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

Journal Article · · Global Change Biology
DOI: https://doi.org/10.1111/gcb.16651 · OSTI ID:1975359
ORCiD logo [1]; ORCiD logo [2]; ORCiD logo [3]; ORCiD logo [1];  [1]; ORCiD logo [1]; ORCiD logo [2]; ORCiD logo [2]; ORCiD logo [2]; ORCiD logo [3]; ORCiD logo [4]; ORCiD logo [2]; ORCiD logo [1]; ORCiD logo [2]; ORCiD logo [1]
  1. Georgia Institute of Technology, Atlanta, GA (United States)
  2. Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
  3. Florida State Univ., Tallahassee, FL (United States)
  4. Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States); Univ. of Tennessee, Knoxville, TN (United States)

Peat mosses (Sphagnum spp.) are keystone species in boreal peatlands, where they dominate net primary productivity and facilitate the accumulation of carbon in thick peat deposits. Sphagnum mosses 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. In this work, we investigate the response of the Sphagnum phytobiome (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 to Sphagnum and its associated microbiome, we identified a series of cascading impacts to the Sphagnum phytobiome triggered by warming and elevated CO2. Under ambient CO2, warming increased plant-available NH4-N in surface peat, excess N accumulated in Sphagnum tissue, and N2 fixation activity decreased. Elevated CO2 offset the effects of warming, disrupting the accumulation of N in peat and Sphagnum tissue. Methane concentrations in porewater increased with warming irrespective of CO2 treatment, resulting in a ~10× rise in methanotrophic activity within Sphagnum from 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 N2 fixation and significant losses of keystone microbial taxa. In addition to changes in the Sphagnum microbiome, we observed ~94% mortality of Sphagnum between 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 the Sphagnum phytobiome to rising temperatures and atmospheric CO2 concentrations, with significant implications for carbon and nitrogen cycling in boreal peatlands.

Research Organization:
Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER); National Science Foundation (NSF)
Grant/Contract Number:
AC05-00OR22725
OSTI ID:
1975359
Journal Information:
Global Change Biology, Journal Name: Global Change Biology Journal Issue: 11 Vol. 29; ISSN 1354-1013
Publisher:
WileyCopyright Statement
Country of Publication:
United States
Language:
English

References (81)

