Abstract
Aims
The contribution of boreal forest plants to the methane (CH4) cycle is still uncertain. We studied the above and belowground CH4 fluxes of common boreal plants, and assessed the possible contribution of CH4 producing and oxidizing microbes (methanogens and methanotrophs, respectively) to the fluxes.
Methods
We measured the CH4 fluxes and the amounts of methanogens and methanotrophs in the above- and belowground parts of Vaccinium myrtillus, Vaccinium vitis-idaea, Calluna vulgaris and Pinus sylvestris seedlings and in non-planted soil in a microcosm experiment.
Results
The shoots of C. vulgaris and P. sylvestris showed on average emissions of CH4, while the shoots of the Vaccinium species indicated small CH4 uptake. All the root-soil-compartments consumed CH4, however, the non-rooted soils showed on average small CH4 emission. We found methanotrophs from all the rooted and non-rooted soils. Methanogens were not detected in the plant or soil materials.
Conclusions
The presence of plant roots seem to increase the amount of methanotrophs and thus CH4 uptake in the soil. The CH4 emissions from the shoots of C. vulgaris and P. sylvestris demonstrate that the plants have an important contribution to the CH4 exchange dynamics in the plant-soil systems.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Adamczyk B, Ahvenainen A, Sietiö O-M, Kanerva S, Kieloaho A-J, Smolander A, Kitunen V, Saranpää P, Laakso T, Straková P, Heinonsalo J (2016) The contribution of ericoid plants to soil nitrogen chemistry and organic matter decomposition in boreal forest soil. Soil Biol Biochem 103:394–404. https://doi.org/10.1016/j.soilbio.2016.09.016
Amaral JA, Knowles R (1997) Inhibition of methane consumption in forest soils and pure cultures of methanotrophs by aqueous forest soil extracts. Soil Biol Biochem 29:1713–1720. https://doi.org/10.1016/S0038-0717(97)00070-9
Andersen BL, Bidoglio G, Leip A, Rembges D (1998) A new method to study simultaneous methane oxidation and methane production in soils. Glob Biogeochem Cycles 12:587–594. https://doi.org/10.1029/98GB01975
Angel R, Matthies D, Conrad R (2011) Activation of methanogenesis in arid biological soil crusts despite the presence of oxygen. PLoS One 6:1–8. https://doi.org/10.1371/journal.pone.0020453
Angel R, Claus P, Conrad R (2012) Methanogenic archaea are globally ubiquitous in aerated soils and become active under wet anoxic conditions. ISME J 6:847–862. https://doi.org/10.1038/ismej.2011.141
Aronson EL, Helliker BR (2010) Methane flux in non-wetland soils in response to nitrogen addition: a meta-analysis. Ecology 91:3242–3251. https://doi.org/10.1890/09-2185.1
Auman AJ, Speake CC, Lidstrom ME (2001) nifH sequences and nitrogen fixation in type I and type II methanotrophs. Appl Environ Microbiol 67:4009–4016. https://doi.org/10.1128/AEM.67.9.4009
Berry FH, Beaton JA (1972) Decay in oak in the central hardwood region. USDA for Serv Res Pap NE-242:11 pp.
