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Methane fluxes and the functional groups of methanotrophs and methanogens in a young Arctic landscape on Disko Island, West Greenland

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Abstract

Arctic soils are known to be important methane (CH4) consumers and sources. This study integrates in situ fluxes of CH4 between upland and wetland soils with potential rates of CH4 oxidation and production as well as abundance and diversity of the methanotrophs and methanogens measured with pyrosequencing of 16S DNA and rRNA fragments in soil and permafrost layers. Here, the spatial patterns of in situ CH4 fluxes for a 2,000 years old Arctic landscape in West Greenland reveal similar CH4 uptake rates (−4 ± 0.3 μmol m−2 h−1) as in other Arctic sites, but lower CH4 emissions (14 ± 1.5 μmol m−2 h−1) at wetland sites compared to other Arctic wetlands. Potential CH4 oxidation was similar for upland and wetland soils, but the wetter soils produced more CH4 in active and permafrost layers. Accordingly, the abundance of methanogenic archaea was highest in wetland soils. The methanotrophic community also differed between upland and wetland soils, with predominant activity of Type II methanotrophs in the active layer for upland soils, but only Type I methanotrophs for the wetland. In the permafrost of upland and wetland soils, activity of the methanotrophs belonging to Type I and Type II as well as methanogens were detected. This study indicates that the magnitude of CH4 oxidation and the direction of the flux, i.e. uptake or emission, are linked to different methanotrophic communities in upland and wetland soils. Also, the observed link between production/consumption rates and the microbial abundance and activity indicates that the age of an Arctic landscape is not important for the CH4 consumption but can be very important for CH4 production. Considering the prevalence of dry landscapes and contrasting ages of high Arctic soils, our results highlight that well-drained soils should not be overlooked as an important component of Arctic net CH4 budget.

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References

  • Askaer L, Elberling B, Friborg T et al (2011) Plant-mediated CH4 transport and C gas dynamics quantified in situ in a Phalaris arundinacea-dominant wetland. Plant Soil 343:287–301. doi:10.1007/s11104-011-0718-x

    Article  Google Scholar 

  • Bååth E, Pettersson M, Söderberg KH (2001) Adaptation of a rapid and economical microcentrifugation method to measure thymidine and leucine incorporation by soil bacteria. Soil Biol Biochem 33:1571–1574. doi:10.1016/S0038-0717(01)00073-6

    Article  Google Scholar 

  • Barbier B, Dziduch I, Liebner S et al (2012) Methane-cycling communities in a permafrost-affected soil on Herschel Island, Western Canadian Arctic: active layer profiling of mcrA and pmoA genes. FEMS Microbiol Ecol 82:287–302. doi:10.1111/j.1574-6941.2012.01332.x

    Article  Google Scholar 

  • Barcena TG, Yde JC, Finster KW (2010) Methane flux and high-affinity methanotrophic diversity along the chronosequence of a receding glacier in Greenland. Ann Glaciol 51:23–31

    Article  Google Scholar 

  • Bárcena TG, Finster KW, Yde JC (2011) Spatial Patterns of Soil Development, Methane Oxidation, and Methanotrophic Diversity along a Receding Glacier Forefield, Southeast Greenland. Arctic, Antarct Alp Res 43:178–188. doi:10.1657/1938-4246-43.2.178

    Article  Google Scholar 

  • Bender M, Conrad R (1992) Kinetics of CH4 oxidation in oxic soils exposed to ambient air or high CH4 mixing ratios. FEMS Microbiol Ecol 101:261–269. doi:10.1016/0168-6496(92)90043-S

    Google Scholar 

  • Bender M, Conrad R (1995) Effect of CH4 concentrations and soil conditions on the induction of CH4 oxidation activity. Soil Biol Biochem 27:1517–1527

    Article  Google Scholar 

  • Bengtson P, Basiliko N, Dumont MG et al (2009) Links between methanotroph community composition and CH4 oxidation in a pine forest soil. FEMS Microbiol Ecol 70:356–366. doi:10.1111/j.1574-6941.2009.00751.x

