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Nutrients Alter Methane Production and Oxidation in a Thawing Permafrost Mire

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Abstract

Permafrost thaw releases nutrients and metals from previously frozen soils and these nutrients may affect important biogeochemical processes including methane (CH4) production and oxidation. Here we assessed how concentrations of nutrients, solutes, and metals varied across four plant communities undergoing permafrost thaw and if these geochemical characteristics affected rates of CH4 production and oxidation. We tested nutrient limitation in CH4 production and oxidation by experimentally adding nitrogen (N), phosphorus (P) and a permafrost leachate to peat across these four plant communities. The upper 20 cm of permafrost contained 715 ± 298 mg m−2 of extractable inorganic N and 20 ± 6 mg m−2 of resin-extractable phosphorus (Presin), for a N:P ratio of 36:1. These low amounts of Presin coincide with high acid-digestible aluminum (Al), iron (Fe), and P concentrations in the permafrost soil and suggest that P may accumulate via sorption and constrain easily available forms of P for plants and microbes. Permafrost leachate additions decreased potential CH4 production rates up to 80% and decreased CH4 oxidation rates by 66%, likely due to inhibitory effects of N in the permafrost. In contrast, organic and inorganic P additions increased CH4 oxidation rates up to 36% in the tall graminoid fen, a community where phosphate availability was low and CH4 production was high. Our results suggest that (1) inorganic N is available immediately from permafrost thaw, while (2) P availability is controlled by sorption properties, and (3) plant community, nutrient stoichiometry, and metal availability modulate how permafrost thaw affects CH4 production and oxidation.

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References

  • Åkerman HJ, Johansson M. 2008. Thawing permafrost and thicker active layers in sub-arctic Sweden. Permafr Periglac Process 19:279–292.

    Article  Google Scholar 

  • Anderson G, Williams EG, Moir J. 1974. A Comparison of the Sorption of Inorganic Orthophosphate and Inositol Hexaphosphate By Six Acid Soils. Journal of Soil Science 25.

  • Basiliko N, Yavitt JB. 2001. Influence of Ni Co, Fe, and Na additions on methane production in Sphagnum-dominated Northern American peatlands. Biogeochemistry 52:133–153.

    Article  CAS  Google Scholar 

  • Bloom PR. 1981. Phosphorus adsorption by an aluminum-peat complex. Soil Science Society America Journal 45:267–272.

    Article  CAS  Google Scholar 

  • Bodelier PLE, Laanbroek HJ. 2004. Nitrogen as a regulatory factor of methane oxidation in soils and sediments. FEMS Microbiology Ecology 47:265–277.

    Article  CAS  PubMed  Google Scholar 

  • Bridgham SD, Updegraff K, Pastor J. 1998. Carbon, nitrogen, and phosphorus mineralization in northern wetlands. Ecology 79:1545–1561.

    Article  Google Scholar 

  • Chaikaew P, Chavanich S. 2017. Spatial variability and relationship of mangrove soil organic matter to organic carbon. Applied and Environmental Soil Science 2017.

  • Chauhan A, Pathak A, Ogram A. 2012. Composition of Methane-Oxidizing bacterial communities as a function of nutrient loading in the florida everglades. Microb Ecol 64:750–759.

    Article  CAS  PubMed  Google Scholar 

  • Christensen TR, Johansson T, Jonas Å Kerman H, Mastepanov M, Malmer N, Friborg T, Crill P, Svensson BH. 2004. Thawing sub-arctic permafrost: effects on vegetation and methane emissions. Geophysical Research Letters 31:1–4.

  • Clymo R. 1963. Ion exchange in Sphagnum and its relation to bog ecology. Ann Bot 27:309–324.

    Article  CAS  Google Scholar 

  • Conrad R. 1989. Control of methane production in terrestrial ecosystems. In: Andreae MO, Schimel DS, editors. Exchange of trace gases between terrestrial ecosystems and the atmosphere. pp 39–58.

  • Crill PM, Martikainen PJ, Nykanen H, Silvola J. 1994. Temperature and N fertilization effects on methane oxidation in a drained peatland soil. Soil Biol Biochem 26:1331–9.

