Skip to main content
SpringerLink
Log in

Archaeal Community Structure and Pathway of Methane Formation on Rice Roots

  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

The community structure of methanogenic Archaea on anoxically incubated rice roots was investigated by amplification, sequencing, and phylogenetic analysis of 16S rRNA and methyl-coenzyme M reductase (mcrA) genes. Both genes demonstrated the presence of Methanomicrobiaceae, Methanobacteriaceae, Methanosarcinaceae, Methanosaetaceae, and Rice cluster I, an uncultured methanogenic lineage. The pathway of CH4 formation was determined from the 13C-isotopic signatures of the produced CH4, CO2 and acetate. Conditions and duration of incubation clearly affected the methanogenic community structure and the pathway of CH4 formation. Methane was initially produced from reduction of CO2 exclusively, resulting in accumulation of millimolar concentrations of acetate. Simultaneously, the relative abundance of the acetoclastic methanogens (Methanosarcinaceae, Methanosaetaceae), as determined by T-RFLP analysis of 16S rRNA genes, was low during the initial phase of CH4 production. Later on, however, acetate was converted to CH4 so that about 40% of the produced CH4 originated from acetate. Most striking was the observed relative increase of a population of Methanosarcina spp. (but not of Methanosaeta spp.) briefly before acetate concentrations started to decrease. Both acetoclastic methanogenesis and Methanosarcina populations were suppressed by high phosphate concentrations, as observed under application of different buffer systems. Our results demonstrate the parallel change of microbial community structure and function in a complex environment, i.e., the increase of acetoclastic Methanosarcina spp. when high acetate concentrations become available.

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

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5

Similar content being viewed by others

References

  1. GB Avery RD Shannon JR White CS Martens MJ Alperin (1999) ArticleTitleEffect of seasonal changes in the pathways of methanogenesis on the δ13C values of pore water methane in a Michigan peatland. Global Biogeochem Cycles 13 475–484 Occurrence Handle1:CAS:528:DyaK1MXkslOrurs%3D

    CAS  Google Scholar 

  2. KA Bidle M Kastner DH Bartlett (1999) ArticleTitleA phylogenetic analysis of microbial communities associated with methane hydrate containing marine fluids and sediments in the Cascadia Margin (ODP site 892b). FEMS Microbiol Lett 177 101–108 Occurrence Handle1:CAS:528:DyaK1MXls1SmsbY%3D Occurrence Handle10436927

    CAS  PubMed  Google Scholar 

  3. KJ Chin T Lukow R Conrad (1999) ArticleTitleEffect of temperature on structure and function of the methanogenic archaeal community in an anoxic rice field soil. Appl Environ Microbiol 65 2341–2349

    Google Scholar 

  4. R Conrad P Frenzel (2002) Flooded soils. G Bitton (Eds) Encyclopedia of Environmental Microbiology. John Wiley & Sons New York 1316–1333

    Google Scholar 

  5. R Conrad M Klose (1999) ArticleTitleAnaerobic conversion of carbon dioxide to methane, acetate and propionate on washed rice roots. FEMS Microbiol Ecol 30 147–155 Occurrence Handle10.1016/S0168-6496(99)00048-3 Occurrence Handle1:CAS:528:DyaK1MXmt1emurs%3D Occurrence Handle10508939

    Article  CAS  PubMed  Google Scholar 

  6. R Conrad M Klose (2000) ArticleTitleSelective inhibition of reactions involved in methanogenesis and fatty acid production on rice roots. FEMS Microbiol Ecol 34 27–34 Occurrence Handle10.1016/S0168-6496(00)00071-4 Occurrence Handle1:CAS:528:DC%2BD3cXosVyrt7c%3D Occurrence Handle11053733

    Article  CAS  PubMed  Google Scholar 

  7. R Conrad M Klose P Claus (2000) ArticleTitlePhosphate inhibits acetotrophic methanogenesis on rice roots. Appl Environ Microbiol 66 828–831

    Google Scholar 

  8. R Conrad M Klose P Claus (2002) ArticleTitlePathway of CH4 formation in anoxic rice field soil and rice roots determined by 13C-stable isotope fractionation. Chemosphere 47 797–806 Occurrence Handle10.1016/S0045-6535(02)00120-0 Occurrence Handle1:CAS:528:DC%2BD38XjsVSqsrg%3D Occurrence Handle12079075

