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Biogeochemistry

, Volume 127, Issue 1, pp 57–87 | Cite as

Modeling CH4 and CO2 cycling using porewater stable isotopes in a thermokarst bog in Interior Alaska: results from three conceptual reaction networks

  • Rebecca B. Neumann
  • Steven J. Blazewicz
  • Christopher H. Conaway
  • Merritt R. Turetsky
  • Mark P. Waldrop
Article

Abstract

Quantifying rates of microbial carbon transformation in peatlands is essential for gaining mechanistic understanding of the factors that influence methane emissions from these systems, and for predicting how emissions will respond to climate change and other disturbances. In this study, we used porewater stable isotopes collected from both the edge and center of a thermokarst bog in Interior Alaska to estimate in situ microbial reaction rates. We expected that near the edge of the thaw feature, actively thawing permafrost and greater abundance of sedges would increase carbon, oxygen and nutrient availability, enabling faster microbial rates relative to the center of the thaw feature. We developed three different conceptual reaction networks that explained the temporal change in porewater CO2, CH4, δ 13C–CO2 and δ 13C–CH4. All three reaction-network models included methane production, methane oxidation and CO2 production, and two of the models included homoacetogenesis—a reaction not previously included in isotope-based porewater models. All three models fit the data equally well, but rates resulting from the models differed. Most notably, inclusion of homoacetogenesis altered the modeled pathways of methane production when the reaction was directly coupled to methanogenesis, and it decreased gross methane production rates by up to a factor of five when it remained decoupled from methanogenesis. The ability of all three conceptual reaction networks to successfully match the measured data indicate that this technique for estimating in situ reaction rates requires other data and information from the site to confirm the considered set of microbial reactions. Despite these differences, all models indicated that, as expected, rates were greater at the edge than in the center of the thaw bog, that rates at the edge increased more during the growing season than did rates in the center, and that the ratio of acetoclastic to hydrogenotrophic methanogenesis was greater at the edge than in the center. In both locations, modeled rates (excluding methane oxidation) increased with depth. A puzzling outcome from the effort was that none of the models could fit the porewater dataset without generating “fugitive” carbon (i.e., methane or acetate generated by the models but not detected at the field site), indicating that either our conceptualization of the reactions occurring at the site remains incomplete or our site measurements are missing important carbon transformations and/or carbon fluxes. This model–data discrepancy will motivate and inform future research efforts focused on improving our understanding of carbon cycling in permafrost wetlands.

Keywords

Carbon fluxes Homoacetogenesis Methanogenesis Methanotrophy Microbial rates Peat Model 13CO2 13CH4 Carbon isotopes 

Notes

Acknowledgments

We thank Julie Shoemaker for input and advice on the reaction network modeling; Burt Thomas for input and advice on the peeper method; Monica Haw, Torren Campbell and Sabrina Sevilgen for laboratory assistance; Lily Cohen and Sarah Wood for field assistance; Jack McFarland for sharing oxygen data; Eugénie Euskirchen, Jennifer Harden, and David McGuire for their participation in the APEX research program; and Jeff Chanton, Larry Miller and an anonymous reviewer for input that improved the manuscript. This material is based upon work supported, in part, by the U.S. Department of Energy, Office of Science, Office of Biological and Environmental Research under Award Number DE-SC-0010338; the U.S. National Aeronautics and Space Administration NASA grant NNX11AR16G; the USGS Climate Science Center and USGS Climate and Land R&D Program; and the USGS Mendenhall Postdoctoral Fellowship program. Research Experiences for Undergraduates (REU) funding and considerable logistic support were provided by the Bonanza Creek LTER Program, which is jointly funded by NSF (DEB 1026415) and the USDA Forest Service, Pacific Northwest Research Station (PNW01-JV112619320-16). Any use of trade names is for descriptive purposes only and does not imply endorsement by the U.S. Government. Data used in this publication are available on the Bonanza Creek LTER website (www.lter.uaf.edu/data.cfm).