  • Finger RA, Turetsky MR, Kielland K, Ruess RW, Mack MC, Euskirchen ES. 2016. Effects of permafrost thaw on nitrogen availability and plant–soil interactions in a boreal Alaskan lowland. Journal of Ecology 104:1542–1554.

    Article  Google Scholar 

  • Forsmann DM, Kjaergaard C. 2014. Phosphorus release from anaerobic peat soils during convective discharge–effect of soil Fe: p molar ratio and preferential flow. Geoderma 223–225:21–32. https://doi.org/10.1016/j.geoderma.2014.01.025.

    Article  CAS  Google Scholar 

  • Giesler R, Satoh F, Ilstedt U, Nordgren A. 2004. Microbially available phosphorus in boreal forests: Effects of aluminum and iron accumulation in the humus layer. Ecosystems 7:208–217.

    Article  CAS  Google Scholar 

  • Glass JB, Axler RP, Chandra S, Goldman CR. 2012. Molybdenum limitation of microbial nitrogen assimilation in aquatic ecosystems and pure cultures. Frontiers in Microbiology 3:1–11.

    Article  Google Scholar 

  • Gu S, Gruau G, Dupas R, Petitjean P, Li Q, Pinay G. 2019. Respective roles of Fe-oxyhydroxide dissolution, pH changes and sediment inputs in dissolved phosphorus release from wetland soils under anoxic conditions. Geoderma 338:365–374. https://doi.org/10.1016/j.geoderma.2018.12.034.

    Article  CAS  Google Scholar 

  • Heiberg L, Koch CB, Kjaergaard C, Jensen HS, Hansen HCB. 2012. Vivianite precipitation and phosphate sorption following iron reduction in anoxic soils. Journal of Environmental Quality 41:938–949.

    Article  CAS  PubMed  Google Scholar 

  • Herndon EM, Kinsman-Costello L, Duroe KA, Mills J, Kane ES, Sebestyen SD, Thompson AA, Wullschleger SD. 2019. Iron (Oxyhydr)oxides serve as phosphate traps in tundra and boreal peat soils. Journal of Geophysical Research Biogeosciences 124:227–246.

    Article  CAS  Google Scholar 

  • Hodgkins SB, Tfaily MM, McCalley CK, Logan T a., Crill PM, Saleska SR, Rich VI, Chanton JP. 2014. Changes in peat chemistry associated with permafrost thaw increase greenhouse gas production. Proceedings of the National Academy of Science 111:5819–24.

  • Homyak PM, Slessarev EW, Hagerty S, Greene AC, Marchus K, Dowdy K, Iverson S, Schimel JP. 2021. Amino acids dominate diffusive nitrogen fluxes across soil depths in acidic tussock tundra. New Phytology.

  • Hoyos-Santillan J, Lomax BH, Large D, Turner BL, Lopez OR, Boom A, Sepulveda-Jauregui A, Sjögersten S. 2019. Evaluation of vegetation communities, water table, and peat composition as drivers of greenhouse gas emissions in lowland tropical peatlands. Science of the Total Environment 688:1193–1204.

    Article  CAS  PubMed  Google Scholar 

  • Hugelius G, Loisel J, Chadburn S, Jackson RB, Jones M, MacDonald G, Marushchak M, Olefeldt D, Packalen M, Siewert MB, Treat C, Turetsky M, Voigt C, Yu Z. 2020. Large stocks of peatland carbon and nitrogen are vulnerable to permafrost thaw. Proceedings of the National Academy of Science:201916387.

  • Juutinen S, Moore TR, Bubier JL, Arnkil S, Humphreys E, Marincak B, Roy C, Larmola T. 2018. Long-term nutrient addition increased CH4 emission from a bog through direct and indirect effects. Scientific Reports 8:1–11. https://doi.org/10.1038/s41598-018-22210-2.

    Article  CAS  Google Scholar 

  • Keller JK, Bauers AK, Bridgham SD, Kellogg LE, Iversen CM. 2006. Nutrient control of microbial carbon cycling along an ombrotrophic-minerotrophic peatland gradient. Journal of Geophysical Research Biogeosciences 111:1–14.

    Google Scholar 

  • Keuper F, van Bodegom PM, Dorrepaal E, Weedon JT, van Hal J, van Logtestijn RSP, Aerts R. 2012. A frozen feast: thawing permafrost increases plant-available nitrogen in subarctic peatlands. Global Change Biology 18:1998–2007.

