Skip to main content
Log in

Estimating changes of isotopic fractionation based on chemical kinetics and microbial dynamics during anaerobic methane oxidation: apparent zero- and first-order kinetics at high and low initial methane concentrations

  • Original Paper
  • Published:
Antonie van Leeuwenhoek Aims and scope Submit manuscript

Abstract

Changes in natural isotopic composition may be used to reveal metabolic pathways of substrate transformation by microbial communities (Vavilin in Ecol Model 240:84–92, 2012b). Anaerobic oxidation of methane (AOM) by sulfate has been described using a mathematical model based on chemical kinetics, microbial dynamics and equations for 13C isotope accumulation in products as well as their redistribution between substrate and products. Experimental data for two batch cultures that originated from microbial mats covering methane seep chimneys in the Black Sea, previously obtained by Seifert et al. (Org Geochem 37:1411–1419, 2006) and Holler et al. (Env Microbiol Reports 1(5):370–376, 2009), were used to model AOM. During long-time incubation, changes of isotope signatures in CH4 showed that in the Seifert et al. batch tests (low methane concentration), in contrast to the Holler et al. batch tests (high methane concentration), methane production occurred along with methane oxidation. In accordance with the model, apparent zero and first-order kinetics of methane oxidation were valid for the Holler et al. and Seifert et al. batch tests, respectively. The observed change of \( \delta {}^{13}{\text{CH}}_{4} \) was explained by microbial kinetics reflecting that the rate is lower for heavy substrate microbial utilization when compared to light substrate microbial utilization. The model showed that small amounts of methanogenesis will change the carbon isotopic composition of methane because biogenic methane has a distinct isotopic composition and due to the large difference between the maximum specific rates of methane oxidation and production. The estimated biomass doubling time of methane-oxidizers for high and low methane concentration was 408/126 days and 4640/1160 days, respectively, depending on the value of the half-saturation constant K S (5 and 20 mM).

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

Access this article

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Alperin MJ, Reeburgh WS (1985) Inhibition experiments on anaerobic methane oxidation. Appl Environ Microbiol 50(4):940–945

    PubMed  CAS  Google Scholar 

  • Batstone DJ, Keller J, Angelidaki I, Kalyuzhnyi SV, Pavlosthatis SG, Rozzi A, Sanders WTM, Siegrist H, Vavilin VA (2002) Anaerobic Digestion Model No.1 (ADM1). Scientific and Technical Report No. 13. IWA Publishing, London, p 77

  • Boetius A, Ravenschlag K, Schubert CJ, Rickert D, Widdel F, Gieseke A, Amann R, Jougensen BB, Witte U, Pfannkuche O (2000) A marine microbial consortium apparently mediating oxidation of methane. Nature 407:623–626

    Article  PubMed  CAS  Google Scholar 

  • Craig H (1957) Isotopic standards for carbon and oxygen and correction factors for mass-spectrometric analysis of carbon dioxide. Geochim Cosmochim Acta 12(1–2):133–149

    Article  CAS  Google Scholar 

  • Elvert M, Hopmans E, Treude T, Boetius A, Suess E (2005) Spatial variations of methanotrophic consorthia at cold marine seeps: implications from a high-resolution molecular and isotopic approach. Geobiology 3:195–209

    Article  CAS  Google Scholar 

  • Girguis PR, Cozen AE, DeLong EF (2005) Growth and population dynamics of anaerobic methane-oxidizing archaea and sulfate-reducing bacteria in a continuous-flow bioreactor. Appl Environ Microb 71:3725–3733

    Article  CAS  Google Scholar 

  • Goevert D, Conrad R (2009) Effect of substrate concentration on carbon isotope fractionation during acetoclastic methanogenesis by Methanosarcina barkeri and M. acetivorance and in rice field soil. Appl Environ Microb 75:2605–2612

    Article  CAS  Google Scholar 

  • Hinrichs KU, Boetius A (2002) The anaerobic oxidation of methane: new insights in microbial ecology and biogeochemistry. In: Ocean Margin Systems. G. Wefer et al. (eds). Springer. Berlin. pp 457–477

  • Hinrichs KU, Hayes JM, Sylva SP, Brewer PG, DeLong EF (1999) Methane-consuming archaebacteria in marine sediments. Nature 398:802–805

