Skip to main content
SpringerLink
Log in

Vertical sediment distribution of methanogenic pathways in two shallow Arctic Alaskan lakes

  • Original Paper
  • Published:
Polar Biology Aims and scope Submit manuscript

Abstract

Methanogenesis (MG) occurs in anaerobic lake sediments during the terminal step of organic matter degradation. Methane is typically produced via two primary catabolic pathways (acetoclastic or hydrogenotrophic) in which the primary substrates are acetate or H2/CO2, respectively. The acetoclastic pathway has been shown to dominate in a 2:1 ratio over the hydrogenotrophic pathway in freshwater sediments. Rates of methane production from each pathway are regulated primarily by the quantity and quality of organic matter. As acetate and H2 are produced through decomposition of organic matter, increased terrestrially derived organic matter loading can fuel sediment MG. Increased delivery of terrestrially derived organic matter to arctic lakes is expected under future climate change scenarios. Therefore, we compared unamended rates of MG in anaerobic sediment slurries to those amended with acetate or hydrogen. We also evaluated the vertical sediment distribution of MG pathways in 1-cm increments to a final depth of 5 cm using an inhibitor for the acetoclastic pathway, methyl fluoride. In both lakes, unamended rates of MG decreased with increasing sediment depth. Additions of acetate or hydrogen stimulated rates of MG at all depths in both lakes resulting in rates 1–3 orders of magnitude greater than MG rates in unamended slurries. The ratio of the acetoclastic to the hydrogenotrophic pathway decreased with increasing sediment depth in both lakes. Our findings suggest that increased delivery of terrestrial organic matter to shallow arctic lakes may increase sediment methane production.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Bartlett KB, Crill PM, Sass RL, Harriss RC, Dise NB (1992) Methane emissions from tundra environments in the Yukon-Kuskokwim Delta, Alaska. J Geophys Res 97:16645–16660

    Article  CAS  Google Scholar 

  • Bastviken D, Cole J, Pace M, Tranvik L (2004) Methane emissions from lakes: dependence of lake characteristics, two regional assessments, and a global estimate. Global Biogeochem Cycles. doi:10.1029/2004GB002238

    Google Scholar 

  • Bertilsson S, Tranvik L (2000) Photochemical transformation of dissolved organic matter in lakes. Limnol Oceanogr 45:753–762

    Article  CAS  Google Scholar 

  • Bond DR, Lovley DR (2002) Reduction of Fe(III)oxide by methanogens in the presence and absence of extracelluar quinones. Environ Microbiol 4:115–124

    Article  CAS  PubMed  Google Scholar 

  • Bowden WB, Gooseff MN, Balser A et al (2008) Sediment and nutrient delivery from thermokarst features in the foothills of the North Slope, Alaska: potential impacts on headwater stream systems. J Geophys Res. doi:10.1029/2007JG000470

    Google Scholar 

  • Bretz KA, Whalen SC (2014) Methane cycling dynamics in sediments of Alaskan Arctic Foothill lakes. Inland Waters 4:65–78

    Article  CAS  Google Scholar 

  • Capone DG, Kiene RP (1988) Comparison of microbial dynamics in marine and freshwater sediments: contrasts in anaerobic carbon catabolism. Limnol Oceanogr 33:725–749

    Article  CAS  Google Scholar 

  • Cervantes FJ, van der Velde S, Lettinga G, Field JA (2000) Competition between methanogenesis and quinone respiration for ecological important substrates in aerobic consortia. FEMS Microbiol Ecol 34:161–171

    Article  CAS  PubMed  Google Scholar 

  • Chalfant BA (2004) A landscape level analysis of physical, chemical and biological characteristics of 41 arctic lakes near Toolik Lake, Alaska. Thesis, University of North Carolina at Chapel Hill

  • Chan OC, Claus P, Casper P, Ulrich A, Lueders T, Conrad R (2005) Vertical distribution of structure and function of the methanogenic archaeal community in Lake Dagow sediment. Environ Microbiol 7:1139–1149

    Article  CAS  PubMed  Google Scholar 

  • Clesceri LS (1998) Standard methods for the examination of water and wastewater. American Public Health Association, Washington