Bloom AA, Lee-Taylor J, Madronich S, Messenger DJ, Palmer PI, Reay DS, McLeod AR (2010) Global methane emission estimates from ultraviolet irradiation of terrestrial plant foliage. New Phytol 187:417–425. https://doi.org/10.1111/j.1469-8137.2010.03259.x
Bomberg M, Münster U, Pumpanen J, Ilvesniemi H, Heinonsalo J (2011) Archaeal communities in boreal forest tree rhizospheres respond to changing soil temperatures. Microb Ecol 62:205–217. https://doi.org/10.1007/s00248-011-9837-4
Bourne DG, McDonald IR, Murrell JC (2001) Comparison of pmoA PCR primer sets as tools for investigating methanotroph diversity in three Danish soils. Appl Environ Microbiol 67:3802–3809. https://doi.org/10.1128/AEM.67.9.3802–3809.2001
Broeckling CD, Broz AK, Bergelson J, Manter DK, Vivanco JM (2008) Root exudates regulate soil fungal community composition and diversity. Appl Environ Microbiol 74:738–744. https://doi.org/10.1128/AEM.02188-07
Bruhn D, Mikkelsen TN, Øbro J, Willats WGT, Ambus P (2009) Effects of temperature, ultraviolet radiation and pectin methyl esterase on aerobic methane release from plant material. Plant Biol 11:43–48. https://doi.org/10.1111/j.1438-8677.2009.00202.x
Bruhn D, Mikkelsen TN, Rolsted MMM, Egsgaard H, Ambus P (2014) Leaf surface wax is a source of plant methane formation under UV radiation and in the presence of oxygen. Plant Biol 16:512–516. https://doi.org/10.1111/plb.12137
Carmichael MJ, Bernhardt ES, Bräuer SL, Smith WK (2014) The role of vegetation in methane flux to the atmosphere: should vegetation be included as a distinct category in the global methane budget? Biogeochemistry 119:1–24. https://doi.org/10.1007/s10533-014-9974-1
Cicerone RJ, Shetter JD (1981) Sources of atmospheric methane: measurements in rice paddies and a discussion. J Geophys Res 86:7203–7209. https://doi.org/10.1029/JC086iC08p07203
Corley J (2003) Best practices in establishing detection and quantification limits for pesticide residues in foods. In: Lee PW, Aizawa H, Barefoot AC, Murphy JJ, Roberts T (eds) Handbook of residue analytical methods for agrochemicals. John Wiley & Sons Ltd, Chichester, pp 59–75
Costello AM, Lidstrom ME (1999) Molecular characterization of functional and phylogenetic genes from natural populations of methanotrophs in lake sediments. Appl Environ Microbiol 65:5066–5074
Covey KR, Wood SA, Warren RJ, Lee X, Bradford MA (2012) Elevated methane concentrations in trees of an upland forest. Geophys Res Lett 39:L15705. https://doi.org/10.1029/2012GL052361
Dam B, Dam S, Kube M, Reinhardt R, Liesack W (2012) Complete genome sequence of Methylocystis sp. strain SC2, an aerobic methanotroph with high-affinity methane oxidation potential. J Bacteriol 194:6008–6009. https://doi.org/10.1128/JB.01446-12
Ding W, Cai Z, Tsuruta H (2005) Plant species effects on methane emissions from freshwater marshes. Atmos Environ 39:3199–3207. https://doi.org/10.1016/j.atmosenv.2005.02.022
FAO/UNESCO (1990) FAO–UNESCO soil map of the world: revised legend. In: World Soil Resources Report 60. Food and Agriculture Organization of the United Nations (FAO), Rome
Gauci V, Gowing DJG, Hornibrook ERC, Davis JM, Dise NB (2010) Woody stem methane emission in mature wetland alder trees. Atmos Environ 44:2157–2160. https://doi.org/10.1016/j.atmosenv.2010.02.034
Goebel NL, Turk KA, Achilles KM, Paerl R, Hewson I, Morrison AE, Montoya JP, Edwards CA, Zehr JP (2010) Abundance and distribution of major groups of diazotrophic cyanobacteria and their potential contribution to N2 fixation in the tropical Atlantic Ocean. Environ Microbiol 12:3272–3289. https://doi.org/10.1111/j.1462-2920.2010.02303.x
Gulledge J, Hrywna Y, Cavanaugh C, Steudler PA (2004) Effects of long-term nitrogen fertilization on the uptake kinetics of atmospheric methane in temperate forest soils. FEMS Microbiol Ecol 49:389–400. https://doi.org/10.1016/j.femsec.2004.04.013
