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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. Experimental assessment of tree canopy and leaf litter controls on the microbiome and nitrogen fixation rates of two boreal mosses

   https://doi.org/10.1111/nph.16611  

   Jean, Mélanie ; Holland‐Moritz, Hannah ; Melvin, April M. ; Johnstone, Jill F. ; Mack, Michelle C. ( May 2020 , New Phytologist)

   Nitrogen (N₂)‐fixing moss microbial communities play key roles in nitrogen cycling of boreal forests. Forest type and leaf litter inputs regulate moss abundance, but how they control moss microbiomes and N₂‐fixation remains understudied. We examined the impacts of forest type and broadleaf litter on microbial community composition and N₂‐fixation rates ofHylocomium splendensandPleurozium schreberi.

   We conducted a moss transplant and leaf litter manipulation experiment at three sites with paired paper birch (Betula neoalaskana) and black spruce (Picea mariana) stands in Alaska. We characterized bacterial communities using marker gene sequencing, determined N₂‐fixation rates using stable isotopes (¹⁵N₂) and measured environmental covariates.

   Mosses native to and transplanted into spruce stands supported generally higher N₂‐fixation and distinct microbial communities compared to similar treatments in birch stands. High leaf litter inputs shifted microbial community composition for both moss species and reduced N₂‐fixation rates forH. splendens, which had the highest rates. N₂‐fixation was positively associated with several bacterial taxa, including cyanobacteria.

   The moss microbiome and environmental conditions controlled N₂‐fixation at the stand and transplant scales. Predicted shifts from spruce‐ to deciduous‐dominated stands will interact with the relative abundances of mosses supporting different microbiomes and N₂‐fixation rates, which could affect stand‐level N inputs.

    

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3. Host Identity as a Driver of Moss-Associated N2 Fixation Rates in Alaska

   https://doi.org/10.1007/s10021-020-00534-3  

   Stuart, Julia E. ; Holland-Moritz, Hannah ; Lewis, Lily R. ; Jean, Mélanie ; Miller, Samantha N. ; McDaniel, Stuart F. ; Fierer, Noah ; Ponciano, José Miguel ; Mack, Michelle C. ( August 2020 , Ecosystems)

   null (Ed.)

   Moss-associated N2 fixation provides a substantial but heterogeneous input of new N to nutrient-limited ecosystems at high latitudes. In spite of the broad diversity of mosses found in boreal and Arctic ecosystems, the extent to which host moss identity drives variation in N2 fixation rates remains largely undetermined. We used 15N2 incubations to quantify the fixation rates associated with 34 moss species from 24 sites ranging from 60° to 68° N in Alaska, USA. Remarkably, all sampled moss genera fixed N2, including well-studied feather and peat mosses and genera such as Tomentypnum, Dicranum, and Polytrichum. The total moss-associated N2 fixation rates ranged from almost zero to 3.2 mg N m−2 d−1, with an average of 0.8 mg N m−2 d−1, based on abundance-weighted averages of all mosses summed for each site. Random forest models indicated that moss taxonomic family was a better predictor of rate variation across Alaska than any of the measured environmental factors, including site, pH, tree density, and mean annual precipitation and temperature. Consistent with this finding, mixed models showed that trends in N2 fixation rates among moss genera were consistent across biomes. We also found “hotspots” of high fixation rates in one-fourth of sampled sites. Our results demonstrated the importance of moss identity in influencing N2 fixation rates. This in turn indicates the potential utility of moss identity when making ecosystem N input predictions and exploring other sources of process rate variation. 

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4. Regional biogeography versus intra-annual dynamics of the root and soil microbiome

   https://doi.org/10.1186/s40793-023-00504-x  

   Bell-Dereske, Lukas P. ; Benucci, Gian Maria Niccolò ; da Costa, Pedro Beschoren ; Bonito, Gregory ; Friesen, Maren L. ; Tiemann, Lisa K. ; Evans, Sarah E. ( June 2023 , Environmental Microbiome)

   Root and soil microbial communities constitute the below-ground plant microbiome, are drivers of nutrient cycling, and affect plant productivity. However, our understanding of their spatiotemporal patterns is confounded by exogenous factors that covary spatially, such as changes in host plant species, climate, and edaphic factors. These spatiotemporal patterns likely differ across microbiome domains (bacteria and fungi) and niches (root vs. soil).