    Google Scholar 

  • Conrad R (1999) Contribution of hydrogen to methane production and control of hydrogen concentrations in methanogenic soils and sediments. FEMS Microbiol Ecol 28:193–202

    Article  CAS  Google Scholar 

  • Conrad R (2005) Quantification of methanogenic pathways using stable carbon isotopic signatures: a review and a proposal. Org Geochem 26:739–752

    Article  Google Scholar 

  • Conrad R, Klose M, Claus P, Enrich-Prast A (2010) Methanogenic pathway, 13C isotope fractionation, and archaeal community composition in the sediment of two clear-water lakes of Amazonia. Limnol Oceanogr 55:689–702

    Article  CAS  Google Scholar 

  • Cory RM, McKnight DM, Chin YP, Miller P, Jaros CL (2007) Chemical characteristics of fulvic acids from arctic surface waters: microbial contributions and photochemical transformations. J Geophys Res. doi:10.1029/2006JG000343

    Google Scholar 

  • Cory RM, Miller MP, McKnight DM, Guerard JJ, Miller PL (2010) Effect of instrument-specific response on the analysis of fulvic acid fluorescence spectra. Limnol Oceanogr Methods 8:67–78

    Article  CAS  Google Scholar 

  • Crill PM, Martens CS (1986) Methane production from bicarbonate and acetate in an anoxic marine sediment. Geochim Cosmochim Acta 50:2089–2097

    Article  CAS  Google Scholar 

  • Dan J, Kumai T, Sugimoto A, Murase J (2004) Biotic and abiotic methane releases from Lake Biwa sediment slurry. Limnology 5:149–154

    Article  CAS  Google Scholar 

  • den Heyer C, Kalff J (1998) Organic matter mineralization rates in sediments: a within- and among-lake study. Limnol Oceanogr 43:695–705

  • Deutzmann J, Schink B (2011) Anaerobic oxidation of Lake Constance, and oligotrophic freshwater lake. Appl Environ Microbiol 77:4429–4436

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Dodds WK, Whiles MR (2010) Freshwater ecology: concepts and environmental applications of limnology. Academic Press, San Diego

    Google Scholar 

  • Duc NT, Crill P, Bastviken D (2010) Implications of temperature and sediment characteristics on methane formation and oxidation in lake sediments. Biogeochemistry 100:185–196

    Article  CAS  Google Scholar 

  • Falz KZ, Holliger C, Grosskopf RW et al (1999) Vertical distribution of methanogens in the anoxic sediment of Rotsee (Switzerland). Appl Environ Microbiol 65:2402–2408

    CAS  Google Scholar 

  • Finlay J, Neff JC, Zimov S, Davydova A, Davydova S (2006) Snowmelt dominance of dissolved organic carbon in high-latitude watersheds: implications for characterization and flux of river DOC. Geophys Res Lett. doi:10.1029/2007/GL030689

    Google Scholar 

  • Guo L, Ping CL, Macdonald RW (2007) Mobilization pathways of organic carbon from permafrost to arctic rivers in a changing climate. Geophys Res Lett. doi:10.1029/2007GL0689

    Google Scholar 

  • Hamilton TD (2002) Glacial geology of the Toolik Lake and Upper Kuparuk River region. In: Walker DA (ed) Biological papers of the University of Alaska. University of Alaska Fairbanks, Fairbanks, pp 1–30

    Google Scholar 

  • Hershey AE, Northington RM, Whalen SC (2014) Substrate limitation of sediment methane flux, methane oxidation and use of stable isotopes for assessing methanogenesis pathways in a small arctic lake. Biogeochemistry 117:325–336

    Article  CAS  Google Scholar 

  • Hobbie SE, Miley TA, Weiss MS (2002) Carbon and nitrogen cycling in soils from acidic and nonacidic tundra with different glacial histories in northern Alaska. Ecosystems 5:761–774

    Article  CAS  Google Scholar 

  • Horn MA, Matthies C, Kusel K, Schramm A, Drake HL (2003) Hydrogenotrophic methanogenesis by moderately acid-tolerant methanogenesis of a methane-emitting acidic peat. Appl Environ Microbiol 69:74–83