    Article  PubMed  CAS  Google Scholar 

  • Hoehler TM, Alperin MJ, Albert DB, Martens CS (1994) Field and laboratory studies of methane oxidation in anoxic marine sediment: Evidence for methanogen-sulfate reducer consortium. Global Boigeochem Cycles 8(4):451–463

    Article  CAS  Google Scholar 

  • Holler T, Wegener G, Knittel K, Boetius A, Brunner B, Kuypers MMM, Widdel F (2009) Substantial δ13CH412 CH4 and D/H fractionation during anaerobic oxidation of methane by marine consortia enriched in vitro. Env Microbiol Reports 1(5):370–376

    Article  CAS  Google Scholar 

  • Holler T, Wegner G, Niemann H, Deusner C, Ferdelman TG, Boetius A, Brunner B, Widdel F (2011) Carbon and sulfur back flux during anaerobic microbial oxidation of methane and coupled sulfate reduction. Proc Nat Acad Sci 108(52):E1484–E1490

    Article  PubMed  CAS  Google Scholar 

  • House CH, Orphan VJ, Turk KA, Thomas B, Pernthaler A, Vrentas JM, Joye SB (2009) Extensive carbon heterogeneity among methane seep microbiota. Environ Microbiol 11:2207–2215

    Article  PubMed  CAS  Google Scholar 

  • Iversen N, Jorgensen BB (1985) Atmospheric methane oxidation rates at the sulfate-methane transition in marine sediments from Kattegat and Skaggerak (Denmark). Limnol Oceanogr 30:944–955

    Article  CAS  Google Scholar 

  • Jorgensen BB, Weber A, Zopfi J (2001) Sulfate reduction and anaerobic oxidation in Black Sea sediments. Deep Sea Res J 48:2097–2120

    Article  Google Scholar 

  • Knittel K, Boetius A (2009) Anaerobic oxidation of methane: progress with an unknown process. Ann Rev Microbiol 63:311–334

    Article  CAS  Google Scholar 

  • Mariotti A, Germon JC, Hubert P, Kaiser P, Letolle R, Tardieux A, Tardieux P (1981) Experimental determination of nitrogen kinetic isotope fractionation: some principles; illustration for the denitrification and nitrification processes. Plant Soil 62(3):413–430

    Article  CAS  Google Scholar 

  • Meulepas RJ, Jagersma CG, Khadem AF, Stams AJ, Lens PN (2010) Effect of methanogenic substrates on anaerobic oxidation of methane and sulfate reduction by an anaerobic methanotrophic enrichment. Appl Microbiol Biotechnol 87:1499–1506

    Article  PubMed  CAS  Google Scholar 

  • Michaelis W, Seifert R, Nauhaus K, Treude T, Thiel V, Blumenberg M, Knittel K, Gieseke A, Peterknecht K, Pape T, Boetius A, Amann R, Jørgensen BB, Widdel F, Peckmann J, Pimenov NV, Gulin MB (2002) Microbial reefs in the Black Sea fueled by anaerobic oxidation of methane. Science 297:1013–1015

    Article  PubMed  CAS  Google Scholar 

  • Nauhaus K, Boetius A, Kruger M, Widdel F (2002) In vitro demonstration of anaerobic oxidation of methane coupled to sulfate reduction in sediments from a marine gas hydrate area. Environ Microbiol 4:296–305

    Article  PubMed  CAS  Google Scholar 

  • Nauhaus K, Treude T, Boetius A, Kruger M (2005) Environmental regulation of the anaerobic oxidation of methane: a comparison of ANME-I and ANME-II communities. Environ Microbiol 7:98–106

    Article  PubMed  CAS  Google Scholar 

  • Nauhaus K, Albrecht M, Elvert M, Boetius A, Widdel F (2007) In vitro cell growth of marine archaeal-bacterial consortia during anaerobic oxidation of methane with sulfate. Environ Microbiol 9:187–196

    Article  PubMed  CAS  Google Scholar 

  • Niemann H, Losekann T, de Beer D, Elvert M, Nadalig T, Knitte K, Amann R, Sauter E, Schluter M, Klages M, Foucher J, Boetius A (2006) Novel microbial communities of the Haakon Mosby mud volcano and their role as a methane sink. Nature 443:854–858