   To capture spatial patterns at a regional scale, we sampled the below-ground microbiome of switchgrass monocultures of five sites spanning > 3 degrees of latitude within the Great Lakes region. To capture temporal patterns, we sampled the below-ground microbiome across the growing season within a single site. We compared the strength of spatiotemporal factors to nitrogen addition determining the major drivers in our perennial cropping system. All microbial communities were most strongly structured by sampling site, though collection date also had strong effects; in contrast, nitrogen addition had little to no effect on communities. Though all microbial communities were found to have significant spatiotemporal patterns, sampling site and collection date better explained bacterial than fungal community structure, which appeared more defined by stochastic processes. Root communities, especially bacterial, were more temporally structured than soil communities which were more spatially structured, both across and within sampling sites. Finally, we characterized a core set of taxa in the switchgrass microbiome that persists across space and time. These core taxa represented < 6% of total species richness but > 27% of relative abundance, with potential nitrogen fixing bacteria and fungal mutualists dominating the root community and saprotrophs dominating the soil community.

   Our results highlight the dynamic variability of plant microbiome composition and assembly across space and time, even within a single variety of a plant species. Root and soil fungal community compositions appeared spatiotemporally paired, while root and soil bacterial communities showed a temporal lag in compositional similarity suggesting active recruitment of soil bacteria into the root niche throughout the growing season. A better understanding of the drivers of these differential responses to space and time may improve our ability to predict microbial community structure and function under novel conditions.

    

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5. Climate drivers alter nitrogen availability in surface peat and decouple N2 fixation from CH4 oxidation in the Sphagnum moss microbiome

   https://doi.org/10.1111/gcb.16651  

   Petro, Caitlin ; Carrell, Alyssa A. ; Wilson, Rachel M. ; Duchesneau, Katherine ; Noble‐Kuchera, Sekou ; Song, Tianze ; Iversen, Colleen M. ; Childs, Joanne ; Schwaner, Geoff ; Chanton, Jeffrey P. ; et al ( March 2023 , Global Change Biology)

   Peat mosses (Sphagnumspp.) are keystone species in boreal peatlands, where they dominate net primary productivity and facilitate the accumulation of carbon in thick peat deposits.Sphagnummosses harbor a diverse assemblage of microbial partners, including N₂‐fixing (diazotrophic) and CH₄‐oxidizing (methanotrophic) taxa that support ecosystem function by regulating transformations of carbon and nitrogen. Here, we investigate the response of theSphagnumphytobiome (plant + constituent microbiome + environment) to a gradient of experimental warming (+0°C to +9°C) and elevated CO₂(+500 ppm) in an ombrotrophic peatland in northern Minnesota (USA). By tracking changes in carbon (CH₄, CO₂) and nitrogen (NH₄‐N) cycling from the belowground environment up toSphagnumand its associated microbiome, we identified a series of cascading impacts to theSphagnumphytobiome triggered by warming and elevated CO₂. Under ambient CO₂, warming increased plant‐available NH₄‐N in surface peat, excess N accumulated inSphagnumtissue, and N₂fixation activity decreased. Elevated CO₂offset the effects of warming, disrupting the accumulation of N in peat andSphagnumtissue. Methane concentrations in porewater increased with warming irrespective of CO₂treatment, resulting in a ~10× rise in methanotrophic activity withinSphagnumfrom the +9°C enclosures. Warming's divergent impacts on diazotrophy and methanotrophy caused these processes to become decoupled at warmer temperatures, as evidenced by declining rates of methane‐induced N₂fixation and significant losses of keystone microbial taxa. In addition to changes in theSphagnummicrobiome, we observed ~94% mortality ofSphagnumbetween the +0°C and +9°C treatments, possibly due to the interactive effects of warming on N‐availability and competition from vascular plant species. Collectively, these results highlight the vulnerability of theSphagnumphytobiome to rising temperatures and atmospheric CO₂concentrations, with significant implications for carbon and nitrogen cycling in boreal peatlands.

    

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