Supplementary material

10533_2015_168_MOESM1_ESM.pdf (1.7 mb)
Supplementary material 1 (PDF 1770 kb)

References

  1. Abbott BW, Larouche JR, Jones JB Jr, Bowden WB, Balser AW (2014) Elevated dissolved organic carbon biodegradability from thawing and collapsing permafrost. J Geophys Res 119:2049–2063. doi: 10.1002/2014JG002678 CrossRefGoogle Scholar
  2. Armstrong W (1964) Oxygen diffusion from the roots of some British bog plants. Nature 204:801–802CrossRefGoogle Scholar
  3. Balesdent J, Mariotti A, Guillet B (1987) Natural 13C abundance as a tracer for studies of soil organic matter dynamics. Soil Biol Biochem 19:25–30CrossRefGoogle Scholar
  4. Blair N, Leu A, Muñoz E, Olsen J, Kwong E, Des Marais D (1985) Carbon isotopic fractionation in heterotrophic microbial metabolism. Appl Environ Microbiol 50:996–1001Google Scholar
  5. Blaser MB, Δreisbach LK, Conrad R (2013) Carbon isotope fractionation of 11 acetogenic strains grown on H2 and CO2. Appl Environ Microb 79:1787–1794. doi: 10.1128/AEM.03203-12 CrossRefGoogle Scholar
  6. Blazewicz SJ, Petersen DG, Waldrop MP, Firestone MK (2012) Anaerobic oxidation of methane in tropical and boreal soils: ecological significance in terrestrial methane cycling. J Geophys Res 117:G02033. doi: 10.1029/2011JG001864 Google Scholar
  7. Bloom AA, Palmer PI, Fraser A, Reay DS, Frankenberg C (2010) Large-scale controls of methanogenesis inferred from methane and gravity spaceborne data. Science 327:322–325. doi: 10.1126/science.1175176 CrossRefGoogle Scholar
  8. Botsch KC, Conrad R (2011) Fractionation of stable carbon isotopes during anaerobic production and degradation of propionate in defined microbial cultures. Org Geochem 42:289–295. doi: 10.1016/j.orggeochem.2011.01.005 CrossRefGoogle Scholar
  9. Botz R, Pokojski H-D, Schmitt M, Thomm M (1996) Carbon isotope fractionation during bacterial methanogenesis by CO2 reduction. Org Geochem 25:255–262CrossRefGoogle Scholar
  10. Bridgham SD, Cadillo-Quiroz H, Keller JK, Zhuang Q (2013) Methane emissions from wetlands: biogeochemical, microbial, and modeling perspectives from local to global scales. Glob Chang Biol 19:1325–1346. doi: 10.1111/gcb.12131 CrossRefGoogle Scholar
  11. Cadillo-Quiroz H, Brauer S, Yashiro E, Sun C, Yavitt J, Zinder S (2006) Vertical profiles of methanogenesis and methanogens in two contrasting acidic peatlands in central New York State, USA. Environ Microbiol 8:1428–1440. doi: 10.1111/j.1462-2920.2006.01036.x CrossRefGoogle Scholar
  12. Camill P (1999) Patterns of boreal permafrost peatland vegetation across environmental gradients sensitive to climate warming. Can J Bot 77:721–733Google Scholar
  13. Chambers FM, Beilman DW, Yu Z (2011) Methods for determining peat humification and for quantifying peat bulk density, organic matter and carbon content for palaeostudies of climate and peatland carbon dynamics. Mires Peat 7:1–10Google Scholar
  14. Chanton JP, Bauer JE, Glaser PH, Siegel DI, Kelley CA, Tyler SC, Romanowicz EH, Lazrus A (1995) Radiocarbon evidence for the substrates supporting methane formation within northern Minnesota peatlands. Geochim Cosmochim Acta 59:3663–3668CrossRefGoogle Scholar
  15. Chanton JP, Glaser PH, Chasar LS, Burdige DJ, Hines ME, Siegel DI, Tremblay LB, Cooper WT (2008) Radiocarbon evidence for the importance of surface vegetation on fermentation and methanogenesis in contrasting types of boreal peatlands. Global Biogeochem Cycles 22:GB4022. doi: 10.1029/2008GB003274 CrossRefGoogle Scholar
