Dokument

Summary:
Phylogenetically higher termites emit higher amounts of methane than lower termites, but the reason for this phenomenon has not been clear. Our comparative study based on 16S rRNA gene sequencing and qPCR analysis of archaeal communities in the guts of higher termites revealed that unlike the lower termites, which host mainly members of Methanobacteriales in their guts, higher termites host a diverse assemblage of methanogenic euryarchaeota comprising representatives of four major orders: Methanobacteriales, Methanosarcinales, Methanomicrobiales and the recently discovered Methanoplasmatales. 16S rRNA-based diversity of archaea was highest in soil-feeding taxa, where nearly all major archaeal groups were represented. Besides the euryarchaeotal lineages, the gut contained also lineages closely related to ammonia-oxidizing Thaumarchaeota and a deep-branching termite specific group of uncultured archaea loosely affiliated to Crenarchaeota. Archaeal diversity in the fungus-cultivating Macrotermes species, in the grass-feeding Trinervitermes sp., and in the wood-feeding Microcerotermes sp., which show low methane emission rates, was much lower. These results show the high methane emission rates in higher termites is reflected in the high diversity, density and complex community structure of archaea in the termite hindguts. Higher termites host gut-specific archaeal communities different from those of lower termites and from other environments and these communities seem to co-evolve with the host termite probably with shift in feeding behavior. Higher termites harbor archaeal lineages which are specific to their gut environment and are different from communities from lower termites and from other environments. Methanogenic archaea are heterogeneously distributed in the highly compartmented gut. Density and diversity of archaea was highest in posterior gut compartments, which also harbored most of the methanogenic activities. The highly alkaline anterior gut compartments were preferentially colonized by Methanosarcinales. Archaeal community structure differed strongly among gut compartments, with communities in the more methanogenic posterior gut sections being distinct from those of the anterior sections, a phenomenon that is reflected in the different micro-environmental conditions in the compartments. Experimental stimulation of methanogenesis in isolated gut sections of soil-feeding termites revealed significant activities of hydrogenotrophic methanogens that are obligately dependent on methanol and formate. Our results suggest that community structure in the different microhabitats is shaped by exogenous factors, such as pH, oxygen status and the availability of methanogenic substrates. The recently discovered Methanoplasmatales are the seventh order of methanogenic euryarchaeota comprising methylotrophic lineages which colonizes higher termite guts and various other environments, and helps to explain the high methane emission rates in higher termites. The methylotrophic nature of termite-derived lineage demonstrates that substrates other than hydrogen drive methanogenesis in higher termites.

Bibliographie / References

1. Lemke, T., Stingl, U., Egert, M., Friedrich, M.W., 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. Microbiol. 69:6650–6658.
2. References Boga, H.I., Brune, A. (2003). Hydrogen-dependent oxygen reduction by homoacetogenic bacteria isolated from termite guts. Appl. Environ. Microbiol. 69:779–786.
3. Leadbetter, J.R. Breznak, J.A. (1996). Physiological ecology of Methanobrevibacter cuticularis sp. nov. and Methanobrevibacter curvatus sp. nov., isolated from the hindgut of the termite Reticulitermes flavipes. Appl. Environ. Microbiol. 62:3620– 3631.
4. Miller, T.L., Meyer, J.W. (1985). Methanosphaera stadtmaniae gen. nov., sp. nov.: a species that forms methane by reducing methanol with hydrogen. Arch. Microbiol. 141:116–122.
5. Pester, M., Brune, A. (2007). Hydrogen is the central free intermediated during lignocellulose degradation by termite gut symbionts. ISME J. 1:551–565.
6. Methane and hydrogen production in a termite-symbiont system. Ecol. Res. 13:241– 257.
7. Donovan, S.E. (2002). A morphological study of the enteric valves of the Afrotropical Apicotermitinae (Isoptera: Termitidae). J. Nat. Hist. 36:1823–1840.
8. Tokura, M., Ohkuma, M., Kudo, T. (2000). Molecular phylogeny of methanogens associated with flagellated protists in the gut and with the gut epithelium of termites. FEMS Microbiol. Ecol. 33:233–240.