    Article  Google Scholar 

  • Brandt KK, Jørgensen NOG, Nielsen TH, Winding A (2004) Microbial community-level toxicity testing of linear alkylbenzene sulfonates in aquatic microcosms. FEMS Microbiol Ecol 49:229–241. doi:10.1016/j.femsec.2004.03.006

    Article  Google Scholar 

  • Brummell ME, Farrell RE, Hardy SP, Siciliano SD (2014) Greenhouse gas production and consumption in High Arctic deserts. Soil Biol Biochem 68:158–165. doi:10.1016/j.soilbio.2013.09.034

    Article  Google Scholar 

  • Caporaso JG, Kuczynski J, Stombaugh J et al (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336. doi:10.1038/nmeth.f.303

    Article  Google Scholar 

  • Christensen TR, Friborg T, Sommerkorn M et al (2000) Trace gas exchange in a high-arctic valley. 1. Variation in CO2 and CH4 flux between tundra vegetation types. Glob Biogeochem Cycles 14:701–713

    Article  Google Scholar 

  • Corley J (2003) Best practices in establishing detection and quantification limits for pesticide residues in foods. In: Lee P, Aizawa H, Barefoot A, Murphy J (eds) Handbook of residue analytical methods for agrochemistry. Wiley, New York, pp 1–18

    Google Scholar 

  • Curry CL (2009) The consumption of atmospheric methane by soil in a simulated future climate. Biogeosci Discuss 6:6077–6110. doi:10.5194/bgd-6-6077-2009

    Article  Google Scholar 

  • Dedysh S, Horz H-P, Dunfield P, Liesack W (2002) A novel pmoA lineage represented by the acidophilic methanotrophic bacterium Methylocapsa acidophila B2. Arch Microbiol 177:200. doi:10.1007/s00203-001-0385-z

    Article  Google Scholar 

  • DeSantis TZ, Hugenholtz P, Larsen N et al (2006) Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol 72:5069–5072. doi:10.1128/AEM.03006-05

    Article  Google Scholar 

  • Dunfield PF, Knowles R, Dumont R, Moore TR (1993) Methane production and consumption in temperate and subarctic peat soils: response to temperature and pH. Soil Biol Biochem 25:321–326

    Article  Google Scholar 

  • Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461. doi:10.1093/bioinformatics/btq461

    Article  Google Scholar 

  • Emmerton CA, St. Louis VL, Lehnherr I et al (2014) The net exchange of methane with high Arctic landscapes during the summer growing season. Biogeosciences 11:3095–3106. doi:10.5194/bg-11-3095-2014

    Article  Google Scholar 

  • Funder S, Hansen L (1996) The Greenland ice sheet—a model for its culmination and decay during and after the last glacial maximum. Bull Geol Soc Den 42:137–152

    Google Scholar 

  • Ganzert L, Jurgens G, Münster U, Wagner D (2007) Methanogenic communities in permafrost-affected soils of the Laptev Sea coast, Siberian Arctic, characterized by 16S rRNA gene fingerprints. FEMS Microbiol Ecol 59:476–488. doi:10.1111/j.1574-6941.2006.00205.x

    Article  Google Scholar 

  • Graef C, Hestnes AG, Svenning MM, Frenzel P (2011) The active methanotrophic community in a wetland from the high arctic. Environ Microbiol Rep 3:466–472. doi:10.1111/j.1758-2229.2010.00237.x

    Article  Google Scholar 

  • Griffiths RI, Whiteley AS, O’Donnell AG, Bailey MJ (2000) Rapid method for coextraction of DNA and RNA from natural environments for analysis of ribosomal DNA- and rRNA-based microbial community composition. Appl Environ Microbiol 66:5488–5491. doi:10.1128/AEM.66.12.5488-5491.2000

