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ABSTRACT Methane emission feedbacks in wetlands are predicted to influence global climate under climate change and other anthropogenic stressors. Herein, we review the taxonomy and physiological ecology of the microorganisms responsible for methane production in peatlands. Common in peat soils are five of the eight described orders of methanogens spanning three phyla (Euryarchaeota, Halobacterota and Thermoplasmatota). The phylogenetic affiliation of sequences found in peat suggest that members of the thus-far-uncultivated group Candidatus Bathyarchaeota (representing a fourth phylum) may be involved in methane cycling, either anaerobic oxidation of methane and/or methanogenesis, as at least a few organisms within this group contain the essential gene, mcrA, according to metagenomic data. Methanogens in peatlands are notoriously challenging to enrich and isolate; thus, much remains unknown about their physiology and how methanogen communities will respond to environmental changes. Consistent patterns of changes in methanogen communities have been reported across studies in permafrost peatland thaw where the resulting degraded feature is thermokarst. However much remains to be understood regarding methanogen community feedbacks to altered hydrology and warming in other contexts, enhanced atmospheric pollution (N, S and metals) loading and direct anthropogenic disturbances to peatlands like drainage, horticultural peat extraction, forestry and agriculture, as well as post-disturbance reclamation. Peat-forming wetlands and peatland microorganisms that produce the greenhouse gas methane.

A taste for acid Microbiologists have succeeded in culturing the most acid-loving methanogen ever discovered. The new species, a member of the Methanomicrobiales group, was found in McLean Bog in New York State. It grows at a preferred pH of around 5, beating the previous record-holder, Methanobacterium espanolae , which has an optimum pH of between 5.5 and 6.0. Although some other methanogens can survive a pH as low as 4.5, the new species is the first to show growth and optimal methanogenesis in such acidic conditions. Microbes living in acidic soils are important sources of atmospheric methane, which is linked to global warming. Acidic peatlands are among the largest natural sources of atmospheric methane and harbour a large diversity of methanogenic Archaea 1 . Despite the ubiquity of methanogens in these peatlands, indigenous methanogens capable of growth at acidic pH values have resisted culture and isolation 2 , 3 , 4 ; these recalcitrant methanogens include members of an uncultured family-level clade in the Methanomicrobiales prevalent in many acidic peat bogs in the Northern Hemisphere 1 , 5 , 6 . However, we recently succeeded in obtaining a mixed enrichment culture of a member of this clade 7 . Here we describe its isolation and initial characterization. We demonstrate that the optimum pH for methanogenesis by this organism is lower than that of any previously described methanogen.

ABSTRACT Peatlands both accumulate carbon and release methane, but their broad range in environmental conditions means that the diversity of microorganisms responsible for carbon cycling is still uncertain. Here, we describe a community analysis of methanogenic archaea responsible for methane production in 17 peatlands from 36 to 53 N latitude across the eastern half of North America, including three metal-contaminated sites. Methanogenic community structure was analysed through Illumina amplicon sequencing of the mcrA gene. Whether metal-contaminated sites were included or not, metal concentrations in peat were a primary driver of methanogenic community composition, particularly nickel, a trace element required in the F430 cofactor in methyl-coenzyme M reductase that is also toxic at high concentrations. Copper was also a strong predictor, likely due to inhibition at toxic levels and/or to cooccurrence with nickel, since copper enzymes are not known to be present in anaerobic archaea. The methanogenic groups Methanocellales and Methanosarcinales were prevalent in peatlands with low nickel concentrations, while Methanomicrobiales and Methanomassiliicoccales were abundant in peatlands with higher nickel concentrations. Results suggest that peat-associated trace metals are predictors of methanogenic communities in peatlands. Nickel and copper concentrations, pH, temperature, water table and percentage coverage of Sphagnum mosses strongly influence methanogenic communities in 17 peatlands along a latitudinal gradient in eastern North America.

Cave ecosystems are carbon limited and thus are particularly susceptible to anthropogenic pollution. Yet, how carbon quality and quantity that can modulate the pathways and amount of Mn cycling in caves remains largely unknown. To explore Mn cycling, baseline bacterial, archaeal, and fungal communities associated with Mn(III/IV) oxide deposits were assessed in both relatively ‘pristine’ and anthropogenically impacted caves in the Appalachian Mountains (USA). Cave sites were then amended with various carbon sources that are commonly associated with anthropogenic input to determine whether they stimulate biotic Mn(II) oxidation in situ. Results revealed patterns between sites that had long-term exogenous carbon loading compared to sites that were relatively ‘pristine,’ particularly among Bacteria and Archaea. Carbon treatments that stimulated Mn(II) oxidation at several sites resulted in significant changes to the microbial communities, indicating that anthropogenic input can not only enhance biotic Mn(II) oxidation, but also shape community structure and diversity. Additional carbon sources amended with copper were incubated at various cave sites to test the role that Cu(II) plays in in situ biotic Mn(II) oxidation. Media supplemented with 100 µM Cu(II) inhibited bacterial Mn(II) oxidation but stimulated fungal Mn(II) oxidation, implicating fungal use of multicopper oxidase (MCO) enzymes but bacterial use of superoxide to oxidize Mn(II). In sites with low C:N ratios, the activity of the Mn(II) oxidizing enzyme manganese peroxidase (MnP) appears to be limited (particularly by MnPutilizing Basidiomycetes and/or Zygomycetes).

