568
Views
14
CrossRef citations to date
0
Altmetric
Articles

Geochemical and Microbiological Studies of Nitrous Oxide Variations within the New NEEM Greenland Ice Core during the Last Glacial Period

, , , &
Pages 647-660 | Received 18 Apr 2015, Accepted 10 Jul 2015, Published online: 26 Feb 2016

References

  • Abyzov SS, Barkov NI, Bobin NE, Koudryashov BB, Lipenkov VY, Mitskevich IN, Pashkevich VM, Poglazova MN. 1998. The ice sheet of central Antarctica as an object of study of past ecological events on the earth Izv Akad Nauk USSR Ser Biol 5:610–616.
  • Adav SS, Lee D-J, Lai JY. 2010. Microbial community of acetate utilizing denitrifiers in aerobic granules. Appl Microbiol Biotechnol 85:753–762.
  • Amoroso A, Domine F, Esposito G, Morin S, Savarino J, Nardino M, Montagnoli M, Bonneville JM, Clement JC, Ianniello A, Biene HJ 2010. Microorganisms in dry polar snow are involved in the exchanges of reactive nitrogen species with the atmosphere. Environ Sci Technol 44:714–719. doi: 10.1021/es9027309
  • Anklin M, Schwander J, Stauer B, Tschumi J, Fuchs A, Barnola J-M, Raynaud D. 1997. CO2 record between 40 and 8 Kyr. B.P. J Geochem Res 102(C12):26539–26545.
  • Ashelford KE, Chuzhanova NA, Fry JC, Jones AJ, Weightman AJ. 2006. New screening software shows that most recent large 16S rRNA gene clone libraries contain chimeras. Appl Environ Microbiol 72:5734–5741.
  • Baker GC, Smith JJ, Cowan DA. 2003. Review and re-analysis of domain-specific 16S primers. J Microbiol Meth 55:541–555.
  • Bigler M, for the NEEM Aerosol consortium. 2012. New aerosol measurements from the Greenland NEEM ice core. Geophysical Research Abstracts Vol. 14, EGU2012-5780.
  • Braker G, Dörsch P, Bakken LR. 2012. Genetic characterization of denitrifier communities with contrasting intrinsic functional traits. FEMS Microbiol Ecol 79:542–554.
  • Brook EJ, Harder S, Severinghaus J, Steig EJ, Sucher CM. 2000. On the origin and timing of rapid changes in atmospheric methane during the Last Glacial Period. Global Biogeochem Cycles 14:559–572.
  • Butler JH, Elkins JW, Thompson TM, Egan DB. 1989. Tropospheric and dissolved N2O of the West Pacific and East Indian Oceans during the El Nino southern oscillation event of 1987. J Geophys Res 94:14865–14877.
  • Cameron K, Hodson AJ, Osborn AM. 2012. Carbon and nitrogen biogeochemical cycling potentials of supraglacial cryoconite communities. Polar Biol 35:1375–1393.
  • Campen KR, Sowers T, Alley R. 2003. Evidence for microbial consortia metabolizing within a low latitude mountain glacier. Geology 31:231–234.
  • Chappellaz J, Blunier T, Kints S, Dällenbach A, Barnola J-M, Schwander J, Raynaud D, Stauffer B. 1997. Changes in the atmospheric CH4 gradient between Greenland and Antarctica during the Holocene. J Geophys Res 102(D13):15987–15997.
  • Cua LS, Stein LY. 2014. Characterization of denitrifying activity by the alphaproteobacterium, Sphingomonas wittichii RW1. Front Microbiol 5:404. doi:10.3389/fmicb.2014.00404
  • de Sousa T, Bhosle S. 2012. Microbial denitrification and its ecological implications in the marine system. In: T. Satyanarayana, B. N. Johri and A. Prakash, editors. Microorganisms in Environmental Management. Berlin: Springer, p683–700. DOI 10.1007/978-94-007-2229-3_30
  • Edgar RC, Haas J, Clemente JC, Quince C, Knight R. 2011. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200.