    Article  Google Scholar 

  • Hansen BU, Elberling B, HumLum O, Nielsen N (2006) Meteorological trends (1991–2004) at Arctic Station, Central West Greenland (69°15′N) in a 130 years perspective. Geogr Tidsskr J Geogr 106:45–56

    Article  Google Scholar 

  • Hanson RS, Hanson TE (1996) Methanotrophic bacteria. Microbiol Rev 60:439–471

    Google Scholar 

  • Haroon MF, Hu S, Shi Y et al (2013) Anaerobic oxidation of methane coupled to nitrate reduction in a novel archaeal lineage. Nature 500:567–570. doi:10.1038/nature12375

    Article  Google Scholar 

  • Høj L, Olsen RA, Torsvik VL (2005) Archaeal communities in High Arctic wetlands at Spitsbergen, Norway (78 degrees N) as characterized by 16S rRNA gene fingerprinting. FEMS Microbiol Ecol 53:89–101. doi:10.1016/j.femsec.2005.01.004

    Article  Google Scholar 

  • Humlum O, Christiansen HH, Hansen BU, Hasholt B, Jakobsen BH, Nielsen N, Rasch M (1995) Holocene landscape evolution in the Mellemfjord area, Disko Island, central West Greenland: area presentation and preliminary results. Geogr Tidsskr J Geogr 95:28–41

  • Jensen LA, Schmidt LB, Hollesen J, Elberling B (2006) Accumulation of Soil Organic Carbon Linked to Holocene Sea Level Changes in West Greenland. Arctic, Antarct Alp Res 38:378–383

    Article  Google Scholar 

  • Knoblauch C, Zimmermann U, Blumenberg M et al (2008) Methane turnover and temperature response of methane-oxidizing bacteria in permafrost-affected soils of northeast Siberia. Soil Biol Biochem 40:3004–3013. doi:10.1016/j.soilbio.2008.08.020

    Article  Google Scholar 

  • Kolb S (2009) The quest for atmospheric methane oxidizers in forest soils. Environ Microbiol Rep 1:336–346

    Article  Google Scholar 

  • Liebner S, Wagner D (2007) Abundance, distribution and potential activity of methane oxidizing bacteria in permafrost soils from the Lena Delta, Siberia. Environ Microbiol 9:107–117. doi:10.1111/j.1462-2920.2006.01120.x

    Article  Google Scholar 

  • Liebner S, Rublack K, Stuehrmann T, Wagner D (2009) Diversity of aerobic methanotrophic bacteria in a permafrost active layer soil of the Lena Delta, Siberia. Microb Ecol 57:25–35. doi:10.1007/s00248-008-9411-x

    Article  Google Scholar 

  • Lupascu AM, Wadham JL, Hornibrook ERC et al (2012) Temperature sensitivity of methane production in the permafrost active layer at Stordalen, Sweden : a Comparison with Non-permafrost Northern Wetlands. Arctic, Antarct Alp Res 44:469–482

    Article  Google Scholar 

  • Mackelprang R, Waldrop MP, DeAngelis KM et al (2011) Metagenomic analysis of a permafrost microbial community reveals a rapid response to thaw. Nature 480:368–371. doi:10.1038/nature10576

    Article  Google Scholar 

  • Martineau C, Whyte LG, Greer CW (2010) Stable isotope probing analysis of the diversity and activity of methanotrophic bacteria in soils from the Canadian high Arctic. Appl Environ Microbiol 76:5773–5784. doi:10.1128/AEM.03094-09

    Article  Google Scholar 

  • Martineau C, Pan Y, Bodrossy L et al. (2014) Atmospheric methane oxidizers are present and active in Canadian high Arctic soils. FEMS Microbiol Ecol 1–13. doi: 10.1111/1574-6941.12287

  • Michel PH, Bloem J (1993) Conversion factors for estimation of cell production-rates of soil bacteria from [H-3] thymidine and [H-3] Leucine Incorporation. Soil Biol Biochem 25:943–950