    Article  CAS  PubMed  Google Scholar 

  9. S Dannenberg R Conrad (1999) ArticleTitleEffect of rice plants on methane production and rhizospheric metabolism in paddy soil. Biogeochemistry 45 53–71 Occurrence Handle10.1023/A:1006085605184

    Article  Google Scholar 

  10. EF DeLong NR Pace (2001) ArticleTitleEnvironmental diversity of Bacteria and Archaea. Syst Biol 50 470–478 Occurrence Handle10.1080/106351501750435040 Occurrence Handle1:STN:280:DC%2BD38zntVOmsw%3D%3D Occurrence Handle12116647

    Article  CAS  PubMed  Google Scholar 

  11. C Edwards et al. (1998) ArticleTitleMicrobiological processes in the terrestrial carbon cycle—methane cycling in peat. Atmos Environ 32 3247–3255 Occurrence Handle10.1016/S1352-2310(98)00107-1 Occurrence Handle1:CAS:528:DyaK1cXltFOhtbo%3D

    Article  CAS  Google Scholar 

  12. U Ermler W Grabarse S Shima M Goubeaud RK Thauer (1997) ArticleTitleCrystal structure of methyl coenzyme M reductase—the key enzyme of biological methane formation. Science 278 1457–1462 Occurrence Handle9367957

    PubMed  Google Scholar 

  13. A Fey KJ Chin R Conrad (2001) ArticleTitleThermophilic methanogens in rice field soil. Environ Microbiol 3 295–303 Occurrence Handle10.1046/j.1462-2920.2001.00195.x Occurrence Handle1:CAS:528:DC%2BD3MXlt1eht70%3D Occurrence Handle11422316

    Article  CAS  PubMed  Google Scholar 

  14. A Fey R Conrad (2000) ArticleTitleEffect of temperature on carbon and electron flow and on the archaeal community in methanogenic rice field soil. Appl Environ Microbiol 66 4790–4797 Occurrence Handle11055925

    PubMed  Google Scholar 

  15. MW Friedrich (2002) ArticleTitlePhylogenetic analysis reveals multiple lateral transfers of adenosine-5′-phosphosulfate reductase genes among sulfate-reducing microorganisms. J Bacteriol 184 278–289 Occurrence Handle1:CAS:528:DC%2BD3MXpt1Cmtbk%3D Occurrence Handle11741869

    CAS  PubMed  Google Scholar 

  16. PE Galand S Saarnio H Fritze K Yrjälä (2002) ArticleTitleDepth related diversity of methanogen Archaea in Finnish oligotrophic fen. FEMS Microbiol Ecol 42 441–449 Occurrence Handle10.1016/S0168-6496(02)00381-1 Occurrence Handle1:CAS:528:DC%2BD38XoslGiur0%3D

    Article  CAS  Google Scholar 

  17. R Grosskopf PH Janssen W Liesack (1998) ArticleTitleDiversity and structure of the methanogenic community in anoxic rice paddy soil microcosms as examined by cultivation and direct 16S rRNA gene sequence retrieval. Appl Environ Microbiol 64 960–969 Occurrence Handle1:CAS:528:DyaK1cXhs1art74%3D Occurrence Handle9501436

    CAS  PubMed  Google Scholar 

  18. R Grosskopf S Stubner W Liesack (1998) ArticleTitleNovel euryarchaeotal lineages detected on rice roots and in the anoxic bulk soil of flooded rice microcosms. Appl Environ Microbiol 64 4983–4989 Occurrence Handle1:CAS:528:DyaK1cXnvF2htL8%3D Occurrence Handle9835592

    CAS  PubMed  Google Scholar 

  19. BA Hales C Edwards DA Ritchie G Hall RW Pickup JR Saunders (1996) ArticleTitleIsolation and identification of methanogen-specific DNA from blanket bog feat by PCR amplification and sequence analysis. Appl Environ Microbiol 62 668–675 Occurrence Handle1:CAS:528:DyaK28XovVCqtw%3D%3D Occurrence Handle8593069

    CAS  PubMed  Google Scholar 

  20. MSM Jetten AJM Stams AJB Zehnder (1992) ArticleTitleMethanogenesis from acetate—a comparison of the acetate metabolism in Methanothrix soehngenii and Methanosarcina spp. FEMS Microbiol Rev 88 181–197 Occurrence Handle1:CAS:528:DyaK38Xlt1Ort74%3D