9. Molecular phylogenetic profiling of prokaryotic communities in guts of termites with different feeding habits, FEMS Microbiol. Ecol. 35:27–36.
10. Ohkuma, M., Noda, S., Kudo, T. (1999). Phylogenetic relationships of symbiotic methanogens in diverse termites. FEMS Microbiol. Lett. 171:147–153.
11. Deevong, P., Hattori, S., Yamada, A., Trakulnaleamsai, S., Ohkuma, M., Noparatnaraporn, N., Kudo, T. (2004). Isolation and detection of methanogens from the gut of higher termites. Microb. Environ. 19:221–226.
12. Phylogenetic relationship of symbiotic archaea in the gut of the higher termite Nasutitermes takasagoensis fed with various carbon sources. Microb.
13. Huang, L-N., Zhou, H., Chen, Y-Q., Luo, S., Lan, C-Y., Qu, L-H. (2002). Diversity and structure of the archaeal community in the leachate of a full-scale recirculating landfill as examined by direct 16S rRNA gene sequence retrieval. FEMS Microbiol. Lett. 214:235–240.
14. Noirot, C. (1992). From wood-feeding to soil-feeding: an important trend in termite evolution. In: Billen J (ed.), Biology and evolution of social insects. Leuven University Press, Leuven, pp. 107–119.
15. General discussion and prospects
16. General discussion and prospects 209
17. Sugimoto, A., Bignell, D.E., MacDonald, J.A. (2000). Global impact of termites on the carbon cycle and atmospheric trace gases. In: Abe T, Bignell DE, Higashi M (eds.), Termites: evolution, sociality, symbioses, ecology. Kluwer Academic Publishers, Dordrecht, pp. 409–435.
18. Donovan, S.E., Eggleton, P., Bignell, D.E. (2001). Gut content analysis and a new feeding group classification of termites. Ecol. Entomol. 26:356–366. General discussion and prospects
19. Köhler, T., Dietrich, C., Scheffrahn, R.H., Brune, A. (2012). High-resolution analysis of gut environment and bacterial microbiota reveals functional compartmentation of the gut in wood-feeding higher termites (Nasutitermes spp.). Appl. Environ. Microbiol. 78:4691–4701.
20. Shinzato, N., Yoshino, H., Yara, K. (1992). Methane production by microbial symbionts in the lower and higher termites of the Ryukyu Archipelago. In: Sato S, Ishida M, Ishikawa H (eds.), Endocytobiology V. Tübingen University Press, Tübingen, pp. 161–166.
21. Brune, A. (2010). Methanogens in the digestive tract of termites. In: Hackstein JHP (ed.), (Endo)symbiotic Methanogenic Archaea. Springer, Heidelberg, Germany, pp. 81–100.
22. Sprenger, W.W., van Belzen, M.C., Rosenberg, J., Hackstein, J.H.P., Keltjens, J.T. (2000). Methanomicrococcus blatticola gen. nov., sp., nov., a methanol-and methylamine-reducing methanogen from the hindgut of the cockroach Periplaneta americana. Int. J. Syst. Evol. Microbiol. 50:1989–1999.
23. Mihajlovski, A., Dore, J., Levenez, F., Alric, M., Brugère, J.F. (2010). Molecular evaluation of the human gut methanogenic archaeal microbiota reveals an age- associated increase of the diversity. Environ. Microbiol. Rep. 2:272–280.
24. Ohkuma, M., Noda, S., Horikoshi, K., Kudo, T. (1995). Phylogeny of symbiotic methanogens in the gut of the termite Reticulitermes speratus. FEMS Microbiol. Lett. 134:45–50.
25. Breznak, J.A., Brune, A. (1994). Role of microorganisms in the digestion of lignocelluloses by termites. Annu. Rev. Entomol. 39:453–487.
26. Bignell, D.E., Eggleton, P., Nunes, L., Thomas, K.L. (1997). Termites as mediators of carbon fluxes in tropical forest: budgets for carbon dioxide and methane emissions. General discussion and prospects 206
27. van Hoek, AHAM., van Alen, T.A., Sprakel, V.S.I., Leunissem, JAM., Brigge, T., Vogels, G.D., Hackstein, JHP. (2000). Multiple acquisition of methanogenic archaeal symbionts by anaerobic ciliates. Mol. Biol. Evol. 17:251–258.