    Article  Google Scholar 

  • Moosavi S, Crill PM (1998) CH4 oxidation by tundra wetlands as measured by a selective inhibitor technique. J Geophys Res 103:29093–29106

    Article  Google Scholar 

  • Nauer P, Dam B, Liesack W et al (2012) Activity and diversity of methane-oxidizing bacteria in glacier forefields on siliceous and calcareous bedrock. Biogeosciences 9:2259–2274. doi:10.5194/bg-9-2259-2012

    Article  Google Scholar 

  • Nielsen N (1969) Morphological studies on the eastern coast of Disko, West Greenland. Geogr Tidsskr J Geogr 68:1–34

    Google Scholar 

  • Olefeldt D, Turetsky MR, Crill PM, McGuire aD (2013) Environmental and physical controls on northern terrestrial methane emissions across permafrost zones. Glob Chang Biol 19:589–603. doi:10.1111/gcb.12071

    Article  Google Scholar 

  • Pihlatie MK, Christiansen JR, Aaltonen H et al (2013) Comparison of static chambers to measure CH4 emissions from soils. Agric For Meteorol 171:124–136. doi:10.1016/j.agrformet.2012.11.008

    Article  Google Scholar 

  • Ricke P, Kube M, Nakagawa S et al (2005) First genome data from uncultured upland soil cluster alpha methanotrophs provide further evidence for a close phylogenetic relationship to Methylocapsa acidiphila B2 and for high-affinity methanotrophy involving particulate methane monooxygenase. Appl Environ Microbiol 71:7472–7482. doi:10.1128/AEM.71.11.7472-7482.2005

    Article  Google Scholar 

  • Rousk J, Frey SD, Bååth E (2012) Temperature adaptation of bacterial communities in experimentally warmed forest soils. Glob Chang Biol 18:3252–3258. doi:10.1111/j.1365-2486.2012.02764.x

    Article  Google Scholar 

  • Shrestha PM, Kammann C, Lenhart K et al (2012) Linking activity, composition and seasonal dynamics of atmospheric methane oxidizers in a meadow soil. ISME J 6:1115–1126. doi:10.1038/ismej.2011.179

    Article  Google Scholar 

  • Skiba U, Drewer J, Tang YS et al (2009) Biosphere–atmosphere exchange of reactive nitrogen and greenhouse gases at the NitroEurope core flux measurement sites: measurement strategy and first data sets. Agric Ecosyst Environ 133:139–149. doi:10.1016/j.agee.2009.05.018

    Article  Google Scholar 

  • Smith K, Dobbie KE, Ball BC et al (2000) Oxidation of atmospheric methane in Northern European soils, comparison with other ecosystems, and uncertainties in the global terrestrial sink. Glob Chang Biol 6:791–803. doi:10.1046/j.1365-2486.2000.00356.x

    Article  Google Scholar 

  • Stoecker K, Bendinger B, Schöning B et al (2006) Cohn’s Crenothrix is a filamentous methane oxidizer with an unusual methane monooxygenase. Proc Natl Acad Sci USA 103:2363–2367. doi:10.1073/pnas.0506361103

    Article  Google Scholar 

  • Thauer RK (1998) Biochemistry of methanogenesis: a tribute to Marjory Stephenson. 1998 Marjory Stephenson prize lecture. Microbiology 144(Pt 9):2377–2406. doi:10.1099/00221287-144-9-2377

    Article  Google Scholar 

  • Torn MS, Harte J (1996) Methane consumption by montane soils: implications for positive and negative feedback with climatic change. Biogeochemistry 32:53–67

    Article  Google Scholar 

  • Trotsenko Ya, Khmelenina VN (2005) Aerobic methanotrophic bacteria of cold ecosystems. FEMS Microbiol Ecol 53:15–26. doi:10.1016/j.femsec.2005.02.010

    Article  Google Scholar 

  • Trotsenko Ya, Murrell JC (2008) Metabolic aspects of aerobic obligate methanotrophy. Adv Appl Microbiol 63:183–229. doi:10.1016/S0065-2164(07)00005-6