  16. Ciais P, Sabine C, Bala G, Bopp L, Brovkin V, Canadell J, Chhabra A, DeFries R, Galloway J, Heimann M, Jones C, Le Quéré C, Myneni RB, Piao S, Thornton P (2013) Carbon and other biogeochemical cycles. In: Stocker TF, Qin D, Plattner G-K, Tignor M, Allen SK, Boschung J, Nauels A, Xia Y, Bex V, Midgley PM (eds) Climate change 2013: the physical science basis. Contribution of working group I to the fifth assessment report of the intergovernmental panel on climate change. Cambridge University Press, CambridgeGoogle Scholar
  17. Conrad R (1999) Contribution of hydrogen to methane production and control of hydrogen concentrations in methanogenic soils and sediments. FEMS Microbiol Ecol 28:193–202CrossRefGoogle Scholar
  18. Conrad R (2005) Quantification of methanogenic pathways using stable carbon isotopic signatures: a review and a proposal. Org Geochem 36:739–752. doi: 10.1016/j.orggeochem.2004.09.006 CrossRefGoogle Scholar
  19. Conrad R, Bak F, Seitz HJ, Thebrath B, Mayer HP, Schutz H (1989) Hydrogen turnover by psychrotrophic homoacetogenic and mesophilic methanogenic bacteria in anoxic paddy soil and lake sediment. FEMS Microbiol Ecol 62:285–294CrossRefGoogle Scholar
  20. Conrad R, Claus P, Chidthaisong A, Lu Y, Fernandez Scavino A, Liu Y, Angel R, Galand PE, Casper P, Guerin F, Enrich-Prast A (2014) Stable carbon isotope biogeochemistry of propionate and acetate in methanogenic soils and lake sediments. Org Geochem 73:1–7. doi: 10.1016/j.orggeochem.2014.03.010 CrossRefGoogle Scholar
  21. Corbett JE, Tfaily MM, Burdige DJ, Cooper WT, Glaser PH, Chanton JP (2012) Partitioning pathways of CO2 production in peatlands with stable carbon isotopes. Biogeochem 114:327–340. doi: 10.1007/s10533-012-9813-1 CrossRefGoogle Scholar
  22. Corbett JE, Tfaily MM, Burdige DJ, Cooper WT, Glaser PH, Chanton JP (2013) Partitioning pathways of CO2 production in peatlands with stable carbon isotopes. Biogeochemistry 114:327–340. doi: 10.1007/s10533-012-9813-1 CrossRefGoogle Scholar
  23. Corbett JE, Tfaily MM, Burdige DJ, Glaser PH, Chanton JP (2015) The relative importance of methanogenesis in the decomposition of organic matter in northern peatlands. J Geophys Res 120:280–293. doi: 10.1002/(ISSN)2169-8961 CrossRefGoogle Scholar
  24. Dinel H, Mathur SP, Brown A, Lέvesque M (1988) A Field-Study of the effect of depth on methane production in peatland waters: equipment and preliminary results. J Ecol 76:1083–1091CrossRefGoogle Scholar
  25. Ding W, Cai Z, Tsuruta H (2004) Summertime variation of methane oxidation in the rhizosphere of a Carex dominated freshwater marsh. Atmos Environ 38:4165–4173. doi: 10.1016/j.atmosenv.2004.04.022 CrossRefGoogle Scholar
  26. Dise NB, Gorham E, Verry ES (1993) Environmental factors controlling methane emissions from peatlands in northern Minnesota. J Geophys Res 98:10583–10594CrossRefGoogle Scholar
  27. Euskirchen ES, Edgar CW, Turetsky MR, Waldrop MP, Harden JW (2014) Differential response of carbon fluxes to climate in three peatland ecosystems that vary in the presence and stability of permafrost. J Geophys Res 119:1576–1595. doi: 10.1002/2014JG002683 CrossRefGoogle Scholar
  28. Feisthauer S, Vogt C, Modrzynski J, Szlenkier M, Kruger M, Siegert M, Richnow HH (2011) Different types of methane monooxygenases produce similar carbon and hydrogen isotope fractionation patterns during methane oxidation. Geochim Cosmochim Acta 75:1173–1184. doi: 10.1016/j.gca.2010.12.006 CrossRefGoogle Scholar