28. Hatzenpichler, R., Lebedeva, E.V., Spieck, E., Stoecker, K., Richter, A., Daims, H., Wagner, M. (2008). A moderately thermophilic ammonia-oxidizing crenarchaeote from a hot spring. Proc. Natl. Acad. Sci. 105:2134–2139.
29. Hongoh, Y., Ohkuma, M. (2010). Termite gut flagellates and their methanogenic and eubacterial symbionts. In: Hackstein JHP (ed.), (Endo)symbiotic Methanogenic Archaea. Springer, Heidelberg, pp. 55–79.
30. Purdy, K.J. (2007). The distribution and diversity of Euryarchaeota in termite guts. Adv. Appl. Microbiol. 62:63–80.
31. Brauman, A., Kane, D.M., Labat, M., Breznak, J.A. (1992). Genesis of acetate and methane by gut bacteria of nutritionally diverse termites. Science 257: 1384–1387.
32. Hatamoto, M., Imachi, H., Ohashi, A., Hara, H. (2007). Identification and cultivation of anaerobic, syntrophic long-chain fatty acid-degrading microbes from mesophilic and thermophilic methanogenic sludges. Appl. Environ. Microbiol. 73:1332–1340.
33. Pester, M., Tholen, A., Friedrich, M.W., Brune, A. (2007). Methane oxidation in termite hindguts: absence of evidence and evidence of absence. Appl. Environ. Microbiol. 73:2024–2028.
34. Wright, A-D.G, Auckland, C.H., Lynn, D.H. (2007). Molecular diversity of methanogens in feedlot cattle from Ontario and Prince Edward Island, Canada. Appl. Environ. Microbiol. 73:4206–4210.
35. Anderson, I., Ulrich, L.E., Lupa, B., Susanti, D., Porat, I., Hooper, S.D., Lykidis, A., Sieprawska-Lupa, M., Dharmarajan, L., Goltsman, E., Lapidus, A., Saunders, E., Han, C., Land, M., Lucas, S., Mukhopadhyay, B., Whitman, W.B., Woese, C., Bristow, J., Kyrpides, N. (2009). Genomic characterization of Methanomicrobiales reveals three classes of methanogens. PLoS ONE 4:e5797.
36. Nitrososphaera viennensis, an ammonia oxidizing archaeon from soil. PNAS 108:8420–8425.
37. Paul, K., Nonoh, J.O., Mikulski, L., Brune, A. (2012). " Methanoplasmatales, " Thermoplasmatales-related archaea in termite guts and other environments, are the Seventh order of methanogens. Appl. Environ. Microbiol. 78:8245–8253.
38. Acinas S.G., Marcelino, L.A., Klepac-Ceraj, V., Polz, M.F. (2004). Divergence and redundancy of 16S rRNA sequences in genomes with multiple rrn operons. J. Bacteriol. 186:2629–2635.
39. Phylogenetic diversity of symbiotic methanogens living in the hindgut of the lower termite Reticulitermes speratus analyzed by PCR and in situ hybridization. Appl. Environ. Microbiol. 65:837–840.
40. Chin, K.J., Lukow, T., Conrad, R. (1999). Effect of temperature on structure and function of the methanogenic archaeal community in an anoxic rice field soil. Appl. Environ. Microbiol. 65:2341–2349.
41. 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. Microbiol. 65:4490–4496.
42. Tholen, A., Brune, A. (1999). Localization and in situ activities of homoacetogenic bacteria in the highly compartmentalized hindgut of soil-feeding higher termites (Cubitermes spp.). Appl. Environ. Microbiol. 65:4497–4505. General discussion and prospects 211
43. Mihajlovski, A., Alric, M., Brugère, J-F. (2008). A putative new order of methanogenic Archaea inhabiting the human gut, as revealed by molecular analyses of the mcrA gene. Res. Microbiol. 159:516–521.
44. Bapteste, E., Brochier, C., Boucher, Y. (2005). Higher-level classification of the Archaea: evolution of methanogenesis and methanogens. Archaea 1:353–363.

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