    Article  Google Scholar 

  • Keuper F, Dorrepaal E, van Bodegom PM, van Logtestijn R, Venhuizen G, van Hal J, Aerts R. 2017. Experimentally increased nutrient availability at the permafrost thaw front selectively enhances biomass production of deep-rooting subarctic peatland species. Global Change Biology 23:4257–4266.

    Article  PubMed  Google Scholar 

  • Klaminder J, Yoo K, Rydberg J, Giesler R. 2008. An explorative study of mercury export from a thawing palsa mire. Journal of Geophysical Research Biogeosciences 113:1–9.

    Google Scholar 

  • Kuhn M, Lundin EJ, Giesler R, Johansson M, Karlsson J. 2018. Emissions from thaw ponds largely offset the carbon sink of northern permafrost wetlands. Scientific Reports 8:1–7.

    Article  Google Scholar 

  • Laanbroek HJ. 2010. Methane emission from natural wetlands: interplay between emergent macrophytes and soil microbial processes. A mini-review. Annals of Botany 105:141–153.

    Article  CAS  PubMed  Google Scholar 

  • Larmola T, Leppänen SM, Tuittila E-S, Aarva M, Merilä P, Fritze H, Tiirola M. 2014. Methanotrophy induces nitrogen fixation during peatland development. Proceedings of the National Academy of Sciences USA 111:734–739.

    Article  CAS  Google Scholar 

  • Malhotra A, Roulet NT. 2015. Environmental correlates of peatland carbon fluxes in a thawing landscape: do transitional thaw stages matter? Biogeosciences 12:3119–3130.

    Article  Google Scholar 

  • Malmer N, Johansson T, Olsrud M, Christensen TR. 2005. Vegetation, climatic changes and net carbon sequestration in a North-Scandinavian subarctic mire over 30 years. Global Change Biology 11:1895–1909.

    Google Scholar 

  • Nykänen H, Vasander H, Huttunen JT, Martikainen PJ, Plant S, I NM, Huttunen JT, Martikainen PJ, Vasander H, Sciences E. 2002. Effect of experimental nitrogen load on methane and nitrous oxide fluxes on ombrotrophic boreal peatland. Plant and Soil 242:147–55.

  • Olid C, Klaminder J, Monteux S, Johansson M, Dorrepaal E. 2020. Decade of experimental permafrost thaw reduces turnover of young carbon and increases losses of old carbon, without affecting the net carbon balance. Global Chang Biology:1–13.

  • Palace M, Herrick C, DelGreco J, Finnell D, Garnello AJ, McCalley C, McArthur K, Sullivan F, Varner RK. 2018. Determining subarctic peatland vegetation using an unmanned aerial system (UAS). Remote Sensing 10:1–20.

    Article  Google Scholar 

  • Patzner M, Mueller C, Malusova M, Baur M, Nikeleit V, Scholten T, Hoeschen C, Byrne J, Borch T, Kappler A, Bryce C. 2020. Iron mineral dissolution releases iron and associated organic carbon during permafrost thaw. Nature Communications. https://doi.org/10.1038/s41467-020-20102-6.

    Article  PubMed  PubMed Central  Google Scholar 

  • Perryman CR, McCalley CK, Malhotra A, Fahnestock MF, Kashi NN, Bryce JG, Giesler R, Varner RK. 2020. Thaw transitions and redox conditions drive methane oxidation in a permafrost peatland. Journal of Geophysical Research Biogeosciences 125:1–15.

    Article  Google Scholar 

  • Redeker KR, Baird AJ, Teh YA. 2015. Quantifying wind and pressure effects on trace gas fluxes across the soil-atmosphere interface. Biogeosciences 12:7423–7434.

    Article  Google Scholar 

  • Reyes FR, Lougheed VL. 2015. Rapid nutrient release from permafrost thaw in arctic aquatic ecosystems. Arctic, Antarctic and Alpine Research 47:35–48.