  29. Galand PE, Fritze H, Conrad R, Yrjälä K (2005) Pathways for methanogenesis and diversity of methanogenic Archaea in three boreal peatland ecosystems. Appl Environ Microbiol 71:2195–2198. doi: 10.1128/AEM.71.4.2195-2198.2005 CrossRefGoogle Scholar
  30. Games LM, Hayes JM, Gunsalus RP (1978) Methane-producing bacteria: natural factionations of the stable carbon isotopes. Geochim Cosmochim Acta 42:1295–1297CrossRefGoogle Scholar
  31. Gelwicks JT, Risatti JB, Hayes JM (1994) Carbon isotope effects associated with aceticlastic methanogenesis. Appl Environ Microb 60:467–472Google Scholar
  32. Hines ME, Duddleston KN, Rooney-Varga JN, Fields D, Chanton JP (2008) Uncoupling of acetate degradation from methane formation in Alaskan wetlands: Connections to vegetation distribution: pathways of methanogenesis in wetlands. Glob Biogeochem Cycles 22: GB2017. doi:  10.1029/2006GB002903
  33. Hodgkins SB, Tfaily MM, McCalley CK, Logan TA, Crill PM, Saleska SR, Rich VI, Chanton JP (2014) Changes in peat chemistry associated with permafrost thaw increase greenhouse gas production. Proc Natl Acad Sci USA. doi: 10.1073/pnas.1314641111 Google Scholar
  34. Holmes ME, Chanton JP, Tfaily MM, Ogram A (2015) CO2 and CH4 isotope compositions and production pathways in a tropical peatland. Global Biogeochem Cycles 28:1–18. doi: 10.1002/2014GB004951 CrossRefGoogle Scholar
  35. Hultman J, Waldrop MP, Mackelprang R et al (2015) Multi-omics of permafrost, active layer and thermokarst bog soil microbiomes. Nature. doi: 10.1038/nature14238 Google Scholar
  36. Jahne B, Heinz G, Dietrich W (1987) Measurement of the diffusion coefficients of sparingly soluble gases in water. J Geophys Res 92(C10):10767–10776CrossRefGoogle Scholar
  37. Johnston CE, Ewing SA, Harden JW et al (2014) Effect of permafrost thaw on CO2 and CH4 exchange in a western Alaska peatland chronosequence. Environ Res Lett 9:085004. doi: 10.1088/1748-9326/9/8/085004 CrossRefGoogle Scholar
  38. Jones JG, Simon BM (1985) Interaction of acetogens and methanogens in anaerobic freshwater sediments. Appl Environ Microbiol 49:944–948Google Scholar
  39. Jones MC, Booth RK, Yu Z, Ferry P (2012) A 2200-year record of permafrost dynamics and carbon cycling in a collapse-scar bog, Interior Alaska. Ecosyst 16:1–19. doi: 10.1007/s10021-012-9592-5 CrossRefGoogle Scholar
  40. Keller JK, Weisenhorn PB, Megonigal JP (2009) Humic acids as electron acceptors in wetland decomposition. Soil Biol Biochem 41:1518–1522. doi: 10.1016/j.soilbio.2009.04.008 CrossRefGoogle Scholar
  41. Keuper F, van Bodegom PM, Dorrepaal E, Weedon J, van Hal J, van Logtestijn RSP, Aerts R (2012) A frozen feast: thawing permafrost increases plant-available nitrogen in subarctic peatlands. Global Chang Biol 18:1998–2007. doi: 10.1111/j.1365-2486.2012.02663.x CrossRefGoogle Scholar
  42. Klapstein SJ, Turetsky MR, McGuire AD, Harden JW, Czimczik CI, Xu X, Chanton JP, Waddington JM (2014) Controls on methane released through ebullition in peatlands affected by permafrost degradation. J Geophys Res 119:418–431. doi: 10.1002/2013JG002441 CrossRefGoogle Scholar
  43. Kotsyurbenko OR, Nozhevnikova AN, Zavarzin GA (1993) Methanogenic degradation of organic-matter by anaerobic bacteria at low temperature. Chemosphere 27:1745–1761CrossRefGoogle Scholar