  • Edwards A, Mur LAJ, Girdwood SE, Anesio AM, Stibal M, Rassner SME, Hell K, Pachebat JA, Post B, Bussell JS, Cameron SJS, Griffith GW, Hodson AJ, Sattler B. 2014. Coupled cryoconite ecosystem structure–function relationships are revealed by comparing bacterial communities in alpine and Arctic glaciers. FEMS Microbiol Ecol 89:222–237.
  • Fischer H, Wagenbach D, Kipfstuhl J. 1998. Sulfate and nitrate firn concentrations on the Greenland ice sheet: 1. Largescale geographical deposition changes, J Geophys Res 103:21927–21934.
  • Fischer HS, Schüpbach S, Gfeller G, Bigler M, Röthlisberger R, Erhardt T. Stocker TF, Mulvaney R, Wolff E. 2015. Millennial changes in North American wildfire and soil activity over the last glacial cycle. Nature Geosci 8:723–727 doi:10.1038/ngeo2495.
  • Fluckiger J, Blunier T, Stauffer B, Chappellaz J, Spahni R, Kawamura K, Schwander J, Stocker T, Dahl-Jensen D. 2004. N2O and CH4 variations during the last glacial epoch: Insight into global processes. Global Biogeochem Cycles 18:(1)1–14. doi:10.1029/2003GB002122
  • Fluckiger J, Dallenbach A, Blunier T, Stauffer B, Stocker T, Raynaud D, Barnola J-M. 1999. Variations in atmospheric N2O concentration during abrupt climate changes. Nature 285:227–230.
  • Fluckiger J, Monnin E, Stauffer B, Schwander J, Stocker T, Chappellaz J, Raynaud D, Barnola J-M. 2002. High-resolution Holocene N2O ice core record and its relationship with CH4 and CO2. Global Biogeochem Cycles 16:10–29.
  • Good IJ.1953. The population frequencies of species and the estimation of population parameters. Biometrika 40:237–264.
  • Green SJ, Prakash O, Gihring TM, Akob DM, Jasrotia P, Jardine PM, Watson DB, Brown SD, Palumbo AV, Kostka JE 2010. Denitrifying bacteria isolated from terrestrial subsurface sediments exposed to mixed-waste contamination. Appl Environ Microbiol 76(10): 3244–3254.
  • Guillevic M, Bazin L, Landais A, Kindler P, Orsi A, Masson-Delmotte V, Blunier T, Buchardt SL, Capron E, Leuenberger M, Martinerie P, Prie F, Vinther BM. 2012. Spatial gradient of temperature, accumulation and d18O-ice in Greenland over a series of Dansgaard-Oeschger events. Climate Past 8:5209–5261.
  • Hell K, Edwards A, Zarsky J, Podmirseg SM, Girdwood S, Pachebat JA, Insam H, Sattler B. 2013. The dynamic bacterial communities of a melting High Arctic glacier snowpack. ISME J 7:1814–1826.
  • Heylen K, Vanparys B, Wittebolle L, Verstraete W, Boon N, De Vos P 2006. Cultivation of denitrifying bacteria: Optimization of isolation conditions and diversity study. Appl Environ Microbiol 72(4):2637–2643.
  • Hodson A, Anesio AM, Tranter M, Fountain A, Osborn M, Priscu J, Laybourn-Parry J, Sattler B. 2008. Glacial ecosystems. Ecol Mono 78(1):41–67.
  • Jones CM, Stres B, Rosenquist M, Hallin S. 2008. Phylogenetic analysis of nitrite, nitric oxide, and nitrous oxide respiratory enzymes reveal a complex evolutionary history for denitrification. Mol Biol Evol 25:1955–1966.
  • Jones CM, Welsh A, Throback IN, Dorsch P, Bakken LR, Hallin S. 2011. Phenotypic and genotypic heterogeneity among closely related soil-borne N2—and N2O-producing Bacillus isolates harboring the nosZ gene. FEMS Microbiol Ecol 76:541–552.
  • Junge K, Christner B, Staley J. 2011. Diversity of psychrophilic bacteria from sea ice - and glacial ice communities. In: Horikoshi K, editor. Extremophiles Handbook, Berlin: Springer, p794–815.
