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1. Defining the Sphagnum Core Microbiome across the North American Continent Reveals a Central Role for Diazotrophic Methanotrophs in the Nitrogen and Carbon Cycles of Boreal Peatland Ecosystems

   https://doi.org/10.1128/mbio.03714-21  

   Kolton, Max; Weston, David J.; Mayali, Xavier; Weber, Peter K.; McFarlane, Karis J.; Pett-Ridge, Jennifer; Somoza, Mark M.; Lietard, Jory; Glass, Jennifer B.; Lilleskov, Erik A.; et al (February 2022, mBio)

   Martiny, Jennifer B. (Ed.)

   ABSTRACT Peat mosses of the genus Sphagnum are ecosystem engineers that frequently predominate over photosynthetic production in boreal peatlands. Sphagnum spp. host diverse microbial communities capable of nitrogen fixation (diazotrophy) and methane oxidation (methanotrophy), thereby potentially supporting plant growth under severely nutrient-limited conditions. Moreover, diazotrophic methanotrophs represent a possible “missing link” between the carbon and nitrogen cycles, but the functional contributions of the Sphagnum -associated microbiome remain in question. A combination of metagenomics, metatranscriptomics, and dual-isotope incorporation assays was applied to investigate Sphagnum microbiome community composition across the North American continent and provide empirical evidence for diazotrophic methanotrophy in Sphagnum -dominated ecosystems. Remarkably consistent prokaryotic communities were detected in over 250 Sphagnum SSU rRNA libraries from peatlands across the United States (5 states, 17 bog/fen sites, 18 Sphagnum species), with 12 genera of the core microbiome comprising 60% of the relative microbial abundance. Additionally, nitrogenase ( nifH ) and SSU rRNA gene amplicon analysis revealed that nitrogen-fixing populations made up nearly 15% of the prokaryotic communities, predominated by Nostocales cyanobacteria and Rhizobiales methanotrophs. While cyanobacteria comprised the vast majority (>95%) of diazotrophs detected in amplicon and metagenome analyses, obligate methanotrophs of the genus Methyloferula (order Rhizobiales ) accounted for one-quarter of transcribed nifH genes. Furthermore, in dual-isotope tracer experiments, members of the Rhizobiales showed substantial incorporation of 13 CH 4 and 15 N 2 isotopes into their rRNA. Our study characterizes the core Sphagnum microbiome across large spatial scales and indicates that diazotrophic methanotrophs, here defined as obligate methanotrophs of the rare biosphere ( Methyloferula spp. of the Rhizobiales ) that also carry out diazotrophy, play a keystone role in coupling of the carbon and nitrogen cycles in nutrient-poor peatlands. IMPORTANCE Nitrogen availability frequently limits photosynthetic production in Sphagnum moss-dominated high-latitude peatlands, which are crucial carbon-sequestering ecosystems at risk to climate change effects. It has been previously suggested that microbial methane-fueled fixation of atmospheric nitrogen (N 2 ) may occur in these ecosystems, but this process and the organisms involved are largely uncharacterized. A combination of omics (DNA and RNA characterization) and dual-isotope incorporation approaches illuminated the functional diversity of Sphagnum -associated microbiomes and defined 12 bacterial genera in its core microbiome at the continental scale. Moreover, obligate diazotrophic methanotrophs showed high nitrogen fixation gene expression levels and incorporated a substantial amount of atmospheric nitrogen and methane-driven carbon into their biomass. Thus, these results point to a central role for members of the rare biosphere in Sphagnum microbiomes as keystone species that couple nitrogen fixation to methane oxidation in nutrient-poor peatlands. 

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2. Large stocks of peatland carbon and nitrogen are vulnerable to permafrost thaw

   https://doi.org/10.1073/pnas.1916387117  

   Hugelius, Gustaf; Loisel, Julie; Chadburn, Sarah; Jackson, Robert B.; Jones, Miriam; MacDonald, Glen; Marushchak, Maija; Olefeldt, David; Packalen, Maara; Siewert, Matthias B.; et al (August 2020, Proceedings of the National Academy of Sciences)

   Northern peatlands have accumulated large stocks of organic carbon (C) and nitrogen (N), but their spatial distribution and vulnerability to climate warming remain uncertain. Here, we used machine-learning techniques with extensive peat core data ( n > 7,000) to create observation-based maps of northern peatland C and N stocks, and to assess their response to warming and permafrost thaw. We estimate that northern peatlands cover 3.7 ± 0.5 million km 2 and store 415 ± 150 Pg C and 10 ± 7 Pg N. Nearly half of the peatland area and peat C stocks are permafrost affected. Using modeled global warming stabilization scenarios (from 1.5 to 6 °C warming), we project that the current sink of atmospheric C (0.10 ± 0.02 Pg C⋅y −1 ) in northern peatlands will shift to a C source as 0.8 to 1.9 million km 2 of permafrost-affected peatlands thaw. The projected thaw would cause peatland greenhouse gas emissions equal to ∼1% of anthropogenic radiative forcing in this century. The main forcing is from methane emissions (0.7 to 3 Pg cumulative CH 4 -C) with smaller carbon dioxide forcing (1 to 2 Pg CO 2 -C) and minor nitrous oxide losses. We project that initial CO 2 -C losses reverse after ∼200 y, as warming strengthens peatland C-sinks. We project substantial, but highly uncertain, additional losses of peat into fluvial systems of 10 to 30 Pg C and 0.4 to 0.9 Pg N. The combined gaseous and fluvial peatland C loss estimated here adds 30 to 50% onto previous estimates of permafrost-thaw C losses, with southern permafrost regions being the most vulnerable. 