  44. Kotsyurbenko OR, Glagolev MV, Nozhevnikova AN, Conrad R (2001) Competition between homoacetogenic bacteria and methanogenic archaea for hydrogen at low temperature. FEMS Microbiol Ecol 38:153–159CrossRefGoogle Scholar
  45. Kotsyurbenko OR, Chin K-J, Glagolev MV, Stubner S, Simankova MV, Nozhevnikova AN, Conrad R (2004) Acetoclastic and hydrogenotrophic methane production and methanogenic populations in an acidic West-Siberian peat bog. Environ Microbiol 6:1159–1173. doi: 10.1111/j.1462-2920.2004.00634.x CrossRefGoogle Scholar
  46. Levy ZF, Siegel DI, Dasgupta SS, Glaser PH, Welker JM (2013) Stable isotopes of water show deep seasonal recharge in northern bogs and fens. Hydrol Process 28:4938–4952. doi: 10.1002/hyp.9983 CrossRefGoogle Scholar
  47. Londry KL, Dawson KG, Grover HD, Summons RE, Bradley AS (2008) Stable carbon isotope fractionation between substrates and products of Methanosarcina barkeri. Org Geochem 39:608–621. doi: 10.1016/j.orggeochem.2008.03.002 CrossRefGoogle Scholar
  48. Moore TR, Knowles R (1990) Methane emissions from fen, bog and swamp peatlands in Quebec. Biogeochemistry 11:45–61CrossRefGoogle Scholar
  49. O’Leary MH (1988) Carbon isotopes in photosynthesis. Bioscience 38:328–336CrossRefGoogle Scholar
  50. Penning H, Conrad R (2006) Carbon isotope effects associated with mixed-acid fermentation of saccharides by Clostridium papyrosolvens. Geochim Cosmochim Acta 70:2283–2297. doi: 10.1016/j.gca.2006.01.017 CrossRefGoogle Scholar
  51. Popp TJ, Chanton JP, Whiting GJ, Grant N (1999) Methane stable isotope distribution at a Carex dominated fen in north central Alberta. Glob Biogeochem Cycles 13:1063–1077. doi: 10.1029/1999GB900060 CrossRefGoogle Scholar
  52. Popp TJ, Chanton JP, Whiting GJ, Grant N (2000) Evaluation of methane oxidation in therhizosphere of a Carex dominated fen in northcentral Alberta, Canada. Biogeochem 51:259–281CrossRefGoogle Scholar
  53. Prater JL, Chanton JP, Whiting GJ (2007) Variation in methane production pathways associated with permafrost decomposition in collapse scar bogs of Alberta, Canada. Glob Biogeochem Cycles 21: GB4004. doi:  10.1029/2006GB002866
  54. Preuss I, Knoblauch C, Gebert J, Pfeiffer EM (2013) Improved quantification of microbial CH4 oxidation efficiency in arctic wetland soils using carbon isotope fractionation. Biogeoscience 10:2539–2552. doi: 10.5194/bg-10-2539-2013 CrossRefGoogle Scholar
  55. Segers R (1998) Methane production and methane consumption: a review of processes underlying wetland methane fluxes. Biogeochemistry 41:23–51CrossRefGoogle Scholar
  56. Shea KM (2010) Physical and ecological controls on methane release from a boreal peatland in Interior Alaska. Dissertation, University of GuelphGoogle Scholar
  57. Shoemaker JK, Schrag DP (2010) Subsurface characterization of methane production and oxidation from a New Hampshire wetland. Geobiol 8:234–243. doi: 10.1111/j.1472-4669.2010.00239.x CrossRefGoogle Scholar
  58. Shoemaker JK, Varner RK, Schrag DP (2012) Characterization of subsurface methane production and release over 3 years at a New Hampshire wetland. Geochim et Cosmochim Acta 91:120–139. doi: 10.1016/j.gca.2012.05.029 CrossRefGoogle Scholar
  59. Stumm W, Morgan JJ (1996) Aquatic Chemistry. Wiley, New YorkGoogle Scholar
  60. Tfaily MM, Hamdan R, Corbett JE, Chanton JP, Glaser PH, Cooper WT (2013) Investigating dissolved organic matter decomposition in northern peatlands using complimentary analytical techniques. Geochim Cosmochim Acta 112:116–129. doi: 10.1016/j.gca.2013.03.002 CrossRefGoogle Scholar