    Article  Google Scholar 

  • Richardson CJ. 1985. Mechanisms controlling phosphorus retention capacity in freshwater wetlands. Science(Washington) 228:1424–7. http://www.ldeo.columbia.edu/~sanpisa/wetlands/reading/richardson1985.pdf%5Cnpapers2://publication/uuid/CE0C88E8-F77B-4765-99CA-0A7882293C81

  • Rinne J. 2021. Swedish National Network. Ecosystem eco time series (ICOS Sweden), Abisko-Stordalen Palsa Bog, 2018-12-31–2019-12-31. https://meta.icos-cp.eu/objects/s5oBzukX_FaXpHU___86QasO.

  • Robertson GP, Wedin D, Groffman PM, Blair JM, Holland EA, Nedelhoffer KJ, Harris D. 1999. Soil carbon and nitrogen availability. Nitrogen mineralization, nitrification, and soil respiration potentials. In: Standard soil methods for long-term ecological research. pp 258–71.

  • Saaltink RM, Dekker SC, Eppinga MB, Griffioen J, Wassen MJ. 2017. Plant-specific effects of iron-toxicity in wetlands. Plant and Soil 416:83–96.

    Article  CAS  Google Scholar 

  • Saggar S, Hedley MJ, White RE. 1990. A simplified resin membrane technique for extracting phosphorus from soils. Fertilizer Research 24:173–180.

    Article  CAS  Google Scholar 

  • Salmon VG, Soucy P, Mauritz M, Celis G, Natali SM, Mack MC, Schuur EAG. 2016. Nitrogen availability increases in a tundra ecosystem during five years of experimental permafrost thaw. Global Change Biology 22:1927–1941.

    Article  PubMed  Google Scholar 

  • Saunois M, Stavert AR, Poulter B, Jackson RB, Carlson KM, Bousquet P, Canadell JG, Raymond PA, Dlugokencky EJ, Houweling S, Frankenberg C, Höglund-isaksson L, Gedney N, Krummel PB, Jensen KM, Joos F, Mcnorton J, Miller PA, Melton JR, Doherty SO, Parker RJ, Prigent C, Prinn R, Ramonet M, Steele LP, Thornton BF, Tubiello FN, Regnier P, Riley WJ, Tsuruta A, Viovy N, Voulgarakis A, Werf GR Van Der, Weiss RF, Yoshida Y. 2020. The Global Methane Budget 2000 – 2017 1 Introduction 2 Methodology 3 Methane sources and sinks: bottom-up estimates. 12.

  • Schuur EAG, McGuire AD, Schadel C, Grosse G, Harden JW, Hayes DJ, Hugelius G, Koven CD, Kuhry P, Lawrence DM, Natali SM, Olefeldt D, Romanovsky VE, Schaefer K, Turetsky MR, Treat C, Vond JE. 2015. Climate change and the permafrost carbon feedback. Nature 520:171–179.

    Article  CAS  PubMed  Google Scholar 

  • Singleton CM, McCalley CK, Woodcroft BJ, Boyd JA, Evans PN, Hodgkins SB, Chanton JP, Frolking S, Crill PM, Saleska SR, Rich VI, Tyson GW. 2018. Methanotrophy across a natural permafrost thaw environment. ISME J 12:2544–2558.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sjögersten S, Cheesman AW, Lopez O, Turner BL. 2011. Biogeochemical processes along a nutrient gradient in a tropical ombrotrophic peatland. Biogeochemistry 104:147–163.

    Article  Google Scholar 

  • Smemo KA, Yavitt JB. 2007. Evidence for anaerobic CH4 oxidation in freshwater peatlands. Geomicrobiology Journal 24:583–597.

    Article  CAS  Google Scholar 

  • Song C, Yang G, Liu D, Mao R. 2012. Phosphorus availability as a primary constraint on methane emission from a freshwater wetland. Atmospheric Environment 59:202–206. https://doi.org/10.1016/j.atmosenv.2012.06.003.

    Article  CAS  Google Scholar 

  • Sterner R, Elser J. 2002. Ecological stoichiometry: the biology of elements from molecules to the biosphere. pp 44–80.

  • Strom L, Tagesson T, Mastepanov M, Christensen TR. 2012. Presence of Eriophorum scheuchzeri enhances substrate availability and methane emission in an Arctic wetland. Soil Biol and Biochemistry 45:61–70. https://doi.org/10.1016/j.soilbio.2011.09.005.

    Article  CAS  Google Scholar 

  • Sundh I, Nilsson M, Granberg G, Svensson BH. 1994. Depth distribution of microbial production and oxidation of methane in northern boreal peatlands. Microb Ecol 27:253–265.

