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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. Spectral Indices of Vegetation Condition and Soil Water Content Reflect Controls on CH ₄ and CO ₂ Exchange in Sphagnum ‐Dominated Northern Peatlands

   https://doi.org/10.1029/2021JG006486  

   Tucker, Colin; O’Neill, Ally; Meingast, Karl; Bourgeau‐Chavez, Laura; Lilleskov, Erik; Kane, Evan S. (June 2022, Journal of Geophysical Research: Biogeosciences)

   Abstract Northern peatlands play an important role in the global C cycle due to their large C stocks and high potential methane (CH₄) emissions. The CH₄and CO₂cycles of these systems are closely linked to hydrology, with water table level regulating the balance of oxic and anoxic conditions and the water content ofSphagnummosses that dominate primary production. Previous work has demonstrated that hyperspectral indices well‐suited to the detection of altered hydrology inSphagnumpeatlands are also highly correlated with GPP. However, little work has been done to extend these findings to CH₄effluxes. In this study, we evaluate the utility of four hyperspectral indices, two reflecting vegetation photosynthetic function (chlorophyll index (CI); normalized difference vegetation index) and two reflecting water content (wetness index (WI); floating water band index), for detecting effects of altered water table, precipitation, and vegetation community on CH₄and CO₂exchange in two peatland mesocosm studies. We found that CI is a good predictor of net CO₂exchange, and that it captured both drought and vegetation effects consistently across a broad range of vegetation treatments. Further, we demonstrate for the first time that WI combined with CI explained a significant percentage of CH₄efflux (R² = 0.32–0.57). Our results indicate that CI and WI together may be effective tools for detecting effects of altered hydrology and vegetation on northernSphagnum‐peatland CH₄and CO₂emissions, with implications for detecting and modeling changes in emissions of greenhouse gases at scales ranging from the ecosystem to the Earth system. 

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3. 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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4. 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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5. Habitat‐adapted microbial communities mediate Sphagnum peatmoss resilience to warming

   https://doi.org/10.1111/nph.18072  

   Carrell, Alyssa A.; Lawrence, Travis J.; Cabugao, Kristine Grace M.; Carper, Dana L.; Pelletier, Dale A.; Lee, Jun Hyung; Jawdy, Sara S.; Grimwood, Jane; Schmutz, Jeremy; Hanson, Paul J.; et al (March 2022, New Phytologist)

   Summary Sphagnumpeatmosses are fundamental members of peatland ecosystems, where they contribute to the uptake and long‐term storage of atmospheric carbon. Warming threatensSphagnummosses and is known to alter the composition of their associated microbiome. Here, we use a microbiome transfer approach to test if microbiome thermal origin influences host plant thermotolerance.We leveraged an experimental whole‐ecosystem warming study to collect field‐grownSphagnum, mechanically separate the associated microbiome and then transfer onto germ‐free laboratorySphagnumfor temperature experiments. Host and microbiome dynamics were assessed with growth analysis, Chlafluorescence imaging, metagenomics, metatranscriptomics and 16S rDNA profiling.Microbiomes originating from warming field conditions imparted enhanced thermotolerance and growth recovery at elevated temperatures. Metagenome and metatranscriptome analyses revealed that warming altered microbial community structure in a manner that induced the plant heat shock response, especially the HSP70 family and jasmonic acid production. The heat shock response was induced even without warming treatment in the laboratory, suggesting that the warm‐microbiome isolated from the field provided the host plant with thermal preconditioning.Our results demonstrate that microbes, which respond rapidly to temperature alterations, can play key roles in host plant growth response to rapidly changing environments. 

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