  • Kaufmann P, Federer U, Hutterli MA, Bigler M, Schüpbach S, Ruth U, Schmitt J, Stocker TF. 2008. An improved Continuous Flow Analysis (CFA) system for high-resolution field measurements on ice cores, Environ Sci Technol 42:8044–8050. doi:10.1021/es8007722.
  • Kemp PF, Aller JY. 2004. Estimating prokaryotic diversity: When are 16S rRNA libraries large enough? Limnol Oceanogr Meth 2:114–125.
  • Kindler P, Guillevic M, Baumgartner M, Schwander J, Landais A, Leuenberger M. 2014. Temperature reconstruction from 10 to 120 kyr b2k from the NGRIP ice core. Climate Past 10:887–902. doi:10.5194/cp-10-887-2014.
  • Larkin MA, Blackshields NP, Brown RC, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez AR, Thompson JD, Gibson TJ, Higgins DG 2007. Clustal W and Clustal X version 2.0. Bioinformatics 2321:2947–2948.
  • Larose C, Dommergue A, Vogel TM. 2013. Microbial nitrogen cycling in Arctic snowpacks. Environ Res Lett 8:035004.
  • Liu B, Morkved PT, Frostegard A, Bakken LR (2010) Denitrification gene pools, transcription and kinetics of NO, N2O and N2 production as affected by soil pH. FEMS Microbiol Ecol 72:407–417.
  • Mackelprang R, Waldrop MP, DeAngelis KM, David MM, Chavarria KL, Blazewicz SJ, Rubin EM, Jansson JK. 2011. Metagenomic analysis of a permafrost microbial community reveals a rapid response to thaw. Nature 480:368–371.
  • Mader HM, Pettitt ME, Wadham JL, Wolff EW, Parkes RJ. 2006. Subsurface ice as a microbial habitat. Geology 34:169–172.
  • Mao Y, Yannarell AC, Mackie RI. 2011. Changes in N-transforming Archaea and Bacteria in soil during the establishment of bioenergy crops. PLoS ONE 6(9):e24750. doi:10.1371/journal.pone.0024750
  • Margesin R, Miteva V. 2011. Diversity and ecology of psychrophilic microorganisms. Res Microbiol 162:346–361.
  • Miteva V. 2008. Bacteria in snow and glacier ice. In: Margesin R, Schinner F, Marx J-C, Gerday C, editors. Psychrophiles: From Biodiversity to Biotechnology. Berlin: Springer, p31–50.
  • Miteva V, Rinehold K, Sowers T, Sebastian A, Brenchley J. 2015. Abundance, viability and diversity of the indigenous microbial populations at different depths of the NEEM Greenland ice core. Polar Res 34:25057. doi.:10.3402/polar.v34.25057.
  • Miteva VI, Sheridan PP, Brenchley JB. 2004. Phylogenetic and physiological diversity of microorganisms isolated from a deep Greenland ice core. Appl Environ Microbiol 70:202–213.
  • Miteva, V, Sowers T, Brenchley J. 2007. Production of N2O by ammonia oxidizing bacteria at subfreezing temperatures as a model for assessing the N2O anomalies in the Vostok ice core. Geomicrobiol J 24:451–459.
  • Miteva V, Teacher C, Sowers T, Brenchley J. 2009. Comparison of microbial diversity at different depths of the GISP2 Greenland ice core in relation to deposition climate. Environ Microbiol 11:640–656.
  • NEEM (North Greenland Eemian Ice Drilling) Community Members. 2013. Eemian interglacial reconstructed from a Greenland folded ice core. Nature 493 (7433):489–494.
  • Orellana LH, Rodriguez-R LM, Higgins S, Chee-Sanford JC, Sanford R, Ritalahti K, Löffler FE, Konstantinidis KT. 2014. Detecting nitrous oxide reductase (nosZ) genes in soil metagenomes: Method development and implications for the nitrogen cycle. mBio 5(3):e01193–14. doi:10.1128/mBio.01193-14.
  • Palmer K, Biasi C, Horn MA. 2012. Contrasting denitrifier communities relate to contrasting N2O emission patterns from acidic peat soils in arctic tundra. ISME J 6:1058–1077.
