Arctic permafrost soils store large amounts of soil organic carbon (SOC) that could be released into the atmosphere as methane (CH ₄) in a future warmer climate. How warming affects the complex ...microbial network decomposing SOC is not understood. We studied CH ₄ production of Arctic peat soil microbiota in anoxic microcosms over a temperature gradient from 1 to 30 °C, combining metatranscriptomic, metagenomic, and targeted metabolic profiling. The CH ₄ production rate at 4 °C was 25% of that at 25 °C and increased rapidly with temperature, driven by fast adaptations of microbial community structure, metabolic network of SOC decomposition, and trophic interactions. Below 7 °C, syntrophic propionate oxidation was the rate-limiting step for CH ₄ production; above this threshold temperature, polysaccharide hydrolysis became rate limiting. This change was associated with a shift within the functional guild for syntrophic propionate oxidation, with Firmicutes being replaced by Bacteroidetes. Correspondingly, there was a shift from the formate- and H ₂-using Methanobacteriales to Methanomicrobiales and from the acetotrophic Methanosarcinaceae to Methanosaetaceae . Methanogenesis from methylamines, probably stemming from degradation of bacterial cells, became more important with increasing temperature and corresponded with an increased relative abundance of predatory protists of the phylum Cercozoa. We concluded that Arctic peat microbiota responds rapidly to increased temperatures by modulating metabolic and trophic interactions so that CH ₄ is always highly produced: The microbial community adapts through taxonomic shifts, and cascade effects of substrate availability cause replacement of functional guilds and functional changes within taxa.
Significance Microorganisms are key players in emissions of the greenhouse gas (GHG) methane from anoxic carbon-rich peat soils of the Arctic permafrost region. Although available data and modeling suggest a significant temperature-induced increase of GHG emissions from these regions by the end of this century, the controls of and interactions within the underlying microbial networks are largely unknown. This temperature-gradient study of an Arctic peat soil using integrated omics techniques reveals critical temperatures at which microbial adaptations cause changes in metabolic bottlenecks of anaerobic carbon-degradation pathways. In particular taxonomic shifts within functional guilds at different levels of the carbon degradation cascade enable a fast adaptation of the microbial system resulting in high methane emissions at all temperatures.
We provide the first detailed identification of Barents Sea cold seep frenulate hosts and their symbionts. Mitochondrial COI sequence analysis, in combination with detailed morphological ...investigations through both light and electron microscopy was used for identifying frenulate hosts, and comparing them to Oligobrachia haakonmosbiensis and Oligobrachia webbi, two morphologically similar species known from the Norwegian Sea. Specimens from sites previously assumed to host O. haakonmosbiensis were included in our molecular analysis, which allowed us to provide new insight on the debate regarding species identity of these Oligobrachia worms. Our results indicate that high Arctic seeps are inhabited by a species that though closely related to Oligobrachia haakonmosbiensis, is nonetheless distinct. We refer to this group as the Oligobrachia sp. CPL-clade, based on the colloquial names of the sites they are currently known to inhabit. Since members of the Oligobrachia sp. CPL-clade cannot be distinguished from O. haakonmosbiensis or O. webbi based on morphology, we suggest that a complex of cryptic Oligobrachia species inhabit seeps in the Norwegian Sea and the Arctic. The symbionts of the Oligobrachia sp. CPL-clade were also found to be closely related to O. haakonmosbiensis symbionts, but genetically distinct. Fluorescent in situ hybridization and transmission electron micrographs revealed extremely dense populations of bacteria within the trophosome of members of the Oligobrachia sp. CPL-clade, which is unusual for frenulates. Bacterial genes for sulfur oxidation were detected and small rod shaped bacteria (round in cross section), typical of siboglinid-associated sulfur-oxidizing bacteria, were seen on electron micrographs of trophosome bacteriocytes, suggesting that sulfide constitutes the main energy source. We hypothesize that specific, local geochemical conditions, in particular, high sulfide fluxes and concentrations could account for the unusually high symbiont densities in members of the Oligrobrachia sp. CPL-clade.
