-versus 9.0-m depth at 3 degrees C and 15 times higher GWP at 13 degrees C. Considering that yedoma is vulnerable to processes that thaw deep OC, our findings imply that it is important to account for this increasing GHG production and GWP with depth to better understand the disproportionate impact of yedoma on the magnitude of the permafrost carbon feedback.
Microbial community composition and abundance after millennia of submarine permafrost warming
(2019)
Warming of the Arctic led to an increase in permafrost temperatures by about 0.3 degrees C during the last decade. Permafrost warming is associated with increasing sediment water content, permeability, and diffusivity and could in the long term alter microbial community composition and abundance even before permafrost thaws. We studied the long-term effect (up to 2500 years) of submarine permafrost warming on microbial communities along an onshore-offshore transect on the Siberian Arctic Shelf displaying a natural temperature gradient of more than 10 degrees C. We analysed the in situ development of bacterial abundance and community composition through total cell counts (TCCs), quantitative PCR of bacterial gene abundance, and amplicon sequencing and correlated the microbial community data with temperature, pore water chemistry, and sediment physicochemical parameters. On timescales of centuries, permafrost warming coincided with an overall decreasing microbial abundance, whereas millennia after warming microbial abundance was similar to cold onshore permafrost. In addition, the dissolved organic carbon content of all cores was lowest in submarine permafrost after millennial-scale warming. Based on correlation analysis, TCC, unlike bacterial gene abundance, showed a significant rank-based negative correlation with increasing temperature, while bacterial gene copy numbers showed a strong negative correlation with salinity. Bacterial community composition correlated only weakly with temperature but strongly with the pore water stable isotopes delta O-18 and delta D, as well as with depth. The bacterial community showed substantial spatial variation and an overall dominance of Actinobacteria, Chloroflexi, Firmicutes, Gemmatimonadetes, and Proteobacteria, which are amongst the microbial taxa that were also found to be active in other frozen permafrost environments. We suggest that, millennia after permafrost warming by over 10 degrees C, microbial community composition and abundance show some indications for proliferation but mainly reflect the sedimentation history and paleoenvironment and not a direct effect through warming.
Permafrost thaw liberates frozen organic carbon, which is decomposed into carbon dioxide (CO2) and methane (CH4). The release of these greenhouse gases (GHGs) forms a positive feedback to atmospheric CO2 and CH4 concentrations and accelerates climate change(1,2). Current studies report a minor importance of CH4 production in water-saturated (anoxic) permafrost soils(3-6) and a stronger permafrost carbon-climate feedback from drained (oxic) soils(1,7). Here we show through seven-year laboratory incubations that equal amounts of CO2 and CH4 are formed in thawing permafrost under anoxic conditions after stable CH4-producing microbial communities have established. Less permafrost carbon was mineralized under anoxic conditions but more CO2-carbon equivalents (CO2Ce) were formed than under oxic conditions when the higher global warming potential (GWP) of CH4 is taken into account(8). A model of organic carbon decomposition, calibrated with the observed decomposition data, predicts a higher loss of permafrost carbon under oxic conditions (113 +/- 58 g CO2-C kgC(-1) (kgC, kilograms of carbon)) by 2100, but a twice as high production of CO2-Ce (241 +/- 138 g CO2-Ce kgC(-1)) under anoxic conditions. These findings challenge the view of a stronger permafrost carbon-climate feedback from drained soils1,7 and emphasize the importance of CH4 production in thawing permafrost on climate-relevant timescales.
Since the beginning of the Anthropocene, lacustrine biodiversity has been influenced by climate change and human activities. These factors advance the spread of harmful cyanobacteria in lakes around the world, which affects water quality and impairs the aquatic food chain. In this study, we assessed changes in cyanobacterial community dynamics via sedimentary DNA (sedaDNA) from well-dated lake sediments of Lake Tiefer See, which is part of the Klocksin Lake Chain spanning the last 350 years. Our diversity and community analysis revealed that cyanobacterial communities form clusters according to the presence or absence of varves. Based on distance-based redundancy and variation partitioning analyses (dbRDA and VPA) we identified that intensified lake circulation inferred from vegetation openness reconstructions, delta C-13 data (a proxy for varve preservation) and total nitrogen content were abiotic factors that significantly explained the variation in the reconstructed cyanobacterial community from Lake Tiefer See sediments. Operational taxonomic units (OTUs) assigned to Microcystis sp. and Aphanizomenon sp. were identified as potential eutrophication-driven taxa of growing importance since circa common era (ca. CE) 1920 till present. This result is corroborated by a cyanobacteria lipid biomarker analysis. Furthermore, we suggest that stronger lake circulation as indicated by non-varved sediments favoured the deposition of the non-photosynthetic cyanobacteria sister clade Sericytochromatia, whereas lake bottom anoxia as indicated by subrecent- and recent varves favoured the Melainabacteria in sediments. Our findings highlight the potential of high-resolution amplicon sequencing in investigating the dynamics of past cyanobacterial communities in lake sediments and show that lake circulation, anoxic conditions, and human-induced eutrophication are main factors explaining variations in the cyanobacteria community in Lake Tiefer See during the last 350 years.
As the Arctic coast erodes, it drains thermokarst lakes, transforming them into lagoons, and, eventually, integrates them into subsea permafrost. Lagoons represent the first stage of a thermokarst lake transition to a marine setting and possibly more saline and colder upper boundary conditions. In this research, borehole data, electrical resistivity surveying, and modeling of heat and salt diffusion were carried out at Polar Fox Lagoon on the Bykovsky Peninsula, Siberia. Polar Fox Lagoon is a seasonally isolated water body connected to Tiksi Bay through a channel, leading to hypersaline waters under the ice cover. The boreholes in the center of the lagoon revealed floating ice and a saline cryotic bed underlain by a saline cryotic talik, a thin ice-bearing permafrost layer, and unfrozen ground. The bathymetry showed that most of the lagoon had bedfast ice in spring. In bedfast ice areas, the electrical resistivity profiles suggested that an unfrozen saline layer was underlain by a thick layer of refrozen talik. The modeling showed that thermokarst lake taliks can refreeze when submerged in saltwater with mean annual bottom water temperatures below or slightly above 0 degrees C. This occurs, because the top-down chemical degradation of newly formed ice-bearing permafrost is slower than the refreezing of the talik. Hence, lagoons may precondition taliks with a layer of ice-bearing permafrost before encroachment by the sea, and this frozen layer may act as a cap on gas migration out of the underlying talik.