Hartmann DJ, Klein Tank AMG, Rusticucci M et al (2013) Observations: atmosphere and surface. 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, Cambridge, New York, pp 159–254
Ho A, de Roy K, Thas O, De Neve J, Hoefman S, Vandamme P, Heylen K, Boon N (2014) The more, the merrier: heterotroph richness stimulates methanotrophic activity. ISME J 8:1945–1948. https://doi.org/10.1038/ismej.2014.74
Holmes AJ, Costello A, Lidstrom ME, Murrell JC (1995) Evidence that participate methane monooxygenase and ammonia monooxygenase may be evolutionarily related. FEMS Microbiol Lett 132:203–208. https://doi.org/10.1111/j.1574-6968.1995.tb07834.x
Innes L, Hobbs PJ, Bardgett RD (2004) The impacts of individual plant species on rhizosphere microbial communities in soils of different fertility. Biol Fertil Soils 40:7–13. https://doi.org/10.1007/s00374-004-0748-0
Joabsson A, Christensen TR, Wallén B (1999) Vascular plant controls on methane emissions from northern peatforming wetlands. Trends Ecol Evol 14:385–388. https://doi.org/10.1016/S0169-5347(99)01649-3
Keppler F, Hamilton JTG, Braß M, Röckmann T (2006) Methane emissions from terrestrial plants under aerobic conditions. Nature 439:187–191. https://doi.org/10.1038/nature04420
Kirschke S, Bousquet P, Ciais P et al (2013) Three decades of global methane sources and sinks. Nat Geosci 6:813–823. https://doi.org/10.1038/NGEO1955
Knief C, Kolb S, Bodelier PLE, Lipski A, Dunfield PF (2006) The active methanotrophic community in hydromorphic soils changes in response to changing methane concentration. Environ Microbiol 8:321–333. https://doi.org/10.1111/j.1462-2920.2005.00898.x
Kolari P, Pumpanen J, Kulmala L, Ilvesniemi H, Nikinmaa E, Grönholm T, Hari P (2006) Forest floor vegetation plays an important role in photosynthetic production of boreal forests. For Ecol Manag 221:241–248. https://doi.org/10.1016/j.foreco.2005.10.021
Kolb S (2009) The quest for atmospheric methane oxidizers in forest soils. Environ Microbiol Rep 1:336–346. https://doi.org/10.1111/j.1758-2229.2009.00047.x
Kolb S, Knief C, Dunfield PF, Conrad R (2005) Abundance and activity of uncultured methanotrophic bacteria involved in the consumption of atmospheric methane in two forest soils. Environ Microbiol 7:1150–1161. https://doi.org/10.1111/j.1462-2920.2005.00791.x
Kulmala L, Pumpanen J, Kolari P, Muukkonen P, Hari P, Vesala T (2011) Photosynthetic production of ground vegetation in different-aged Scots pine (Pinus sylvestris) forests. Can J For Res 41:2020–2030. https://doi.org/10.1139/X11-121
Lenhart K, Bunge M, Ratering S, Neu TR, Schüttmann I, Greule M, Kammann C, Schnell S, Müller C, Zorn H, Keppler F (2012) Evidence for methane production by saprotrophic fungi. Nat Commun 3:1046. https://doi.org/10.1038/ncomms2049
Lenhart K, Weber B, Elbert W, Steinkamp J, Clough T, Crutzen P, Pöschl U, Keppler F (2015) Nitrous oxide and methane emissions from cryptogamic covers. Glob Chang Biol 21:3889–3900. https://doi.org/10.1111/gcb.12995
Livingston GP, Hutchinson GL (1995) Enclosure-based measurement of trace gas exchange: applications and sources of error. In: Matson PA, Lawton JH, Harriss RC, Likens GE (eds) Biogenic trace gases: measuring emissions from soil and water. Blackwell Science, Oxford, pp 14–51
Lohila A, Aalto T, Aurela M et al (2016) Large contribution of boreal upland forest soils to a catchment-scale CH4 balance in a wet year. Geophys Res Lett 43:2946–2953. https://doi.org/10.1002/2016GL067718
Macdonald JA, Fowler D, Hargreaves KJ, Skiba U, Leith ID, Murray MB (1998) Methane emission rates from a northern wetland; response to temperature, water table and transport. Atmos Environ 32:3219–3227. https://doi.org/10.1016/S1352-2310(97)00464-0