Celotno besedilo
Dostopno za:
DOBA, IZUM, KILJ, NUK, PILJ, PNG, SAZU, SIK, UILJ, UKNU, UL, UM, UPUK
The response of methanogens to thawing permafrost is an important factor for the global greenhouse gas budget. We tracked methanogenic community structure, activity, and abundance along the ...degradation of sub-Arctic palsa peatland permafrost. We observed the development of pronounced methane production, release, and abundance of functional (mcrA) methanogenic gene numbers following the transitions from permafrost (palsa) to thaw pond structures. This was associated with the establishment of a methanogenic community consisting both of hydrogenotrophic (Methanobacterium, Methanocellales), and potential acetoclastic (Methanosarcina) members and their activity. While peat bog development was not reflected in significant changes of mcrA copy numbers, potential methane production, and rates of methane release decreased. This was primarily linked to a decline of potential acetoclastic in favor of hydrogenotrophic methanogens. Although palsa peatland succession offers similarities with typical transitions from fen to bog ecosystems, the observed dynamics in methane fluxes and methanogenic communities are primarily attributed to changes within the dominant Bryophyta and Cyperaceae taxa rather than to changes in peat moss and sedge coverage, pH and nutrient regime. Overall, the palsa peatland methanogenic community was characterized by a few dominant operational taxonomic units (OTUs). These OTUs seem to be indicative for methanogenic species that thrive in terrestrial organic rich environments. In summary, our study shows that after an initial stage of high methane emissions following permafrost thaw, methane fluxes, and methanogenic communities establish that are typical for northern peat bogs.
Abstract Lakes and ponds are considered as a major natural source of CH4 emissions, particularly during the ice-free period in boreal ecosystems. Aerobic methane-oxidizing bacteria (MOB), which ...utilize CH4 using oxygen as an electron acceptor, are one of the dominant microorganisms in the CH4-rich water columns. Metagenome-assembled genomes (MAGs) have revealed the genetic potential of MOB from boreal aquatic ecosystems for various microaerobic/anaerobic metabolic functions. However, experimental proof of these functions, i.e., organic acid production via fermentation, by lake MOB is lacking. In addition, psychrophilic (i.e., cold-loving) MOB and their CH4-oxidizing process have rarely been investigated. In this study, we isolated, provided a taxonomic description, and analyzed the genome of Methylobacter sp. S3L5C, a psychrophilic MOB, from a boreal lake in Finland. Based on phylogenomic comparisons to MAGs, Methylobacter sp. S3L5C represented a ubiquitous cluster of Methylobacter spp. in boreal aquatic ecosystems. At optimal temperatures (3–12 °C) and pH (6.8–8.3), the specific growth rates (µ) and CH4 utilization rate were in the range of 0.018–0.022 h−1 and 0.66–1.52 mmol l−1 d−1, respectively. In batch cultivation, the isolate could produce organic acids, and the concentrations were elevated after replenishing CH4 and air into the headspace. Up to 4.1 mM acetate, 0.02 mM malate, and 0.07 mM propionate were observed at the end of the test under optimal operational conditions. The results herein highlight the key role of Methylobacter spp. in regulating CH4 emissions and their potential to provide CH4-derived organic carbon compounds to surrounding heterotrophic microorganisms in cold ecosystems.
Northern peatlands typically develop through succession from fens dominated by the moss family Amblystegiaceae to bogs dominated by the moss genus Sphagnum. How the different plants and abiotic ...environmental conditions provided in Amblystegiaceae and Sphagnum peat shape the respective moss associated microbial communities is unknown. Through a large-scale molecular and biogeochemical study spanning Arctic, sub-Arctic and temperate regions we assessed how the endo- and epiphytic microbial communities of natural northern peatland mosses relate to peatland type (Sphagnum and Amblystegiaceae), location, moss taxa and abiotic environmental variables. Microbial diversity and community structure were distinctly different between Amblystegiaceae and Sphagnum peatlands, and within each of these two peatland types moss taxon explained the largest part of microbial community variation. Sphagnum and Amblystegiaceae shared few (< 1% of all operational taxonomic units (OTUs)) but strikingly abundant (up to 65% of relative abundance) OTUs. This core community overlapped by one third with the Sphagnum-specific core-community. Thus, the most abundant microorganisms in Sphagnum that are also found in all the Sphagnum plants studied, are the same OTUs as those few shared with Amblystegiaceae. Finally, we could confirm that these highly abundant OTUs were endophytes in Sphagnum, but epiphytes on Amblystegiaceae. We conclude that moss taxa and abiotic environmental variables associate with particular microbial communities. While moss taxon was the most influential parameter, hydrology, pH and temperature also had significant effects on the microbial communities. A small though highly abundant core community is shared between Sphagnum and Amblystegiaceae.
