Biology and Fertility of Soils

, Volume 53, Issue 5, pp 491–499 | Cite as

Stimulation of methane oxidation by CH4-emitting rose chafer larvae in well-aerated grassland soil

  • Claudia Kammann
  • Stefan Ratering
  • Carolyn-Monika Görres
  • Cécile Guillet
  • Christoph Müller
Short Communication

Abstract

In this study, the impact of rose chafer (Cetonia aurata L.) larvae on net and gross methane (CH4) fluxes in soil from an old permanent grassland site (Giessen, Germany) was investigated. Previous studies at this site suggested the existence of Scarabaeidae larvae-induced “CH4-emitting hot spots” within the soil profile which may subsequently lead to increased CH4 oxidation. The net (soil + larvae) and gross (soil and larvae separated) CH4 fluxes were studied in a 3-month laboratory incubation. Addition of larvae changed the soil from a net sink (−330 ± 11 ng CH4 kg−1 h−1) to a net source (637 ± 205 ng CH4 kg−1 h−1). Supply of plant litter to the soil + larvae incubation jars tended to increase CH4 emissions which was not significant due to large variability. After 11–13 weeks of incubation, the net soil CH4 oxidation was significantly stimulated by 13–21% in the treatments containing larvae when these were taken out. Analysis of archaeal 16S rRNA genes revealed that the majority of the obtained clones were closely related to uncultured methanogens from guts of insects and other animals. Other sequences were relative to cultivated species of Methanobrevibacter, Methanoculleus, and Methanosarcina. Hence, Scarabaeidae larvae in soils (i) may represent an underestimated source of CH4 emissions in aerobic upland soils, (ii) may stimulate gross CH4 consumption in their direct soil environment, and, thus, (iii) contribute to the spatial heterogeneity often observed in the field with closed-chamber measurements. Long-term CH4-flux balances may be wrongly assessed when “exceptional” net CH4 flux rates (due to larvae hot spots) are excluded from data sets.

Keywords

Scarabaeidae larvae Cetonia aurata Methane production Stimulation of CH4 consumption Methanogenic Archaea Grassland soil 