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Houser JN, Bade DL, Cole JJ, Pace ML (2003) The dual influences of dissolved organic carbon on hypolimnetic metabolism: organic substrate and photosynthetic reduction. Biogeochemistry 64:247–269

    Article  CAS  Google Scholar 

  • Judd KE, Crump BC, Kling GW (2007) Bacterial responses in activity and community composition to photo-oxidation of dissolved organic matter from soil and surface waters. Aquat Sci 69:96–107

    Article  CAS  Google Scholar 

  • Karlsson J, Christensen TR, Crill P, Forster J et al (2010) Quantifying the relative importance of lake emissions in the carbon budget of a subarctic catchment. J Geophys Res. doi:10.1029/2010JG001305

    Google Scholar 

  • Kling GW (1995) Land-water interactions: the influence of terrestrial diversity on aquatic ecosystems. In: Chapin FS, Korner C (eds) Arctic and alpine diversity: patterns, causes, and ecosystem consequences. Springer, Berlin, pp 297–310

    Chapter  Google Scholar 

  • Levine MA, Whalen SC (2001) Nutrient limitation of phytoplankton production in Alaskan Arctic Foothill lakes. Hydrobiologia 455:189–201

    Article  Google Scholar 

  • Lofton DD (2012) Factors regulating methane production and oxidation in two shallow Arctic Alaskan lakes. Dissertation, University of North Carolina at Chapel Hill

  • Lofton DD, Whalen SC, Hershey AE (2014) Effect of temperature on methane dynamics and evaluation of methane oxidation kinetics in shallow Arctic Alaskan lakes. Hydrobiologia 721:209–222

    Article  CAS  Google Scholar 

  • Mazéas O, von Fischer JC, Rhew RC (2009) Impact of terrestrial carbon input on methane emissions from an Alaskan Arctic lake. Geophyl Res Lett. doi:10.1029/2009GL039861

    Google Scholar 

  • McDonald JH (2009) Handbook of Biological Statistics. Sparky House Publishing, Baltimore, Maryland

  • McGuire DA, Anderson LG, Christensen TR et al (2009) Sensitivity of the carbon cycle in the Arctic to climate change. Ecol Monogr 79:523–555

    Article  Google Scholar 

  • McKnight DM, Boyer EW, Westerhoff PK et al (2001) Spectrofluorometric characterization of dissolved organic matter of precursor organic material and aromaticity. Limnol Oceanogr 46:38–48

    Article  CAS  Google Scholar 

  • Michaelson GJ, Ping CL, Kimble JM (1996) Carbon storage and distribution in tundra soils of Arctic Alaska, USA. Arct Alp Res 28:414–424

    Article  Google Scholar 

  • Michaelson GJ, Ping CL, Kling GW, Hobbie JE (1998) The character and bioactivity of dissolved organic matter at thaw and in the spring runoff waters of the arctic tundra north slope, Alaska. J Geophys Res 103:28939–28946

    Article  CAS  Google Scholar 

  • Moran MA, Zepp RG (1997) Role of photoreactions in the formation of biologically labile compounds from dissolved organic matter. Limnol Oceanogr 42:1307–1316

    Article  CAS  Google Scholar 

  • Mueller DR, Van Hove P, Antoniades D et al (2009) High arctic lakes as sentinel ecosystems: cascading regime shifts in climate, ice cover, and mixing. Limnol Oceanogr 54:2371–2385

    Article  Google Scholar 

  • Nozhevnikova AN, Hollinger C, Anmann A, Zehnder AJB (1997) Methanogenesis in sediments from deep lakes at different temperatures (2–70 °C). Water Sci Tech 36:57–64

    Article  CAS  Google Scholar 

  • Nozhevnikova AN, Hollinger C, Anmann A, Zehnder AJB et al (2007) Influence of temperature and high acetate concentrations on methanogenesis in lake sediment slurries. FEMS Microbiol Ecol 62:336–344

    Article  CAS  PubMed  Google Scholar 

  • Nusslein B, Conrad R (2000) Methane production in eutrophic Lake Plubsee: seasonal change, temperature effect and metabolic processes in the profundal sediment. Arch Hydrobiol 149:597–623