How Sphagnum bogs down other plants journal July 1995
Rapid loss of an ecosystem engineer: Sphagnum decline in an experimentally warmed bog journal October 2019
Methylorosula polaris gen. nov., sp. nov., an aerobic, facultatively methylotrophic psychrotolerant bacterium from tundra wetland soil
  • Berestovskaya, Julia Ju.; Kotsyurbenko, Oleg R.; Tourova, Tatyana P.
  • International Journal of Systematic and Evolutionary Microbiology, Vol. 62, Issue Pt_3 https://doi.org/10.1099/ijs.0.007005-0
journal March 2012
Methanotrophic symbionts provide carbon for photosynthesis in peat bogs journal August 2005
The resilience and functional role of moss in boreal and arctic ecosystems: Tansley review journal August 2012
Methane Oxidation by Endophytic Bacteria Inhabiting Sphagnum sp. and Some Vascular Plants journal February 2018
Methanol in Plant Life journal November 2018
A Comparison of Nutrient Availability Indices Along an Ombrotrophic-Minerotrophic Gradient in Minnesota Wetlands journal January 2001
Global wetland contribution to 2000–2012 atmospheric methane growth rate dynamics journal September 2017
Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample journal June 2010
Vascular plant species response to warming and elevated carbon dioxide in a boreal peatland journal December 2020
Experimental nitrogen addition alters structure and function of a boreal bog: critical load and thresholds revealed journal June 2019
Climate change drives a shift in peatland ecosystem plant community: Implications for ecosystem function and stability journal June 2014
Nitrogen fixation and methanotrophy in forest mosses along a N deposition gradient journal June 2013
Long-term carbon and nitrogen dynamics at SPRUCE revealed through stable isotopes in peat profiles journal January 2017
Warming and elevated CO 2 promote rapid incorporation and degradation of plant‐derived organic matter in an ombrotrophic peatland journal November 2021
The Sensitivity of Moss-Associated Nitrogen Fixation towards Repeated Nitrogen Input journal January 2016
Habitat‐adapted microbial communities mediate Sphagnum peatmoss resilience to warming journal March 2022
Elevated CO2 and nitrate levels increase wheat root-associated bacterial abundance and impact rhizosphere microbial community composition and function journal November 2020
Massive peatland carbon banks vulnerable to rising temperatures journal May 2020
The role of mosses in ecosystem succession and function in Alaska’s boreal forestThis article is one of a selection of papers from The Dynamics of Change in Alaska’s Boreal Forests: Resilience and Vulnerability in Response to Climate Warming. journal July 2010
Controls over carbon storage and turnover in high-latitude soils journal December 2000
The importance of the microbiome of the plant holobiont journal February 2015
DADA2: High-resolution sample inference from Illumina amplicon data journal May 2016
Methanotrophy induces nitrogen fixation during peatland development journal December 2013
Methylopila jiangsuensis sp. nov., an aerobic, facultatively methylotrophic bacterium journal July 2011
A synthesis of methane emissions from 71 northern, temperate, and subtropical wetlands journal April 2014
Methylopila capsulata gen. nov., sp. nov., a novel non-pigmented aerobic facultatively methylotrophic bacterium journal October 1998
Minor revision to V4 region SSU rRNA 806R gene primer greatly increases detection of SAR11 bacterioplankton journal June 2015
Cutadapt removes adapter sequences from high-throughput sequencing reads journal May 2011
Practical innovations for high-throughput amplicon sequencing journal September 2013
Effects of nutrient addition on vegetation and carbon cycling in an ombrotrophic bog journal June 2007
Rapid expansion of northern peatlands and doubled estimate of carbon storage journal October 2019
N2-fixation by methanotrophs sustains carbon and nitrogen accumulation in pristine peatlands journal August 2014
Sources and flux of natural gases from Mono Lake, California journal November 1987
Persistent high temperature and low precipitation reduce peat carbon accumulation journal May 2016
Ecological interpretations of nitrogen isotope ratios of terrestrial plants and soils journal June 2015
Three decades of global methane sources and sinks journal September 2013
Experimental warming alters the community composition, diversity, and N 2 fixation activity of peat moss ( Sphagnum fallax ) microbiomes journal May 2019
The Ecology of Sphagnum book January 1982
Growth reduction of Sphagnum magellanicum subjected to high nitrogen deposition: the role of amino acid nitrogen concentration journal March 2003
Effects of nitrogen fertilization on diazotrophic activity of microorganisms associated with Sphagnum magellanicum journal March 2016
Long‐term warming effects on the microbiome and nifH gene abundance of a common moss species in sub‐Arctic tundra journal November 2021
Stability of peatland carbon to rising temperatures journal December 2016
Sphagnum mosses harbour highly specific bacterial diversity during their whole lifecycle journal November 2011
Amino acid accumulation and growth ofSphagnumunder different levels of N deposition journal January 2000
Direct physiological effects of nitrogen on Sphagnum: a greenhouse experiment: Direct effects of N application on Sphagnum journal December 2011
The Sphagnum microbiome supports bog ecosystem functioning under extreme conditions journal September 2014
Soil metabolome response to whole-ecosystem warming at the Spruce and Peatland Responses under Changing Environments experiment journal June 2021
Peatland Biogeochemistry and Watershed Hydrology at the Marcell Experimental Forest book January 2011
Carbon respiration from subsurface peat accelerated by climate warming in the subarctic journal July 2009
Synthetic Ion‐Exchange Resins: Soil and Environmental Studies journal January 1996
Response of photosynthesis of Sphagnum species from contrasting microhabitats to tissue water content and repeated desiccation journal December 1998
Nitrogen fertilization reduces Sphagnum production in bog communities journal September 2000
Methane emissions from wetlands: biogeochemical, microbial, and modeling perspectives from local to global scales journal February 2013
Effects of NH+4-N and NO+3-N on growth and metabolism of Sphagnum magellanicum journal February 1986
Biophysical drivers of seasonal variability in Sphagnum gross primary production in a northern temperate bog journal May 2017
Climatic modifiers of the response to nitrogen deposition in peat-forming Sphagnum mosses: a meta-analysis journal March 2011
Above- and belowground linkages in Sphagnum peatland: climate warming affects plant-microbial interactions journal December 2012
From The Cover: Plant community responses to experimental warming across the tundra biome journal January 2006
CO2 enhancement of forest productivity constrained by limited nitrogen availability journal October 2010
Transfer of fixed-N from N2-fixing cyanobacteria associated with the moss Sphagnum riparium results in enhanced growth of the moss journal May 2012
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 journal February 2022
Nutrient additions in pristine Patagonian Sphagnum bog vegetation: can phosphorus addition alleviate (the effects of) increased nitrogen loads: Nutrient additions in pristine Patagonian Sphagnum bog vegetation journal December 2011
Experimental warming interacts with soil moisture to discriminate plant responses in an ombrotrophic peatland journal May 2015
Diazotrophic methanotrophs in peatlands: the missing link? journal February 2015
Northern peatland carbon stocks and dynamics: a review journal January 2012
Ecohydrological controls on water distribution and productivity of moss communities in western boreal peatlands, Canada: Moisture Dynamics and Productivity of Boreal Fen Mosses journal March 2015
Peatland warming strongly increases fine-root growth journal July 2020
Effects of climate warming on Sphagnum photosynthesis in peatlands depend on peat moisture and species‐specific anatomical traits journal September 2019
Methanotrophic activity and diversity in different Sphagnum magellanicum dominated habitats in the southernmost peat bogs of Patagonia journal January 2012
The Sphagnum microbiome: new insights from an ancient plant lineage journal February 2016
Vegetation feedbacks of nutrient addition lead to a weaker carbon sink in an ombrotrophic bog journal October 2013
Latitudinal limits to the predicted increase of the peatland carbon sink with warming journal September 2018
Elevated CO 2 increases nitrogen rhizodeposition and microbial immobilization of root-derived nitrogen journal March 2007
Global prevalence of methane oxidation by symbiotic bacteria in peat-moss ecosystems journal August 2010
A climatic threshold triggers the die-off of peat mosses during an extreme heat wave journal September 2008
Rapid Net Carbon Loss From a Whole‐Ecosystem Warmed Peatland journal July 2020
Interactions between plant growth and soil nutrient cycling under elevated CO 2 : a meta-analysis journal November 2006
Natural nitrogen filter fails in polluted raised bogs journal June 2000
Novel metabolic interactions and environmental conditions mediate the boreal peatmoss-cyanobacteria mutualism journal November 2021