Peatlands of all latitudes play an integral role in global climate change by serving as a carbon sink and a primary source of atmospheric methane; however, the microbial ecology of mid-latitude peatlands is vastly understudied. Herein, next generation Illumina amplicon sequencing of small subunit rRNA genes was utilized to elucidate the microbial communities in three southern Appalachian peatlands. In contrast to northern peatlands, Proteobacteria dominated over Acidobacteria in all three sites. An average of 11 bacterial phyla was detected at relative abundance values >1%, with three candidate divisions (OP3, WS3 and NC10) represented, indicating high phylogenetic diversity. Physiological traits of isolates within the candidate alphaproteobacterial order, Ellin 329, obtained here and in previous studies indicate that bacteria of this order may be involved in hydrolysis of poly-, di- and monosaccharides. Community analyses indicate that Ellin 329 is the third most abundant order and is most abundant near the surface layers where plant litter decomposition should be primarily occurring. In sum, members of Ellin 329 likely play important roles in organic matter decomposition, in southern Appalachian peatlands and should be investigated further in other peatlands and ecosystem types. A new order of bacteria, Ellin 329, are abundant in peatlands and may contribute to the decomposition of organic matter and subsequent release of methane to the atmosphere.

In order to identify bacteria that assimilate dissolved inorganic carbon (DIC) in the northeast Pacific Ocean, stable isotope probing (SIP) experiments were conducted on water collected from 3 different sites off the Oregon and Washington coasts in May 2010, and one site off the Oregon Coast in September 2008 and March 2009. Samples were incubated in the dark with 2 mM (13)C-NaHCO(3), doubling the average concentration of DIC typically found in the ocean. Our results revealed a surprising diversity of marine bacteria actively assimilating DIC in the dark within the Pacific Northwest coastal waters, indicating that DIC fixation is relevant for the metabolism of different marine bacterial lineages, including putatively heterotrophic taxa. Furthermore, dark DIC-assimilating assemblages were widespread among diverse bacterial classes. Alphaproteobacteria, Gammaproteobacteria, and Bacteroidetes dominated the active DIC-assimilating communities across the samples. Actinobacteria, Betaproteobacteria, Deltaproteobacteria, Planctomycetes, and Verrucomicrobia were also implicated in DIC assimilation. Alteromonadales and Oceanospirillales contributed significantly to the DIC-assimilating Gammaproteobacteria within May 2010 clone libraries. 16S rRNA gene sequences related to the sulfur-oxidizing symbionts Arctic96BD-19 were observed in all active DIC assimilating clone libraries. Among the Alphaproteobacteria, clones related to the ubiquitous SAR11 clade were found actively assimilating DIC in all samples. Although not a dominant contributor to our active clone libraries, Betaproteobacteria, when identified, were predominantly comprised of Burkholderia. DIC-assimilating bacteria among Deltaproteobacteria included members of the SAR324 cluster. Our research suggests that DIC assimilation is ubiquitous among many bacterial groups in the coastal waters of the Pacific Northwest marine environment and may represent a significant metabolic process.

Standing dead trees (snags) are recognized for their influence on methane (CH4) cycling in coastal wetlands, yet the biogeochemical processes that control the magnitude and direction of fluxes across the snag-atmosphere interface are not fully elucidated. Herein, we analyzed microbial communities and fluxes at one height from ten snags in a ghost forest wetland. Snag-atmosphere CH4 fluxes were highly variable (− 0.11–0.51 mg CH4 m−2 h−1). CH4 production was measured in three out of ten snags; whereas, CH4 consumption was measured in two out of ten snags. Potential CH4 production and oxidation in one core from each snag was assayed in vitro. A single core produced CH4 under anoxic and oxic conditions, at measured rates of 0.7 and 0.6 ng CH4 g−1 h−1, respectively. Four cores oxidized CH4 under oxic conditions, with an average rate of − 1.13 ± 0.31 ng CH4 g−1 h−1. Illumina sequencing of the V3/V4 region of the 16S rRNA gene sequence revealed diverse microbial communities and indicated oxidative decomposition of deadwood. Methanogens were present in 20% of the snags, with a mean relative abundance of < 0.0001%. Methanotrophs were identified in all snags, with a mean relative abundance of 2% and represented the sole CH4-cycling communities in 80% of the snags. These data indicate potential for microbial attenuation of CH4 emissions across the snag-atmosphere interface in ghost forests. A better understanding of the environmental drivers of snag-associated microbial communities is necessary to forecast the response of CH4 cycling in coastal ghost forest wetlands to a shifting coastal landscape.