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3. Newly identified sex chromosomes in the Sphagnum (peat moss) genome alter carbon sequestration and ecosystem dynamics

   https://doi.org/10.1038/s41477-022-01333-5  

   Healey, Adam L.; Piatkowski, Bryan; Lovell, John T.; Sreedasyam, Avinash; Carey, Sarah B.; Mamidi, Sujan; Shu, Shengqiang; Plott, Chris; Jenkins, Jerry; Lawrence, Travis; et al (February 2023, Nature Plants)

   Abstract Peatlands are crucial sinks for atmospheric carbon but are critically threatened due to warming climates.Sphagnum(peat moss) species are keystone members of peatland communities where they actively engineer hyperacidic conditions, which improves their competitive advantage and accelerates ecosystem-level carbon sequestration. To dissect the molecular and physiological sources of this unique biology, we generated chromosome-scale genomes of twoSphagnumspecies:S. divinumandS. angustifolium.Sphagnumgenomes show no gene colinearity with any other reference genome to date, demonstrating thatSphagnumrepresents an unsampled lineage of land plant evolution. The genomes also revealed an average recombination rate an order of magnitude higher than vascular land plants and short putative U/V sex chromosomes. These newly described sex chromosomes interact with autosomal loci that significantly impact growth across diverse pH conditions. This discovery demonstrates that the ability ofSphagnumto sequester carbon in acidic peat bogs is mediated by interactions between sex, autosomes and environment. 

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4. Fresh Air for the Mire-Breathing Hypothesis: Sphagnum Moss and Peat Structure Regulate the Response of CO2 Exchange to Altered Hydrology in a Northern Peatland Ecosystem

   https://doi.org/10.3390/w14203239  

   O’Neill, Ally; Tucker, Colin; Kane, Evan S. (October 2022, Water)

   Sphagnum-dominated peatlands store more carbon than all of Earth’s forests, playing a large role in the balance of carbon dioxide. However, these carbon sinks face an uncertain future as the changing climate is likely to cause water stress, potentially reducing Sphagnum productivity and transitioning peatlands to carbon sources. A mesocosm experiment was performed on thirty-two peat cores collected from two peatland landforms: elevated mounds (hummocks) and lower, flat areas of the peatland (hollows). Both rainfall treatments and water tables were manipulated, and CO2 fluxes were measured. Other studies have observed peat subsiding and tracking the water table downward when experiencing water stress, thought to be a self-preservation technique termed ‘Mire-breathing’. However, we found that hummocks tended to compress inwards, rather than subsiding towards the lowered water table as significantly as hollows. Lower peat height was linearly associated with reduced gross primary production (GPP) in response to lowered water tables, indicating that peat subsidence did not significantly enhance the resistance of GPP to drought. Conversely, Sphagnum peat compression was found to stabilize GPP, indicating that this mechanism of resilience to drought may transmit across the landscape depending on which Sphagnum landform types are dominant. This study draws direct connections between Sphagnum traits and peatland hydrology and carbon cycling. 

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5. Quantifying the inhibitory impact of soluble phenolics on anaerobic carbon mineralization in a thawing permafrost peatland

   https://doi.org/10.1371/journal.pone.0252743  

   Cory, Alexandra B.; Chanton, Jeffrey P.; Spencer, Robert G.; Ogles, Olivia C.; Rich, Virginia I.; McCalley, Carmody K.; Wilson, Rachel M. (February 2022, PLOS ONE)

   Riaz, Muhammad (Ed.)

   The mechanisms controlling the extraordinarily slow carbon (C) mineralization rates characteristic of Sphagnum -rich peatlands (“bogs”) are not fully understood, despite decades of research on this topic. Soluble phenolic compounds have been invoked as potentially significant contributors to bog peat recalcitrance due to their affinity to slow microbial metabolism and cell growth. Despite this potentially significant role, the effects of soluble phenolic compounds on bog peat C mineralization remain unclear. We analyzed this effect by manipulating the concentration of free soluble phenolics in anaerobic bog and fen peat incubations using water-soluble polyvinylpyrrolidone (“PVP”), a compound that binds with and inactivates phenolics, preventing phenolic-enzyme interactions. CO 2 and CH 4 production rates (end-products of anaerobic C mineralization) generally correlated positively with PVP concentration following Michaelis-Menten (M.M.) saturation functions. Using M.M. parameters, we estimated that the extent to which phenolics inhibit anaerobic CO 2 production was significantly higher in the bog—62 ± 16%—than the fen—14 ± 4%. This difference was found to be more substantial with regards to methane production—wherein phenolic inhibition for the bog was estimated at 54 ± 19%, while the fen demonstrated no apparent inhibition. Consistent with this habitat difference, we observed significantly higher soluble phenolic content in bog vs. fen pore-water. Together, these findings suggest that soluble phenolics could contribute to bogs’ extraordinary recalcitrance and high (relative to other peatland habitats) CO 2 :CH 4 production ratios. 

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