References

  1. Borrel G, Parisot N, Harris HMB, Peyretaillade E, Gaci N, Tottey W, Bardot O, Raymann K, Gribaldo S, Peyret P, O'Toole PW, Brugere J-F (2014) Comparative genomics highlights the unique biology of Methanomassiliicoccales, a Thermoplasmatales-related seventh order of methanogenic archaea that encodes pyrrolysine. BMC Genomics 15:679. doi:10.1186/1471-2164-15-679 CrossRefPubMedPubMedCentralGoogle Scholar
  2. Bradley RL, Chronáková A, Elhottová D, Simek M (2012) Interactions between land-use history and earthworms control gross rates of soil methane production in an overwintering pasture. Soil Biol Biochem 53:64–71. doi:10.1016/j.soilbio.2012.04.025 CrossRefGoogle Scholar
  3. Brauman A, Doré J, Eggleton P, Bignell D, Breznak JA, Kane MD (2001) Molecular phylogenetic profiling of prokaryotic communities in guts of termites with different feeding habits. FEMS Microbiol Ecol 35:27–36. doi:10.1111/j.1574-6941.2001.tb00785.x CrossRefPubMedGoogle Scholar
  4. Breznak JA (1975) Symbiotic relationships between termites and their intestinal microbiota. Sym Soc Exp Biol 29:559–580Google Scholar
  5. Brune A (2010) Methanogenesis in the digestive tracts of insects. In: Timmis KN (ed) Handbook of hydrocarbon and lipid microbiology. Springer, Berlin Heidelberg, pp 707–728CrossRefGoogle Scholar
  6. Ciais P, Sabine C, Bala G, Bopp L, Brovkin V, Canadell J, Chhabra A, De Fries R, Galloway J, Heimann M, Jones C, Le Quéré C, Myneni RB, Piao S, Thornton P (2013) Carbon and other biogeochemical cycles. In: Stocker TF, Qin D, Plattner GK, 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 and New York, pp 465–570Google Scholar
  7. Dunfield PF, Liesack W, Henckel T, Knowles R, Conrad R (1999) High-affinity methane oxidation by a soil enrichment culture containing a type II methanotroph. Appl Environ Microb 65:1009–1014Google Scholar
  8. Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200. doi:10.1093/bioinformatics/btr38 CrossRefPubMedPubMedCentralGoogle Scholar
  9. Egert M, Wagner B, Lemke T, Brune A, Friedrich MW (2003) Microbial community structure in midgut and hindgut of the humus-feeding larva of Pachnoda ephippiata (Coleoptera: Scarabaeidae). Appl Environ Microb 69:6659–6668. doi:10.1128/AEM.69.11.6659-6668.2003 CrossRefGoogle Scholar
  10. Egert M, Stingl U, Dyhrberg Bruun L, Pommerenke B, Brune A, Friedrich MW (2005) Structure and topology of microbial communities in the major gut compartments of Melolontha melolontha larvae (Coleoptera: Scarabaeidae). Appl Environ Microb 71:4556–4566. doi:10.1128/AEM.71.8.4556-4566.2005 CrossRefGoogle Scholar
  11. Felsenstein J (1989) PHYLIP—phylogeny inference package (version 3.2). Cladistics 5:164–166Google Scholar
  12. Gentzel T, Hershey AE, Rublee PA, Whalen SC (2012) Net sediment production of methane, distribution of methanogens and methane-oxidizing bacteria, and utilization of methane-derived carbon in an arctic lake. Inland Waters 2:77–88. doi:10.5268/IW-2.2.416 CrossRefGoogle Scholar
  13. Gijzen HJ, Van Der Drift C, Barugahare M, Op Den Camp HJM (1994) Effect of host diet and hindgut microbial composition on cellulolytic activity in the hindgut of the American cockroach, Periplaneta americana. Appl Environ Microb 60:1822–1826Google Scholar
  14. Großkopf R, Janssen PH, Liesack W (1998) Diversity 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 Microb 64:960–969Google Scholar
  15. Hackstein JHP, Stumm CK (1994) Methane production in terrestrial arthropods. Proc Natl Acad Sci U S A 91:5441–5445CrossRefPubMedPubMedCentralGoogle Scholar
  16. Hackstein JHP, Langer P, Rosenberg J (1996) Genetic and evolutionary constraints for the symbiosis between animals and methanogenic bacteria. Environ Monit and Assess 42:39–56CrossRefGoogle Scholar
  17. Hackstein JHP, van Alen TA, Rosenberg J (2006) Methane production by terrestrial arthropods. In: König H, Varma A (eds) Soil biology—manual for soil analysis. Springer, Berlin Heidelberg, pp 155–180Google Scholar
  18. Hery M, Singer AC, Kumaresan D, Bodrossy L, Stralis-Pavese N, Prosser JI, Thompson IP, Murrell JC (2007) Effect of earthworms on the community structure of active methanotrophic bacteria in a landfill cover soil. ISME J 2:92–104. doi:10.1038/ismej.2007.66 CrossRefPubMedGoogle Scholar
  19. Jäger H-J, Schmidt SW, Kammann C, Grünhage L, Müller C, Hanewald K (2003) The University of Giessen Free-Air Carbon Dioxide Enrichment study: description of the experimental site and of a new enrichment system. J Appl Bot 77:117–127Google Scholar
  20. Kajan R, Frenzel P (1999) The effect of chironomid larvae on production, oxidation and fluxes of methane in a flooded rice soil. FEMS Microbiol Ecol 28:121–129. doi:10.1016/S0168-6496(98)00097-X CrossRefGoogle Scholar
  21. Kammann C, Grünhage L, Jäger H-J, Wachinger G (2001a) Methane fluxes from differentially managed grassland study plots: the important role of CH4 oxidation in grassland with a high potential for CH4 production. Environ Pollut 115:261–273. doi:10.1016/S0269-7491(01)00103-8 CrossRefPubMedGoogle Scholar
  22. Kammann C, Grünhage L, Jäger H-J (2001b) A new sampling technique to monitor concentrations of CH4, N2O and CO2 in air at well-defined depths in soils with varied water potential. Eur J Soil Sci 52:297–303. doi:10.1046/j.1365-2389.2001.00380.x CrossRefGoogle Scholar
  23. Kammann C, Hepp S, Lenhart K, Müller C (2009) Stimulation of methane consumption by endogenous CH4 production in aerobic grassland soil. Soil Biol Biochem 41:622–629. doi:10.1016/j.soilbio.2008.12.025 CrossRefGoogle Scholar