  • Pearce DA, Newsham KK, Thorne MAS, Calvo-Bado L, Krsek M, Laskaris P, Hodson A, Wellington EM. 2012. Metagenomic analysis of a southern maritime Antarctic soil. Front Microbiol 3:403, 1–13, doi:10.3389/fmicb.2012.00403
  • Philippot L, Andert J, Jones CM, Bru D, Hallin S. 2011. Importance of denitrifiers lacking the genes encoding the nitrous oxide reductase for N2O emissions from soil. Global Change Biol 17:1497–1504. doi: 10.1111/j.1365-2486.2010.02334.x
  • Philippot L, Hallin S, Schloter M. 2007. Ecology of denitrifying prokaryotes in agricultural soil. Adv Agron 96:259–305.
  • Price PB. 2000. A habitat for psychrophiles in deep Antarctic ice. Proc Natl Acad Sci USA 97:1247–1251.
  • Price PB. 2007. Microbial life in glacier ice and implications for a cold origin of life. FEMS Microbiol Ecol 59:217–231.
  • Price PB, Sowers T. 2004. Temperature dependence of metabolic rates for microbial growth, maintenance, and survival. Proc Natl Acad Sci USA 101:4631–4636.
  • Priscu JC, Christner BC. 2004. Earth's icy biosphere In: Bull AT editor. Microbial Diversity and Bioprospecting. Washington, DC: ASM Press, p130–145.
  • Pruesse E, Quast C, Knittel K, Fuchs BM, Ludwig W, Peplies J, Glöckner FO 2007. SILVA, a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucl Acids Res 35:7188–7196.
  • Qiagen 2012. Qiagen Supplementary Protocol. Purification of DNA Amplified with REPLI-g kits (RG21 Nov-12). Hilden, Germany: Qiagen.
  • Rasmussen SO, Abbott PM, Blunier T, Bourne AJ, Brook E, Buchardt SL, Buizert C, Chappellaz J, Clausen HB, Cook E, Dahl-Jensen D, Davies SM, Guillevic M, Kipfstuhl S, Laepple T, Seierstad IK, Severinghaus JP, Steffensen JP, Stowasser C, Svensson A, Vallelonga P, Vinther BM, Wilhelms F, Winstrup M. 2013. A first chronology for the North Greenland Eemian Ice Drilling (NEEM) ice core. Climate Past 9:2713–2730.
  • Rhodes RH, Fain X, Stowasser C, Blunier T, Chappellaz J, McConnell JR, Romanini D, Mitchell LE, Brook EJ. 2013. Continuous methane measurements from a late Holocene Greenland ice core: Atmospheric and in-situ signals. Earth Planet Sci Lett 368:9–19.
  • Ritalahti K, Hatt JK, Lugmayr V, Henn K, Petrovskis E, Ogles D, Davis G, Yeager C, Lebron C, Loffler F. 2010. Comparing on-site to off-site biomass collection for Dehalococcoides biomarker gene quantification to predict in situ chlorinated ethene detoxification potential. Environ Sci Technol 44:5127–5133.
  • Rogers SO, Theraisnathan V, Ma LJ, Zhao Y, Zhang G, Shin SG, Castelo JD, Starmer WT. 2004. Comparisons of protocols for decontamination of environmental ice samples for biological and molecular examinations. Appl Environ Microbiol 70:2540–2544.
  • Rohde RA, Price PB. 2007. Diffusion-controlled metabolism for long-term survival of single isolated microorganisms trapped within ice crystals. Proc Natl Acad Sci USA 104:16592–16597.
  • Rohde RA, Price PB, Bay RC, Bramall NE. 2008. In-situ microbial metabolism as a cause of gas anomalies in ice. Proc Natl Acad Sci USA 105:8687–8672.
  • Schilt A, Baumgartner M, Blunier T, Schwander J, Spahni R, Fischer H, Stocker TF. 2010a. Glacial–interglacial and millennial scale variations in the atmospheric nitrous oxide concentration during the last 800,000 years. Quat Sci Rev 29:182–192.