    Article  PubMed  CAS  Google Scholar 

  • Orcutt B, Samarkin V, Boetius A, Joye S (2008) On the relationship between methane production and oxidation by anaerobic methanotrophic communities from cold seeps of the Gulf of Mexico. Environ Microbiol 10:1108–1117

    Article  PubMed  CAS  Google Scholar 

  • Orphan VJ, House CH, Hinrichs KU, McKeegan KD, DeLong EF (2001) Methane-consuming archaea revealed by directly coupled isotopic and phylogenetic analysis. Science 293:484–487

    Article  PubMed  CAS  Google Scholar 

  • Orphan VJ, Turk KA, Green AM, House CH (2009) Patterns of 15N assimilation and growth of methanotrophic ANME-2 archaea and sulfate-reducing bacteria within structured syntrophic consortia revealed by FISH-SIMS. Environ Microbiol 11:1777–1791

    Article  PubMed  CAS  Google Scholar 

  • Rayleigh JWC (1896) Theoretical consideration respecting the separation of gases by diffusion and similar processes. Philos Mag 42:493–498

    Article  Google Scholar 

  • Reeburgh WC (2007) Oceanic methane biogeochemistry. Chem Rev 107:486–513

    Article  PubMed  CAS  Google Scholar 

  • Seifert R, Nauhaus K, Blumenberg M, Kruger M, Michaelis W (2006) Org Geochem 37:1411–1419

    Article  CAS  Google Scholar 

  • Thauer RK (2011) Anaerobic oxidation of methane with sulfate: on the reversibility of the reactions that are catalyzed by enzymes also involved in methanogenesis from CO2. Curr Opin Microbiol 14:292–299

    Article  PubMed  CAS  Google Scholar 

  • Tong JY, Yankwich PE (1957) Calculation of experimental isotope effects for pseudo first-order irreversible reactions. J Phys Chem 61:540–543

    Article  CAS  Google Scholar 

  • Valentine DL, Chidthaisong A, Rice A, Reeburgh WS, Tyler SC (2004) Carbon and hydrogen isotope fractionation by moderately thermophilic methanogens. Geochim Cosmochim Acta 68(7):1571–1590

    Article  CAS  Google Scholar 

  • van Breukelen BM (2007) Extending the Rayleigh equation to allow competing isotope fractionating pathways to improve quantification of biodegradation. Environ Sci Technol 41:4004–4010

    Article  PubMed  Google Scholar 

  • Vavilin VA (2010) Equation for isotope accumulation in products and biomass as a way to reveal the pathways in mesophilic methanol methanization by microbial community. Ecol Model 221:2881–2886

    Article  CAS  Google Scholar 

  • Vavilin VA (2012a) Estimating evolution of δ13CH4 during methanization of cellulosic waste based on stoichiometric chemical reactions, microbial dynamics and stable carbon isotope fractionation. Biores Technol 110:706–710

    Article  CAS  Google Scholar 

  • Vavilin VA (2012b) Estimating evolution of δ13CH4 during methanogenesis in the boreal peatland ecosystems based on stoichiometric chemical reactions, microbial dynamics and stable carbon isotope fractionation. Ecol Model 240:84–92

    Article  CAS  Google Scholar 

  • Vavilin VA, Li T, Chapleur O, Mazeas L, Bouchez T (2010) Modelling thermophilic methanol and cellulose methanization based on chemical reactions and isotope accumulation in products. In: Proc. World Congress on Anaerobic Digestion AD12. Guadalajara. 31 October–4 November 2010. Oral Presentation. CD

  • Wegener G (2008) Methane oxidation and carbon assimilation in marine sediments. Dissertation. Bremen University, p 153

  • Wegener G, Boetius A (2009) An experimental study on short-term changes in the anaerobic oxidation of methane in response to varying methane and sulfate fluxes. Biogeosciences 6:867–876

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to V. A. Vavilin.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Vavilin, V.A. Estimating changes of isotopic fractionation based on chemical kinetics and microbial dynamics during anaerobic methane oxidation: apparent zero- and first-order kinetics at high and low initial methane concentrations. Antonie van Leeuwenhoek 103, 375–383 (2013). https://doi.org/10.1007/s10482-012-9818-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10482-012-9818-8

Keywords

Navigation