  24. Kampmann K, Ratering S, Kramer I, Schmidt M, Zerr W, Schnell S (2012) Unexpected stability of Bacteroidetes and Firmicutes communities in laboratory biogas reactors fed with different defined substrates. Appl Environ Microb 78:2106–2119. doi:10.1128/AEM.06394-11 CrossRefGoogle Scholar
  25. Kane MD, Breznak JA (1991) Effect of host diet on production of organic acids and methane by cockroach gut bacteria. Appl Environ Microb 57:2628–2634Google Scholar
  26. Keidel L, Kammann C, Grünhage L, Moser G, Müller C (2015) Positive feedback of elevated CO2 on soil respiration rate in late autumn and winter. Biogeosciences 12:1257–1269. doi:10.5194/bg-12-1257-2015 CrossRefGoogle Scholar
  27. Kernecker M, Whalen JK, Bradleyet RL (2015) Endogeic earthworms lower net methane production in saturated riparian soils. Biol Fertil Soils 51:271–274. doi:10.1007/s00374-014-0965-0 CrossRefGoogle Scholar
  28. Koubová A, Goberna M, Šimek M, Chroňáková A, Pižl V, Insam H, Elhottová D (2012) Effects of the earthworm Eisenia andrei on methanogens in a cattle-impacted soil: a microcosm study. Eur J Soil Biol 48:32–40. doi:10.1016/j.ejsobi.2011.09.007 CrossRefGoogle Scholar
  29. Leal JJF, dos Santos Furtado AL, de Assis EF, Bozelli RL, Figueiredo-Barros M (2007) The role of Campsurus notatus (Ephemeroptera: Polymitarcytidae) bioturbation and sediment quality on potential gas fluxes in a tropical lake. Hydrobiologia 586:143–154. doi:10.1007/s10750-006-0570-9 CrossRefGoogle Scholar
  30. Lemke T, Stingl U, Egert M, Friedrich MW, Brune A (2003) Physicochemical conditions and microbial activities in the highly alkaline gut of the humus-feeding larva of Pachnoda ephippiata (Coleoptera: Scarabaeidae). Appl Environ Microb 69:6650–6658. doi:10.1128/AEM.69.11.6650-6658.2003 CrossRefGoogle Scholar
  31. Loftfield N, Flessa H, Augustin J, Beese F (1997) Automated gas chromatographic system for rapid analysis of the atmospheric trace gases methane, carbon dioxide, and nitrous oxide. J Environ Qual 26:560–564. doi:10.2134/jeq1997.00472425002600020030x CrossRefGoogle Scholar
  32. Ludwig W, Strunk O, Westram R, Richter L, Meier H et al (2004) ARB: a software environment for sequence data. Nucleic Acids Res 32:1363–1371. doi:10.1093/nar/gkh293 CrossRefPubMedPubMedCentralGoogle Scholar
  33. Mohanty SR, Tiwari S, Dubey G, Ahirwar U, Kollah B (2016) How methane feedback response influence redox processes in a tropical vertisol. Biol Fertil Soils 52:479–490. doi:10.1007/s00374-016-1090-z CrossRefGoogle Scholar
  34. Paul K, Nonoh JO, Mikulski L, Brune A (2012) “Methanoplasmatales,” thermoplasmatales-related archaea in termite guts and other environments, are the seventh order of methanogens. Appl Environ Microb 78:8245–8253. doi:10.1128/AEM.02193-12 CrossRefGoogle Scholar
  35. Pruesse E, Peplies J, Glöckner FO (2012) SINA: accurate high-throughput multiple sequence alignment of ribosomal RNA genes. Bioinformatics 28:1823–1829. doi:10.1093/bioinformatics/bts252 CrossRefPubMedPubMedCentralGoogle Scholar
  36. Rasmussen RA, Khalil MAK (1983) Global production of methane by termites. Nature 301:700–702CrossRefGoogle Scholar
  37. Schmitt-Wagner D, Brune A (1999) Hydrogen profiles and localization of methanogenic activities in the highly compartmentalized hindgut of soil-feeding higher termites (Cubitermes spp.) Appl Environ Microb 65:4490–4496Google Scholar
  38. Shrestha PM, Kammann C, Lenhart K, Dam B, Liesack W (2012) Linking activity, composition and seasonal dynamics of atmospheric methane oxidizers in a meadow soil. ISME J 6:1115–1126. doi:10.1038/ismej.2011.179 CrossRefPubMedGoogle Scholar
  39. Söllinger A, Schwab C, Weinmaier T, Loy A, Tveit AT, Schleper C, Urich T, King G (2016) Phylogenetic and genomic analysis of Methanomassiliicoccales in wetlands and animal intestinal tracts reveals clade-specific habitat preferences. FEMS Microbiol Ecol 92. doi:10.1093/femsec/fiv149
  40. Stahl DA, Amann A (1991) Development and application of nucleic acid probes in bacterial systematics. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. Wiley, Chichester, pp 205–248Google Scholar
  41. Šustr V, Chroňáková A, Semanová S, Tajovský K, Šimek M, Oliveira PL (2014) Methane production and methanogenic archaea in the digestive tracts of millipedes (Diplopoda). PLoS One 9:e102659. doi:10.1371/journal.pone.0102659 CrossRefPubMedPubMedCentralGoogle Scholar
  42. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739. doi:10.1093/molbev/msr121 CrossRefPubMedPubMedCentralGoogle Scholar
  43. Thummes K, Schäfer J, Kämpfer P, Jäckel U (2007) Thermophilic methanogenic archaea in compost material: occurrence, persistence and possible mechanisms for their distribution to other environments. Syst Appl Microbiol 30:634–643. doi:10.1016/j.syapm.2007.08.001 CrossRefPubMedGoogle Scholar
  44. Yarza P, Richter M, Peplies J, Euzeby J, Amann R, Schleifer K-H, Ludwig W, Glöckner FO, Rosselló-Móra R (2008) The all-species living tree project: a 16S rRNA-based phylogenetic tree of all sequenced type strains. Syst Appl Microbiol 31:241–250. doi:10.1016/j.syapm.2008.07.001 CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  1. 1.Department of Soil Science and Plant Nutrition, WG Climate Change Research for Special CropsHochschule Geisenheim UniversityGeisenheimGermany
  2. 2.Department of Plant EcologyUniversity GießenGiessenGermany
  3. 3.Department of Applied MicrobiologyUniversity GießenGiessenGermany
  4. 4.School of Biology and Environmental Science and Earth Science InstituteUniversity College DublinDublin 4Ireland

Personalised recommendations