Machacova K, Bäck J, Vanhatalo A, Halmeenmäki E, Kolari P, Mammarella I, Pumpanen J, Acosta M, Urban O, Pihlatie M (2016) Pinus sylvestris as a missing source of nitrous oxide and methane in boreal forest. Sci Rep 6:23410. https://doi.org/10.1038/srep23410
Maier M, Machacova K, Lang F, Svobodova K, Urban O (2017a) Combining soil and tree-stem flux measurements and soil gas profiles to understand CH4 pathways in Fagus sylvatica forests. J Plant Nutr Soil Sci. https://doi.org/10.1002/jpln.201600405
Maier M, Paulus S, Nicolai C, Stutz KP, Nauer PA (2017b) Drivers of plot-scale variability of CH4 consumption in a well-aerated pine forest soil. Forests 8:1–16. https://doi.org/10.3390/f8060193
Marklund LG (1988) Biomassafunktioner för tall, gran och björk i Sverige. Swedish University of Agricultural Sciences. Umeå, Sweden
Matson A, Pennock D, Bedard-Haughn A (2009) Methane and nitrous oxide emissions from mature forest stands in the boreal forest, Saskatchewan, Canada. For Ecol Manag 258:1073–1083. https://doi.org/10.1016/j.foreco.2009.05.034
Mosier A, Schimel D, Valentine D, Bronson K, Parton W (1991) Methane and nitrous oxide fluxes in native, fertilized and cultivated grasslands. Nature 350:330–332. https://doi.org/10.1038/350330a0
Mukhin VA, Voronin PY (2011) Methane emission from living tree wood. Russ J Plant Physiol 58:344–350. https://doi.org/10.1134/S1021443711020117
Murrell JC, Dalton H (1983) Nitrogen fixation in obligate methanotrophs. J Gen Microbiol 129:3481–3486. https://doi.org/10.1099/00221287-129-11-3481
Olguin-Lora P, Puig-Grajales L, Razo-Flores E (2003) Inhibition of the acetoclastic methanogenic activity by phenol and alkyl phenols. Environ Technol 24:999–1006. https://doi.org/10.1080/09593330309385638
Pangala SR, Moore S, Hornibrook ERC, Gauci V (2013) Trees are major conduits for methane egress from tropical forested wetlands. New Phytol 197:524–531. https://doi.org/10.1111/nph.12031
Pangala SR, Hornibrook ERC, Gowing DJ, Gauci V (2015) The contribution of trees to ecosystem methane emissions in a temperate forested wetland. Glob Chang Biol 21:2642–2654. https://doi.org/10.1111/gcb.12891
Pihlatie MK, Christiansen JR, Aaltonen H et al (2013) Comparison of static chambers to measure CH4 emissions from soils. Agric For Meteorol 171–172:124–136. https://doi.org/10.1016/j.agrformet.2012.11.008
Poirier S, Bize A, Bureau C, Bouchez T, Chapleur O (2016) Community shifts within anaerobic digestion microbiota facing phenol inhibition: towards early warning microbial indicators? Water Res 100:296–305. https://doi.org/10.1016/j.watres.2016.05.041
Praeg N, Wagner AO, Illmer P (2016) Plant species, temperature, and bedrock affect net methane flux out of grassland and forest soils. Plant Soil. https://doi.org/10.1007/s11104-016-2993-z
Pumpanen JS, Heinonsalo J, Rasilo T, Hurme K-R, Ilvesniemi H (2009) Carbon balance and allocation of assimilated CO2 in Scots pine, Norway spruce, and silver birch seedlings determined with gas exchange measurements and 14C pulse labelling. Trees 23:611–621. https://doi.org/10.1007/s00468-008-0306-8
Redding TE, Hannam KD, Quideau SA, Devito KJ (2005) Particle density of aspen, spruce, and pine forest floors in Alberta, Canada. Soil Sci Soc Am J 69:1503–1506. https://doi.org/10.2136/sssaj2005.0018
Repola J, Ojansuu R, Kukkola M (2007) Biomass functions for Scots pine, Norway spruce and birch in Finland. Working Papers of the Finnish Forest Research Institute, Helsinki
Rice AL, Butenhoff CL, Shearer MJ, Teama D, Rosenstiel TN, Khalil MAK (2010) Emissions of anaerobically produced methane by trees. Geophys Res Lett 37:L03807. https://doi.org/10.1029/2009GL041565
Rusch H, Rennenberg H (1998) Black alder (Alnus glutinosa (L.) Gaertn.) trees mediate methane and nitrous oxide emission from the soil to the atmosphere. Plant Soil 201:1–7. https://doi.org/10.1023/A:1004331521059