    CAS  Google Scholar 

  • Oremland RS (1988) Biogeochemistry of methanogenic bacteria. In: Zehnder AJB (ed) Biology of anaerobic microorganisms, 3rd edn. Wiley, New York, pp 641–705

    Google Scholar 

  • Pastor J, Solin J, Bridgham SD et al (2003) Global warming and the export of dissolved organic carbon from boreal peatlands. Oikos 100:380–386

    Article  Google Scholar 

  • Ping CL, Bockheim JG, Kimble JM et al (1998) Characteristics of cryogenic soils along a latitudinal transect in Arctic Alaska. J Geophys Res 103:28917–28928

    Article  CAS  Google Scholar 

  • Prater JL, Chanton JP, Whiting GJ (2007) Variation in methane production pathways associated with permafrost decomposition in collapse scar bogs of Alberta. Global Biogeochem Cycles, Canada. doi:10.1029/2006GB002866

    Google Scholar 

  • Rautio M, Mariash H, Forsstrom L (2011) Seasonal shifts between autochthonous and allochthonous carbon contributions to zooplankton diets in a subarctic lake. Limnol Oceanogr 56:1513–1524

    Article  CAS  Google Scholar 

  • Roehm CL, Giesler R, Karlsson J (2009) Bioavailability of terrestrial organic carbon to lake bacteria: the case of a degrading subarctic permafrost mire complex. J Geophys Res. doi:10.1029/2008JG000863

    Google Scholar 

  • Rooney-Varga JN, Giewat MW, Duddleston KN et al (2007) Links between archaeal community structure, vegetation type and methanogenic pathway in Alaskan peatlands. FEMS Microbiol Ecol 60:240–251

    Article  CAS  PubMed  Google Scholar 

  • Rothfuss F, Bender M, Conrad R (1997) Survival and activity of bacteria in a deep, aged lake sediment (Lake Constance). Microb Ecol 33:69–77

    Article  PubMed  Google Scholar 

  • Schimel JP, Gulledge J (1998) Microbial community structure and global trace gases. Global Change Biol 4:745–758

    Article  Google Scholar 

  • Schink B (1997) Energetics of syntrophic cooperation in methanogenic degradation. Microbiol Mol Biol Rev 61:262–280

    PubMed Central  CAS  PubMed  Google Scholar 

  • Schulz S, Conrad R (1996) Influence of temperature on pathways to methane production in the permanently cold profundal sediment of Lake Constance. FEMS Microbiol Ecol 20:1–14

    Article  CAS  Google Scholar 

  • Schulz S, Matsuyama H, Conrad R (1997) Temperature dependence of methane production from difference precursors in a profundal sediment (Lake Constance). FEMS Microbiol Ecol 22:207–213

    Article  CAS  Google Scholar 

  • Schwarz JK, Eckert W, Conrad R (2008) Response of the methanogenic community of a profundal lake sediment (Lake Kinneret, Israel) to algal deposition. Limnol Oceanogr 53:113–121

    Article  CAS  Google Scholar 

  • Semiltov IP (1999) Aquatic sources and sinks of CO2 and CH4 in the polar regions. J Atmos Sci 56:286–306

    Article  Google Scholar 

  • Sokal RR, Rohlf FJ (1995) Biometry. WH Freeman and Company, New York

    Google Scholar 

  • Stumm W, Morgan JJ (1996) Aquatic chemistry: chemical equilibria and rates in natural waters. John Wiley, New York

  • Sweerts JP, Rudd JWM, Kelly CA (1986) Metabolic activities in flocculent surface sediments and underlying sandy littoral sediments. Limnol Oceanogr 31:330–338

    Article  CAS  Google Scholar 

  • Tranvik LJ, Downing JA, Cotner JB et al (2009) Lakes and reservoirs as regulators of carbon cycling and climate. Limnol Oceanogr 54:2298–2314

    Article  CAS  Google Scholar 

  • Walter KM, Smith LC, Chapin FS (2007) Methane bubbling from northern lakes: present and future contributions to the global methane budget. Philos Trans R Soc Ser B 365:1657–1676

    Article  CAS  Google Scholar 

  • Watanabe T, Kimura M, Asakawa S (2007) Dynamics of methanogenic archaeal Communities based on rRNA analysis and their relation to methanogenic activity In Japanese paddy field soils. Soil Biol Biochem 39:2877–2887