  • Schilt A, Baumgartner M, Eicher O, Chapellaz J, Schwander J, Fischer H, Stocker TF. 2013. The response of atmospheric nitrous oxide to climate variations during the last glacial period. Geophys Res Lett 40:1888–1893.
  • Schilt A, Baumgartner M, Schwander J, Buiron D, Capron E, Chappellaz J, Loulergue L, Schüpbach S, Spahni R, Fischer H, Stocker TF. 2010b. Atmospheric nitrous oxide during the last 140,000 years. Earth Planet Sci Lett 300:33–43.
  • Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF. 2009. Introducing mothur, open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541.
  • Shapleigh JP. 2013. Denitrifying prokaryotes. In: Rosenberg E, DeLong EF, Stackebrandt E, Lory S, Thompson F, editors. The Prokaryotes – Prokaryotic Physiology and Biochemistry. Berlin: Springer p405–425. DOI 10.1007/978-3-642-30141-4_71,
  • Simek M, Cooper JE. 2002. The influence of soil pH on denitrification: progress towards the understanding of this interaction over the last 50 years. Eur J Soil Sci 53:345–354.
  • Sowers T. 2001. The N2O record spanning the penultimate deglaciation from the Vostok ice core. J Geophys Res 106(31):903–931.
  • Sowers T, Alley RB, Jubenville J. 2003. Elemental and isotopic records of atmospheric nitrous oxide covering the last 106,000 years from the GISP II and Taylor Dome ice cores. Science 301:945–948.
  • Sowers T, Jubenville J. 2000. A modified extraction technique for liberating occluded gases from ice cores. J Geophys Res 105:29155–29164.
  • Stauffer B, Tschumi J. 2000. Reconstruction of past atmospheric CO2 concentrations by ice core analyses. In: Hondoh T, editor. Physics of Ice Core Records. Sapporo, Japan: Hokkaido University Press, p217–241.
  • Stein LY. 2011. Surveying N2O-producing pathways in bacteria. Meth Microbiol 486:131–152.
  • Stibal M, Hasan F, Wadham JL, Sharp MJ, Anesio AM. 2012. Prokaryotic diversity in sediments beneath two polar glaciers with contrasting organic carbon substrates. Extremophiles 16:255–265.
  • Telling J, Stibal M, Anesio AM, Tranter M, Nias I, Cook J, Bellas C, Lis G, Wadham JL, Sole A, Nienow P, Hodson A. 2012. Microbial nitrogen cycling on the Greenland ice sheet. Biogeosc 9:2431–2442.
  • Ussiri D, Lal R. 2013. The role of nitrous oxide on climate change. In: Soil Emission of Nitrous Oxide and its Mitigation. Dordrecht: Springer, p1–28. DOI 10.1007/978-94-007-5364-8_1
  • Verbaendert I, De Vos P, Boon N, Heylen K. 2011. Denitrification in Gram-positive bacteria: an underexplored trait. Biochem Soc Trans 39(1):254–258.
  • Wakelin SA, Nelson PN, Armour JD, Rasiah V, Colloff MJ. 2011. Bacterial community structure and denitrifier (nir-gene) abundance in soil water and groundwater beneath agricultural land in tropical North Queensland, Australia. Soil Res 49:65–76.
  • Wang Y, Qianh PY. 2009. Conservative fragments in bacterial 16S rRNA genes and primer design for 16S ribosomal DNA amplicons in metagenomic studies. PloS ONE 4(10):e7401.
  • Wolff EW. 2013. Ice sheets and nitrogen. Phil Trans Roy Soc B 368:20130127.
  • Wright ES, Yilmaz LS, Noguera DR. 2012. DECIPHER, A Search-Based approach to chimera identification for 16S rRNA Sequences. Appl Environ Microbiol 78(3):717–725.
  • Xiang SR, Shang TC, Chen Y, Yao TD. 2009. Deposition and post-deposition mechanisms as possible drivers of microbial population variability in glacier ice. FEMS Microbiol Ecol 70:165–176.
  • Yu L, Liu Y, Wang. G. 2009. Identification of novel denitrifying bacteria Stenotrophomonas sp. ZZ15 and Oceanimonas sp. YC13 and application for removal of nitrate from industrial wastewater. Biodegradation 20:391–400.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.