    CAS  Google Scholar 

  21. M Krüger G Eller R Conrad P Frenzel (2002) ArticleTitleSeasonal variation in pathways of CH4 production and in CH4 oxidation in rice fields determined by stable carbon isotopes and specific inhibitors. Global Change Biol 8 265–280 Occurrence Handle10.1046/j.1365-2486.2002.00476.x

    Article  Google Scholar 

  22. M Krüger P Frenzel R Conrad (2001) ArticleTitleMicrobial processes influencing methane emission from rice fields. Global Change Biol 7 49–63 Occurrence Handle10.1046/j.1365-2486.2001.00395.x

    Article  Google Scholar 

  23. S Lehmann-Richter R Grosskopf W Liesack P Frenzel R Conrad (1999) ArticleTitleMethanogenic archaea and CO2-dependent methanogenesis on washed rice roots. Environ Microbiol 1 159–166 Occurrence Handle10.1046/j.1462-2920.1999.00019.x Occurrence Handle1:CAS:528:DyaK1MXktFykuro%3D Occurrence Handle11207731

    Article  CAS  PubMed  Google Scholar 

  24. J Lelieveld PJ Crutzen FJ Dentener (1998) ArticleTitleChanging concentrations, lifetime and climate forcing of atmospheric methane. Tellus 50B 128–150 Occurrence Handle1:CAS:528:DyaK1cXivFertbk%3D

    CAS  Google Scholar 

  25. D Lloyd et al. (1998) ArticleTitleMicro-ecology of peat—minimally invasive analysis using confocal laser scanning microscopy, membrane inlet mass spectrometry, and PCR amplification of methanogen-specific gene sequences. FEMS Microbiol Ecol 25 179–188 Occurrence Handle10.1016/S0168-6496(97)00094-9 Occurrence Handle1:CAS:528:DyaK1cXht1WgsbY%3D

    Article  CAS  Google Scholar 

  26. T Lueders KJ Chin R Conrad M Friedrich (2001) ArticleTitleMolecular analyses of methyl-coenzyme M reductase alpha-subunit (mcrA) genes in rice field soil and enrichment cultures reveal the methanogenic phenotype of a novel archaeal lineage. Environ Microbiol 3 194–204 Occurrence Handle10.1046/j.1462-2920.2001.00179.x Occurrence Handle11321536

    Article  PubMed  Google Scholar 

  27. T Lueders M Friedrich (2000) ArticleTitleArchaeal population dynamics during sequential reduction processes in rice field soil. Appl Environ Microbiol 66 2732–2742 Occurrence Handle10877762

    PubMed  Google Scholar 

  28. T Lueders MW Friedrich (2002) ArticleTitleEffects of amendment with ferrihydrite and gypsum on the structure and activity of methanogenic populations in rice field soil. Appl Environ Microbiol 68 2484–2494 Occurrence Handle10.1128/AEM.68.5.2484-2494.2002 Occurrence Handle1:CAS:528:DC%2BD38XjsFGqtbg%3D Occurrence Handle11976125

    Article  CAS  PubMed  Google Scholar 

  29. T Lueders MW Friedrich (2003) ArticleTitleEvaluation of PCR amplification bias by terminal restriction fragment length polymorphism analysis of small-subunit rRNA and mcrA genes by using defined template mixtures of methanogenic oure cultures and soil DNA extracts. Appl Environ Microbiol 69 320–326 Occurrence Handle10.1128/AEM.69.1.320-326.2003 Occurrence Handle1:CAS:528:DC%2BD3sXkvValsw%3D%3D Occurrence Handle12514011

    Article  CAS  PubMed  Google Scholar 

  30. PE Luton JM Wayne RJ Sharp PW Riley (2002) ArticleTitleThe mcrA gene as an alternative to 16S rRNA in the phylogenetic analysis of methanogen populations in landfill. Microbiology 148 3521–3530 Occurrence Handle1:CAS:528:DC%2BD38Xpt1ekt7o%3D Occurrence Handle12427943

    CAS  PubMed  Google Scholar 

  31. D Nercessian M Upton D Lloyd C Edwards (1999) ArticleTitlePhylogenetic analysis of peat bog methanogen populations. FEMS Microbiol Lett 173 425–429 Occurrence Handle10.1016/S0378-1097(99)00073-7 Occurrence Handle1:CAS:528:DyaK1MXitFWrtbs%3D

    Article  CAS  Google Scholar 

  32. B Nüsslein KJ Chin W Eckert R Conrad (2001) ArticleTitleEvidence for anaerobic syntrophic acetate oxidation during methane production in the profundal sediment of subtropical Lake Kinneret (Israel). Environ Microbiol 3 460–470 Occurrence Handle10.1046/j.1462-2920.2001.00215.x Occurrence Handle11553236