  61. Thomas B, Arthur MA (2010) Correcting porewater concentration measurements from peepers: application of a reverse tracer. Limnol Oceanogr 8:403–413. doi: 10.4319/lom.2010.8.403 CrossRefGoogle Scholar
  62. Turetsky MR, Wieder RK, Vitt DH, Evans RJ, Scott KD (2007) The disappearance of relict permafrost in boreal north America: effects on peatland carbon storage and fluxes. Glob Chang Biol 13:1922–1934. doi: 10.1111/j.1365-2486.2007.01381.x CrossRefGoogle Scholar
  63. Turetsky MR, Kotowska A, Bubier J et al (2014) A synthesis of methane emissions from 71 northern, temperate, and subtropical wetlands. Glob Chang Biol 20:2183–2197. doi: 10.1111/gcb.12580 CrossRefGoogle Scholar
  64. Tveit A, Schwacke R, Svenning MM, Urich T (2012) Organic carbon transformations in high-Arctic peat soils: key functions and microorganisms. ISME J 7:299–331CrossRefGoogle Scholar
  65. Tveit AT, Urich T, Svenning MM (2014) Metatranscriptomic analysis of arctic peat soil microbiota. Appl Environ Microbiol 80:5761–5772. doi: 10.1128/AEM.01030-14 CrossRefGoogle Scholar
  66. Valentine DW, Holland E, Schimel D (1994) Ecosystem and physiological controls over methane production in northern wetlands. J Geophys Res 99(D1):1563–1571CrossRefGoogle Scholar
  67. Valentine DL, Chidthaisong A, Rice A, Reeburgh WS, Tyler SC (2004) Carbon and hydrogen isotope fractionation by moderately thermophilic methanogens. Geochim Cosmochim Acta 68:1571–1590. doi: 10.1016/j.gca.2003.10.012 CrossRefGoogle Scholar
  68. van den Pol-van Dasselaar A, Oenema O (1999) Methane production and carbon mineralisation of size and density fractions of peat soils. Soil Biol Biochem 31:877–886CrossRefGoogle Scholar
  69. van der Nat F, Middelburg JJ (1998) Seasonal variation in methane oxidation by the rhizosphere of Phragmites australis and Scirpus lacustris. Aquat Bot 61:95–110CrossRefGoogle Scholar
  70. Van Hulzen JB, Segers R, van Bodegom PM, Leffelaar PA (1999) Temperature effects on soil methane production: an explanation for observed variability. Soil Biol Biochem 31:1919–1929CrossRefGoogle Scholar
  71. van Winden JF, Reichart G-J, McNamara NP, Benthien A, Damste JSS (2012) Temperature-induced increase in methane release from peat bogs: a mesocosm experiment. PLoS ONE 7:e39614. doi: 10.1371/journal.pone.0039614.g003 CrossRefGoogle Scholar
  72. Whiticar MJ (1999) Carbon and hydrogen isotope systematics of bacterial formation and oxidation of methane. Chem Geol 161:291–314CrossRefGoogle Scholar
  73. Wuebbles D, Hayhoe K (2002) Atmospheric methane and global change. Earth-Sci Rev 57:177–210CrossRefGoogle Scholar
  74. Ye R, Jin Q, Bohannan B, Keller JK, Bridgham SD (2014) Homoacetogenesis: a potentially underappreciated carbon pathway in peatlands. Soil Biol Biochem. doi: 10.1016/j.soilbio.2013.10.020 Google Scholar

Copyright information

© Springer International Publishing Switzerland 2015

Authors and Affiliations

  • Rebecca B. Neumann
    • 1
  • Steven J. Blazewicz
    • 2
    • 4
  • Christopher H. Conaway
    • 2
  • Merritt R. Turetsky
    • 3
  • Mark P. Waldrop
    • 2
  1. 1.Department of Civil and Environmental EngineeringUniversity of WashingtonSeattleUSA
  2. 2.U.S. Geological SurveyMenlo ParkUSA
  3. 3.Department of Integrative BiologyUniversity of GuelphOntarioCanada
  4. 4.Lawrence Livermore National LaboratoryLivermoreUSA

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