    Article  CAS  Google Scholar 

  • Weller G, Chapin FS, Everett KR, Hobbie JE et al (1995) The Arctic flux study: a regional view of trace gas release. J Biogeogr 22:365–374

    Article  Google Scholar 

  • Wetzel RG (2001) Limnology: lake and river ecosystems. Academic Press, San Diego

    Google Scholar 

  • Wetzel RG, Likens GE (2000) Limnological Analyses. Springer-Verlag, New York

  • Whalen SC, Cornwell JC (1985) Nitrogen, phosphorus, and organic carbon cycling in arctic lakes. Can J Fish Aquat Sci 42:794–808

    Article  Google Scholar 

  • Whalen SC, Chalfant BA, Fischer EN et al (2006) Comparative influence of resuspended glacial sediment on physicochemical characteristics and primary production in two arctic lakes. Aquat Sci 68:65–77

    Article  CAS  Google Scholar 

  • Whalen SC, Chalfant BA, Fischer EN (2008) Epipelic and pelagic primary production in Alaskan Arctic lakes of varying depth. Hydrobiologia 614:243–257

    Article  CAS  Google Scholar 

  • Whalen SC, Lofton DD, McGowan GE, Strohm A (2013) Microphytobenthos in shallow arctic lakes: fine-scale depth distribution of chlorophyll a, radiocarbon assimilation, irradiance, and dissolved O2. Arct Antarct Alp Res 45:285–295

    Article  Google Scholar 

  • Yamamoto S, Alcauskas JB, Crozier TE (1976) Solubility of methane in distilled water and seawater. J Chem Eng Data 21:78–80

  • Yuan Y, Conrad R, Lu Y (2009) Responses of methanogenic archaeal community to oxygen exposure in rice field soil. Environ Microbiol Reports 1:347–354

    Article  CAS  Google Scholar 

  • Zar JH (1996) Biostatistical analysis. Prentice Hall Inc., Upper Saddle River

    Google Scholar 

  • Zehnder AJB, Stumm W (1988) Geochemistry and biogeochemistry of anaerobic habitats. In: Zehnder AJB (ed) Biology of anaerboic microorganisms. Wiley, New York, pp 1–35

    Google Scholar 

  • Zimov SA, Voropaev YV, Semiltov IP et al (1997) North Siberian lakes: a methane source fueled by Pleistocene carbon. Science 277:800–802

    Article  CAS  Google Scholar 

  • Zinder SH (1993) Physiological ecology of methanogens. In: Ferry JG (ed) Methanogenesis: ecology, physiology, biochemistry and genetics. Chapman and Hall, New York, pp 129–206

    Google Scholar 

Download references

Acknowledgments

We would like to thank Dr. Kenneth Fortino and Dr. Cody R. Johnson, for field and laboratory assistance as well as the Toolik Field Station Staff for logistical support. We would also like to thank Dr. Rose M. Cory for fluorescence index determination and Nick Grewe (LimnoTech) for GIS support. We appreciate the thoughtful insight provided by two anonymous reviewers, which significantly improved this manuscript. This work was funded by NSF Grants 0807094 and 0516043.

Author information

Authors and Affiliations

  1. LimnoTech, 7300 Hudson Blvd., Suite 295, Oakdale, MN, 55128, USA

    Dendy D. Lofton

  2. University of North Carolina – Chapel Hill, 166 Rosenau Hall, 135 Dauer Drive, Campus Box 7431, Chapel Hill, NC, 27599-7431, USA

    Stephen C. Whalen

  3. University of North Carolina – Greensboro, 312 Eberhart Building, 321 McIver Street, Greensboro, NC, 27402-6170, USA

    Anne E. Hershey

Authors
  1. Dendy D. Lofton
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Stephen C. Whalen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Anne E. Hershey
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Dendy D. Lofton.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lofton, D.D., Whalen, S.C. & Hershey, A.E. Vertical sediment distribution of methanogenic pathways in two shallow Arctic Alaskan lakes. Polar Biol 38, 815–827 (2015). https://doi.org/10.1007/s00300-014-1641-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00300-014-1641-4

Keywords

Search

Navigation