    Article  CAS  PubMed  Google Scholar 

  • Thompson MS, Giesler R, Karlsson J, Klaminder J. 2015. Size and characteristics of the DOC pool in near-surface subarctic mire permafrost as a potential source for nearby freshwaters. Arctic, Antarctic and Alpine Research 47:49–58.

    Article  Google Scholar 

  • Turner BL, Haygarth PM. 2001. Phosphorus solubilization in rewetted soils. Nature 411:258.

    Article  CAS  PubMed  Google Scholar 

  • Veraart AJ, Steenbergh AK, Ho A, Kim SY, Bodelier PLE. 2015. Beyond nitrogen: the importance of phosphorus for CH4 oxidation in soils and sediments. Geoderma 259:337–346.

    Article  Google Scholar 

  • Vincent AG, Vestergren J, Gröbner G, Persson P, Schleucher J, Giesler R. 2013. Soil organic phosphorus transformations in a boreal forest chronosequence. Plant and Soil 367:149–162.

    Article  CAS  Google Scholar 

  • Waughman GJ. 1980. Chemical aspects of the ecology of some south german peatlands. 68:1025–46.

  • Yang G, Peng Y, Abbott BW, Biasi C, Wei B, Zhang D, Wang J, Yu J, Li F, Wang G, Kou D, Liu F, Yang Y. 2021. Phosphorus rather than nitrogen regulates ecosystem carbon dynamics after permafrost thaw. Global Change Biology 27:5818–5830.

    Article  CAS  PubMed  Google Scholar 

  • Zhang L, Yuan F, Bai J, Duan H, Gu X, Hou L, Huang Y, Yang M, He JS, Zhang Z, Yu L, Song C, Lipson DA, Zona D, Oechel W, Janssens IA, Xu X. 2020. Phosphorus alleviation of nitrogen-suppressed methane sink in global grasslands. Ecology Letters 23:821–830.

    Article  PubMed  Google Scholar 

  • Zheng Y, Zhang LM, He JZ. 2013. Immediate effects of nitrogen, phosphorus, and potassium amendments on the methanotrophic activity and abundance in a Chinese paddy soil under short-term incubation experiment. Journal of Soils and Sediments 13:189–196.

    Article  CAS  Google Scholar 

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Acknowledgements

We thank several funding agencies for support including NASA New Hampshire Space Grant Consortium Program grant 80NSSC20M0051, Lewis and Clark Expedition Fund, Carolyn Thorn Kissel Garden Club of America award, Iranian Association of Boston student award, UNH Department of Earth Sciences, and Department of Energy Genomic Science Program grants DE-SC0010580 and DE-SC001644. We thank Mel Knorr, Jody Potter, and Nathan Thorp for assistance, Dr. Jonatan Klaminder for bulk density data, Swedish Polar Research Secretariate and SITES for the work done and hospitality at Abisko Research Station.

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  1. Earth Systems Research Center, Institute for the Study of Earth, Ocean, and Space, University of New Hampshire, Durham, New Hampshire, USA

    N. Niloufar Kashi, Erik A. Hobbie & Ruth K. Varner

  2. Department of Earth Sciences, University of New Hampshire, Durham, New Hampshire, USA

    N. Niloufar Kashi, Erik A. Hobbie & Ruth K. Varner

  3. Department of Natural Resources and the Environment, University of New Hampshire, Durham, New Hampshire, USA

    Erik A. Hobbie, Adam S. Wymore & Jessica G. Ernakovich

  4. Climate Impacts Research Centre, Department of Ecology and Environmental Science, Umeå University, Umeå, Sweden

    Reiner Giesler

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  1. N. Niloufar Kashi
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Correspondence to N. Niloufar Kashi.

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Author contributions: NNK, designed research, NNK, RG performed research; RKV, RG contributed analytic tools; NNK, RG, and EAH analyzed data; all authors wrote the paper. The authors declare no conflict of interest.

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Kashi, N.N., Hobbie, E.A., Varner, R.K. et al. Nutrients Alter Methane Production and Oxidation in a Thawing Permafrost Mire. Ecosystems 26, 302–317 (2023). https://doi.org/10.1007/s10021-022-00758-5

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