Summary
The dominant terminal process of carbon mineralization in most freshwater wetlands is methanogenesis. With methane being an important greenhouse gas, the predicted warming of the Arctic may ...provide a positive feedback. However, the amount of methane released to the atmosphere may be controlled by the activity of methane‐oxidizing bacteria (methanotrophs) living in the oxic surface layer of wetlands. Previously, methanotrophs have been isolated and identified by genetic profiling in High Arctic wetlands showing the presence of only a few genotypes. Two isolates from Solvatnet (Ny‐Ålesund, Spitsbergen; 79°N) are available: Methylobacter tundripaludum (type I) and Methylocystis rosea (type II), raising the question whether the low diversity is a cultivation effect. We have revisited Solvatnet applying stable isotope probing (SIP) with 13C‐labelled methane. 16S rRNA profiling revealed active type I methanotrophs including M. tundripaludum, while no active type II methanotrophs were identified. These results indicate that the extant M. tundripaludum is an active methane oxidizer at its locus typicus; furthermore, Methylobacter seems to be the dominant active genus. Diversity of methanotrophs was low as compared, e.g. to wetland rice fields in the Mediterranean. This low diversity suggests a high vulnerability of Arctic methanotroph communities, which deserves more attention.
Methane (CH
) is a sustainable carbon feedstock for value-added chemical production in aerobic CH
-oxidizing bacteria (methanotrophs). Under substrate-limited (e.g., oxygen and nitrogen) conditions, ...CH
oxidation results in the production of various short-chain organic acids and platform chemicals. These CH
-derived products could be broadened by utilizing them as feedstocks for heterotrophic bacteria. As a proof of concept, a two-stage system for CH
abatement and 1-alkene production was developed in this study. Type I and Type II methanotrophs,
SV96 and
SV97, respectively, were investigated in batch tests under different CH
and air supplementation schemes. CH
oxidation under either microaerobic or aerobic conditions induced the production of formate, acetate, succinate, and malate in
SV96, accounting for 4.8-7.0% of consumed carbon from CH
(C-CH
), while
SV97 produced the same compounds except for malate, and with lower efficiency than
SV96, accounting for 0.7-1.8% of consumed C-CH
. For the first time, this study demonstrated the use of organic acid-rich spent media of methanotrophs cultivating engineered
ADP1 '
cells for 1-alkene production. The highest yield of 1-undecene was obtained from the spent medium of
SV96 at 68.9 ± 11.6 μmol mol C
. However, further large-scale studies on fermenters and their optimization are required to increase the production yields of organic acids in methanotrophs.
Frenulate species were identified from a high Arctic methane seep area on Vestnesa Ridge, western Svalbard margin (79°N, Fram Strait) based on mitochondrial cytochrome oxidase subunit I (mtCOI). Two ...species were found: Oligobrachia haakonmosbiensis, and a new, distinct, and undescribed Oligobrachia species. The new species adds to the cryptic Oligobrachia species complex found at high latitude methane seeps in the north Atlantic and the Arctic. However, this species displays a curled tube morphology and light brown coloration that could serve to distinguish it from other members of the complex. A number of single tentacle individuals were recovered which were initially thought to be members of the only unitentaculate genus, Siboglinum. However, sequencing revealed them to be the new species and the single tentacle morphology, in addition to thin, colorless, and ringless tubes indicate that they are juveniles. This is the first known report of juveniles of northern Oligobrachia. Since the juveniles all appeared to be at about the same developmental stage, it is possible that reproduction is either synchronized within the species, or that despite continuous reproduction, settlement, and growth in the sediment only takes place at specific periods. The new find of the well‐known species O. haakonmosbiensis extends its range from the Norwegian Sea to high latitudes of the Arctic in the Fram Strait. We suggest bottom currents serve as the main distribution mechanism for high latitude Oligobrachia species and that water depth constitutes a major dispersal barrier. This explains the lack of overlap between the distributions of northern Oligobrachia species despite exposure to similar current regimes. Our results point toward a single speciation event within the Oligobrachia clade, and we suggest that this occurred in the late Neogene, when topographical changes occurred and exchanges between Arctic and North Atlantic water masses and subsequent thermohaline circulation intensified.