Abstract Two methanogenic cultures were enriched from acidic peat soil using a growth medium buffered to c. pH 5. One culture, 6A, was obtained from peat after incubation with H2/CO2, whereas culture NTA was derived from a 10−4 dilution of untreated peat into a modified medium. 16S rRNA gene clone libraries from each culture contained one methanogen and two bacterial sequences. The methanogen 16S rRNA gene sequences were 99% identical with each other and belonged to the novel ‘R-10/Fen cluster’ family of the Methanomicrobiales, whereas their mcrA sequences were 96% identical. One bacterial 16S rRNA gene sequence from culture 6A belonged to the Bacteroidetes and showed 99% identity with sequences from methanogenic enrichments from German and Russian bogs. The other sequence belonged to the Firmicutes and was identical to a thick rod-shaped citrate-utilizing organism isolated from culture 6A, the numbers of which decreased when the Ti (III) chelator was switched from citrate to nitrilotriacetate. Bacterial clones from the NTA culture clustered in the Delta- and Betaproteobacteria. Both cultures contained thin rods, presumably the methanogens, as the predominant morphotype, and represent a significant advance in characterization of the novel acidiphilic R-10 family methanogens.

Anthropogenic impact is a pervasive problem in heavily trafficked cave systems and fecal contamination is equally problematic in many cave and karst waters worldwide. Carter Saltpeter Cave in Carter County, TN exhibits Mn(III/IV) oxide coatings associated with groundwater seeps, as well as manganese oxide growth on litter. Culturing results revealed that Mn(III/IV) oxide production on litter was associated with Mn(II)-oxidizing fungi. Immediately prior to this study, a massive Mn(II)-oxidizing biofilm bloomed at a cave seep. During the course of this study from 2009-2011, the seep exhibited a dramatic visual reduction in Mn(III/IV) oxide production, which was hypothesized to correlate with a decrease in fecal nutrient input. Molecular methods confirmed the presence of Bacteroides-Prevotella human fecal indicators in this seep, and most probable number assays and ion chromatography of the associated seep water confirmed nutrient loading at the site. Further, phylogenetic analysis from clone sequences suggested a strong initial human-specific fecal signature in July 2009, and a weaker human signature by June 2011. Most Probable Number (MPN) analyses of heterotrophic bacteria at this site suggested that Mn(II) oxidation was correlated with heterotrophic activity, due to point source exogenous nutrient loading.

Peatlands are found on all continents, covering 3% of the global land area. However, the spatial extent and causes of metal enrichment in peatlands is understudied and no attempt has been made to evaluate global patterns of metal enrichment in bog and fen peatlands, despite that certain metals and rare earth elements (REE) arise from anthropogenic sources. We analyzed 368 peat cores sampled in 16 countries across five continents and measured metal and other element concentrations at three depths down to 70 cm as well as estimated cumulative atmospheric S deposition (1850–2009) for each site. Sites were assigned to one of three distinct broadly recognized peatland categories (bog, poor fen, and intermediate-to-moderately rich fen) that varied primarily along a pH gradient. Metal concentrations differed among peatland types, with intermediate-to-moderately rich fens demonstrating the highest concentrations of most metals. Median enrichment factors (EFs; a metric comparing natural and anthropogenic metal deposition) for individual metals were similar among bogs and fens (all groups), with metals likely to be influenced by anthropogenic sources (As, Cd, Co, Cu, Hg, Pb, and Sb) demonstrating median enrichment factors (EFs) > 1.5. Additionally, mean EFs were substantially higher than median values, and the positive correlation (< 0.40) with estimated cumulative atmospheric S deposition, confirmed some level of anthropogenic influence of all pollutant metals except for Hg that was unrelated to S deposition. Contrary to expectations, high EFs were not restricted to pollutant metals, with Mn, K and Rb all exhibiting elevated median EFs that were in the same range as pollutant metals likely due to peatland biogeochemical processes leading to enrichment of these nutrients in surface soil horizons. The global patterns of metal enrichment in bogs and fens identified in this study underscore the importance of these peatlands as environmental archives of metal deposition, but also illustrates that biogeochemical processes can enrich metals in surface peat and EFs alone do not necessarily indicate atmospheric contamination.