Shoemaker JK, Keenan TF, Hollinger DY, Richardson AD (2014) Forest ecosystem changes from annual methane source to sink depending on late summer water balance. Geophys Res Lett 41:673–679. https://doi.org/10.1002/2013GL058691
Sjögersten S, Wookey PA (2002) Spatio-temporal variability and environmental controls of methane fluxes at the forest-tundra ecotone in the Fennoscandian mountains. Glob Chang Biol 8:885–894. https://doi.org/10.1046/j.1365-2486.2002.00522.x
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. https://doi.org/10.1016/j.agee.2009.05.018
Smolander A, Kanerva S, Adamczyk B, Kitunen V (2012) Nitrogen transformations in boreal forest soils - does composition of plant secondary compounds give any explanations? Plant Soil 350:1–26. https://doi.org/10.1007/s11104-011-0895-7
Steinberg LM, Regan JM (2008) Phylogenetic comparison of the methanogenic communities from an acidic, oligotrophic fen and an anaerobic digester treating municipal wastewater sludge. Appl Environ Microbiol 74:6663–6671. https://doi.org/10.1128/AEM.00553-08
Steudler PA, Bowden RD, Melillo JM, Aber JD (1989) Influence of nitrogen fertilization on methane uptake in temperate forest soils. Nature 341:314–316. https://doi.org/10.1038/341314a0
Sundqvist E, Crill P, Mlder M, Vestin P, Lindroth A (2012) Atmospheric methane removal by boreal plants. Geophys Res Lett 39:10–15. https://doi.org/10.1029/2012GL053592
Terazawa K, Ishizuka S, Sakata T, Yamada K, Takahashi M (2007) Methane emissions from stems of Fraxinus mandshurica Var. japonica trees in a floodplain forest. Soil Biol Biochem 39:2689–2692. https://doi.org/10.1016/j.soilbio.2007.05.013
Timonen S, Sinkko H, Sun H, Sietiö O-M, Rinta-Kanto JM, Kiheri H, Heinonsalo J (2016) Ericoid roots and mycospheres govern plant-specific bacterial communities in boreal forest humus. Microb Ecol 1–15. https://doi.org/10.1007/s00248-016-0922-6
Topa MA, McLeod KW (1986) Aerenchyma and lenticel formation in pine seedlings: a possible avoidance mechanism to anaerobic growth conditions. Physiol Plant 68:540–550. https://doi.org/10.1111/j.1399-3054.1986.tb03394.x
Vigano I, van Weelden H, Holzinger R, Keppler F, McLeod A, Röckmann T (2008) Effect of UV radiation and temperature on the emission of methane from plant biomass and structural components. Biogeosciences 5:937–947. https://doi.org/10.5194/bg-5-937-2008
von Fischer JC, Hedin LO (2002) Separating methane production and consumption with a field-based isotope pool dilution technique. Global Biogeochem cycles 16:8–1–8–13. doi:https://doi.org/10.1029/2001GB001448
Wang H, Richardson CJ, Ho M (2015) Dual controls on carbon loss during drought in peatlands. Nat Clim Chang 5:584–588. https://doi.org/10.1038/nclimate2643
Whiting GJ, Chanton JP (1992) Plant-dependent CH4 emission in a subarctic Canadian fen. Glob Biogeochem Cycles 6:225–231. https://doi.org/10.1029/92GB00710
Zeikus JG, Ward JC (1974) Methane formation in living trees: a microbial origin. Science 184:1181–1183. https://doi.org/10.1126/science.184.4142.1181
Acknowledgements
This study has been supported by the Emil Aaltonen Foundation, The Academy of Finland Centre of Excellence (project 272041), Academy of Finland Research Fellow projects (292699, 263858, 288494), InGOS, ICOS (271878), ICOS-Finland (281255) and ICOS-ERIC (281250) funded by the Academy of Finland.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Responsible Editor: Paul Bodelier
Electronic supplementary material
ESM 1
(PDF 610 kb)
Rights and permissions
About this article
Cite this article
Halmeenmäki, E., Heinonsalo, J., Putkinen, A. et al. Above- and belowground fluxes of methane from boreal dwarf shrubs and Pinus sylvestris seedlings. Plant Soil 420, 361–373 (2017). https://doi.org/10.1007/s11104-017-3406-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-017-3406-7