    Article  Google Scholar 

  • Turunen J, Tahvanainen T, Tolonen K, Pitkänen A (2001) Carbon accumulation in West Siberian mires, Russia. Glob Biogeochem Cycles 15:285–296

    Article  Google Scholar 

  • Turunen J, Tomppo E, Tolonen K, Reinikainen A (2002) Estimating carbon accumulation rates of undrained mires in Finland—application to boreal and subarctic regions. Holocene 12:69–80. doi:10.1191/0959683602hl522rp

    Article  Google Scholar 

  • Tveit A, Schwacke R, Svenning MM, Urich T (2013) Organic carbon transformations in high-Arctic peat soils: key functions and microorganisms. ISME J 7:299–311. doi:10.1038/ismej.2012.99

    Article  Google Scholar 

  • van Bellen S, Garneau M, Booth RK (2011) Holocene carbon accumulation rates from three ombrotrophic peatlands in boreal Quebec, Canada: impact of climate-driven ecohydrological change. The Holocene 21:1217–1231. doi:10.1177/0959683611405243

    Article  Google Scholar 

  • Wagner S, Reicosky D, Alessi R (1997) Regression models for calculating gas fluxes measured with a closed chamber. Agron J 89:279–284

    Article  Google Scholar 

  • Wagner D, Kobabe S, Pfeiffer E-M, Hubberten H-W (2003) Microbial controls on methane fluxes from a polygonal tundra of the Lena Delta, Siberia. Permafr Periglac Process 14:173–185. doi:10.1002/ppp.443

    Article  Google Scholar 

  • Wagner D, Lipski A, Embacher A, Gattinger A (2005) Methane fluxes in permafrost habitats of the Lena Delta: effects of microbial community structure and organic matter quality. Environ Microbiol 7:1582–1592. doi:10.1111/j.1462-2920.2005.00849.x

    Article  Google Scholar 

  • Walker D, Gould W, Maier H, Raynolds MK (2002) The circumpolar Arctic vegetation map: aVHRR-derived base maps, environmental controls, and integrated mapping procedures. Int J Remote Sens 23:4551–4570. doi:10.1080/01431160110113854

    Article  Google Scholar 

  • Whalen SC, Reeburgh WS (1990) Consumption of atmospheric methane by tundra soils. Nature 346:160–162

    Article  Google Scholar 

  • Yergeau E, Hogues H, Whyte LG, Greer CW (2010) The functional potential of high Arctic permafrost revealed by metagenomic sequencing, qPCR and microarray analyses. ISME J 4:1206–1214. doi:10.1038/ismej.2010.41

    Article  Google Scholar 

  • Yu Y, Lee C, Kim J, Hwang S (2005) Group-specific primer and probe sets to detect methanogenic communities using quantitative real-time polymerase chain reaction. Biotechnol Bioeng 89:670–679. doi:10.1002/bit.20347

    Article  Google Scholar 

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Acknowledgments

We gratefully acknowledge financial support to this study from the Danish National Research Foundation (CENPERM DNRF100) as well as PERMAGAS, Geocenter Danmark project 6-2010 and the Faculty of Science at University of Copenhagen. Lars Hestbjerg and Carsten Suhr at the Geological Survey of Denmark and Greenland (GEUS) are thanked for support to carry out the molecular work and pyro-sequencing at the molecular biology laboratory at GEUS. Also, we extend our gratitude to the students being involved in field measurements, to the staff from Arctic Station for providing the logistical support and many comments and constructive suggestions made by journal reviewers.

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Christiansen, J.R., Romero, A.J.B., Jørgensen, N.O.G. et al. Methane fluxes and the functional groups of methanotrophs and methanogens in a young Arctic landscape on Disko Island, West Greenland. Biogeochemistry 122, 15–33 (2015). https://doi.org/10.1007/s10533-014-0026-7

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