    Article  PubMed  Google Scholar 

  33. M Ohkuma S Noda K Horikoshi T Kudo (1995) ArticleTitlePhylogeny of symbiotic methanogens in the gut of the termite Reticulitermes speratus. FEMS Microbiol Lett 134 45–50 Occurrence Handle10.1016/0378-1097(95)00379-J Occurrence Handle1:CAS:528:DyaK2MXps1WqsLw%3D Occurrence Handle8593954

    Article  CAS  PubMed  Google Scholar 

  34. B Ramakrishnan T Lueders PF Dunfield R Conrad MW Friedrich (2001) ArticleTitleArchaeal community structures in rice soils from different geographical regions before and after initiation of methane production. FEMS Microbiol Ecol 37 175–186 Occurrence Handle10.1016/S0168-6496(01)00158-1 Occurrence Handle1:CAS:528:DC%2BD3MXnslCisbg%3D

    Article  CAS  Google Scholar 

  35. D Scheid S Stubner R Conrad (2003) ArticleTitleEffects of nitrate- and sulfate-amendment on the methanogenic populations in rice roots incubations. FEMS Microbiol Ecol 43 309–315 Occurrence Handle10.1016/S0168-6496(02)00432-4 Occurrence Handle1:CAS:528:DC%2BD3sXhvFeqtr0%3D

    Article  CAS  Google Scholar 

  36. RD Shannon JR White (1996) ArticleTitleThe effects of spatial and temporal variations in acetate and sulfate on methane cycling in two Michigan peatlands. Limnol Oceanogr 41 435–443 Occurrence Handle1:CAS:528:DyaK28XkvFKht7w%3D

    CAS  Google Scholar 

  37. LK Sigren ST Lewis FM Fisher RL Sass (1997) ArticleTitleEffects of field drainage on soil parameters related to methane production and emission from rice paddies. Global Biogeochem Cycles 11 151–162 Occurrence Handle1:CAS:528:DyaK2sXjslSmsr8%3D

    CAS  Google Scholar 

  38. E Springer MS Sachs CR Woese DR Boone (1995) ArticleTitlePartial gene sequences for the A subunit of methyl-coenzyme M reductase (mcrI) as a phylogenetic tool for the family Methanosarcinaceae. Int J Syst Bacteriol 45 554–559

    Google Scholar 

  39. A Watanabe T Takeda M Kimura (1999) ArticleTitleEvaluation of origins of CH4 carbon emitted from rice paddies. J Geophys Res 104 23623–23629 Occurrence Handle10.1029/1999JD900467 Occurrence Handle1:CAS:528:DyaK1MXntleht78%3D

    Article  CAS  Google Scholar 

  40. S Weber T Lueders MW Friedrich R Conrad (2001) ArticleTitleMethanogenic populations involved in the degradation of rice straw in anoxic paddy soil. FEMS Microbiol Ecol 38 11–20 Occurrence Handle10.1016/S0168-6496(01)00168-4 Occurrence Handle1:CAS:528:DC%2BD38XitVyi

    Article  CAS  Google Scholar 

  41. XL Wu KJ Chin R Conrad (2002) ArticleTitleEffect of temperature stress on structure and function of the methanogenic archaeal community in a rice field soil. FEMS Microbiol Ecol 39 211–218 Occurrence Handle10.1016/S0168-6496(01)00216-1 Occurrence Handle1:CAS:528:DC%2BD38XjsFOjurw%3D

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank Peter Claus for analysis of 13C-isotopic data and the Fonds der Chemischen Industrie, Germany, for financial support.

Author information

Authors and Affiliations

  1. Max-Planck-Institut für terrestrische Mikrobiologie, Karl-von-Frisch-Str., 35043 Marburg, Germany

    K. -J. Chin, T. Lueders, M. W. Friedrich, M. Klose & R. Conrad

Authors
  1. K. -J. Chin
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. T. Lueders
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. M. W. Friedrich
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. M. Klose
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. R. Conrad
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to R. Conrad.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Chin, KJ., Lueders, T., Friedrich, M. et al. Archaeal Community Structure and Pathway of Methane Formation on Rice Roots . Microb Ecol 47, 59–67 (2004). https://doi.org/10.1007/s00248-003-2014-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-003-2014-7

Keywords

Search

Navigation