The deepwater (~1,200 m depth), high Arctic (79°N) Vestnesa seep contains two frenulate species: Oligobrachia haakonmosbiensis and a potentially new species. Multitentaculate adults and unitentaculate juveniles of the new species were present. We propose that bottom currents serve as the main dispersal mechanism for high latitude frenulates, although water depth functions as a major distributional barrier.
A substantial part of the Earths' soil organic carbon (SOC) is stored in Arctic permafrost peatlands, which represent large potential sources for increased emissions of the greenhouse gases CH(4) and ...CO(2) in a warming climate. The microbial communities and their genetic repertoire involved in the breakdown and mineralisation of SOC in these soils are, however, poorly understood. In this study, we applied a combined metagenomic and metatranscriptomic approach on two Arctic peat soils to investigate the identity and the gene pool of the microbiota driving the SOC degradation in the seasonally thawed active layers. A large and diverse set of genes encoding plant polymer-degrading enzymes was found, comparable to microbiotas from temperate and subtropical soils. This indicates that the metabolic potential for SOC degradation in Arctic peat is not different from that of other climatic zones. The majority of these genes were assigned to three bacterial phyla, Actinobacteria, Verrucomicrobia and Bacteroidetes. Anaerobic metabolic pathways and the fraction of methanogenic archaea increased with peat depth, evident for a gradual transition from aerobic to anaerobic lifestyles. A population of CH(4)-oxidising bacteria closely related to Methylobacter tundripaludum was the dominating active group of methanotrophs. Based on the in-depth characterisation of the microbes and their genes, we conclude that these Arctic peat soils will turn into CO(2) sources owing to increased active layer depth and prolonged growing season. However, the extent of future CH(4) emissions will critically depend on the response of the methanotrophic bacteria.
Psychrophilic methanotrophic bacteria are abundant and play an important role in methane removal in cold methanogenic environments, such as boreal and arctic terrestrial and aquatic ecosystems. They ...could be also applied in the bioconversion of biogas and natural gas into value-added products (e.g., chemicals and single-cell protein) in cold regions. Hence, isolation and genome sequencing of psychrophilic methanotrophic bacteria are needed to provide important data on their functional capabilities. However, psychrophilic methanotroph isolates and consequently their genome sequences are rare. Fortunately, Leibniz Institute, DSMZ-German Collection of Microorganisms and Cell Cultures GmbH was able to revive the long-extinct pure culture of a psychrophilic methanotrophic tundra soil isolate, Methylobacter psychrophilus Z-0021 (DSM 9914), from their stocks during 2022. Here, we describe the de novo assembled genome sequence of Methylobacter psychrophilus Z-0021 comprising a total of 4691082 bp in 156 contigs with a G+C content of 43.1% and 4074 coding sequences. The preliminary genome annotation analysis of Z-0021 identified genes encoding oxidation of methane, methanol and formaldehyde, assimilation of carbon and nitrate, and N2 fixation. In pairwise genome-to-genome comparisons with closely related methanotrophic strains, the strain Z-0021 had an average nucleotide identity (ANI) of 92.9% and 78.2% and a digital DNA-DNA hybridization (dDDH) value of 50.6% and 22% with a recently described psychrophilic, lake isolate, Methylobacter sp. S3L5C and a psychrotrophic, arctic wetland soil isolate, Methylobacter tundripaludum SV96, respectively. In addition, the respective similarities between genomes of the strains S3L5C and SV96 were 78.1% ANI and 21.8% dDDH. Comparison to widely used ANI and dDDH thresholds to delineate unique species (<95% ANI and <70% dDDH) suggests that Methylobacter psychrophilus Z-0021, Methylobacter tundripaludum SV96 and Methylobacter sp. S3L5C are different species. The draft genome of Z-0021 has been deposited at GenBank under the accession JAOEGU000000000.
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