AEM
Home Help [Feedback] [For Subscribers] [Archive] [Search] [Contents]
This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Other Versions of this Article:
AEM.02190-06v1
73/6/2024    most recent
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Pester, M.
Right arrow Articles by Brune, A.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Pester, M.
Right arrow Articles by Brune, A.
Agricola
Right arrow Articles by Pester, M.
Right arrow Articles by Brune, A.

 Previous Article  |  Next Article 

Applied and Environmental Microbiology, March 2007, p. 2024-2028, Vol. 73, No. 6
0099-2240/07/$08.00+0     doi:10.1128/AEM.02190-06
Copyright © 2007, American Society for Microbiology. All Rights Reserved.

SHORT REPORT

Methane Oxidation in Termite Hindguts: Absence of Evidence and Evidence of Absence{triangledown}

Michael Pester, Anne Tholen,{dagger} Michael W. Friedrich, and Andreas Brune*

Max Planck Institute for Terrestrial Microbiology, Department of Biogeochemistry, Karl-von-Frisch-Strasse, 35043 Marburg, Germany

Received 18 September 2006/ Accepted 11 January 2007


   ABSTRACT
Top
 Abstract
Introduction
 Influence of oxygen on...
 In vivo incubation with...
 Screening for methane-oxidizing...
 Ammonia as a potential...
 References
 
A steep oxygen gradient and the presence of methane render the hindgut internal periphery of termites a potential habitat for aerobic methane-oxidizing bacteria. However, methane emissions of various termites increased, if at all, only slightly when termites were exposed to an anoxic (nitrogen) atmosphere, and 14CH4 added to the air headspace over live termites was not converted to 14CO2. Evidence for the absence of methane oxidation in living termites was corroborated by the failure to detect pmoA, the marker gene for particulate methane monooxygenase, in hindgut DNA extracts of all termites investigated. This adds robustness to our concept of the degradation network in the termite hindgut and eliminates the gut itself as a potential sink of this important greenhouse gas.


   INTRODUCTION
Top
 Abstract
 Introduction
Influence of oxygen on...
 In vivo incubation with...
 Screening for methane-oxidizing...
 Ammonia as a potential...
 References
 
Methane is a metabolic end product in the hindgut of most termites (4, 26, 42), and it has been estimated that these insects contribute 2 to 4% to the global emissions of this important greenhouse gas (36, 41). Methanogenic archaea, which are easily identified by their coenzyme F420 autofluorescence, have been located in several microhabitats within the hindgut. Depending on the termite species, these organisms can be associated either with the hindgut wall (13, 21, 22) or with filamentous prokaryotes attached to the latter (21), or they can occur as ectosymbionts or endosymbionts of certain intestinal flagellates (23, 47).

Oxygen penetrating the gut wall forms a steep gradient in the hindgut internal periphery (50 to 200 µm) (7), where it inevitably overlaps with the methane emanating from within the gut (6). These are ideal conditions for methane-oxidizing bacteria (methanotrophs), which are typically found at the oxic-anoxic interface of, e.g., lake sediments, rice field soil, and peat bogs (8).

Since it is known that the mound walls of termites and the soil surrounding the nest harbor methanotrophic activity (41), a constant inoculation of termites with methanotrophs is easily envisaged. However, previous studies of termite hindgut metabolism either yielded no evidence for the presence of aerobic methane oxidation (27) or simply assumed that net emission rates of methane from living termites equal the gross rate of methanogenesis within the hindgut (e.g., 4, 37, 45). Only in one case has it been pointed out that the potential methane production rate calculated for the methanogenic population in Reticulitermes flavipes exceeds the methane emission rates of the termite by more than threefold (21), suggesting that methane oxidation might be present.

In this study, we aimed to resolve the issue of methane oxidation within termite hindguts by experimentation with various representatives from the most species-rich termite families (18). Investigated termites comprised the lower wood-feeding termites Reticulitermes santonensis (Feytaud), Reticulitermes flavipes (Kollar), Zootermopsis nevadensis (Hagen), Hodotermopsis sjoestedti (Holmgren), Cryptotermes secundus (Hill), Incisitermes marginipennis (Latreille), and Neotermes castaneus (Burmeister) as well as the higher soil-feeding termite Cubitermes orthognathus Emerson and the higher fungus-cultivating termite Macrotermes michaelseni Sjöstedt.


   Influence of oxygen on methane emission.
Top
 Abstract
 Introduction
 Influence of oxygen on...
In vivo incubation with...
 Screening for methane-oxidizing...
 Ammonia as a potential...
 References
 
Methane emission from living termites incubated in rubber-stoppered glass vials was measured by gas chromatography (37). All termite species tested emitted methane at a constant rate when incubated under air. Generally, flushing the headspace with nitrogen evoked a biphasic kinetic of methane emission (exemplified in Fig. 1A): (i) methane accumulation rates increased slightly immediately after flushing, and (ii) a continuous increase in methane emission occurred after approximately 15 to 20 min.


Figure 1
View larger version (13K):
[in this window]
[in a new window]

  		FIG. 1. Methane emission by living termites. (A) Time course of methane emission from Reticulitermes santonensis incubated under an atmosphere of air, which was replaced by flushing with N2 for 1 min at the time point indicated by the arrow. Similar curves were obtained for other species (data not shown). Rates of methane emission were calculated using the slopes of the linear regression curves under air and N2. (B) Methane emission rates by different termites under air and during the first 15 min after changing the headspace to N2. To illustrate the contribution to the carbon mineralization flux through the termite (45), the values in Table 1 were normalized to the combined CO2 and CH4 emission rates under air. Bars represent the average of three independent assays; standard deviations are given.

 
The immediate increase of methane emission after the removal of oxygen can be explained by two different processes. First, the removal of oxygen would immediately cause a cessation of methane oxidation by methanotrophs, thereby increasing the efflux of methane from the gut. Second, methanogenesis itself may increase if oxygen is removed. This has been demonstrated for Methanobrevibacter cuticularis, an oxygen-consuming methanogen residing in the microoxic gut periphery of Reticulitermes flavipes (21), with cell suspensions that were exposed to low oxygen fluxes (43). A diversion of reducing equivalents from methanogenesis toward oxygen reduction is substantiated by the finding of an F420H2-oxidase in Methanobrevibacter arboriphilus (38).

It is not possible to differentiate between the two processes, but even if the small rate changes upon removal of oxygen were completely due to methanotrophic activity, the respective methane oxidation rates would account for at most 0.3% of the carbon mineralization flux through the termite (Fig. 1B). The delayed, continuous increase is most likely an indirect effect of methanogenesis, caused by elevated hindgut hydrogen partial pressures in the absence of oxygen, as previously documented for Reticulitermes flavipes and Cubitermes orthognathus (12, 37), and has no further implications for methane oxidation.

Although methane emission rates increased slightly but not always significantly after gassing with N2 for the majority of the termites investigated (Fig. 1B), the results are somewhat ambiguous when data are compared at the level of the individual assay (Table 1). Generally, there was a strong variance between assays, and in the case of Cryptotermes secundus and Hodotermopsis sjoestedti, several batches even showed a decreased methane emission after the removal of oxygen, corroborating that methane oxidation, if present at all, is only marginal.


View this table:
[in this window]
[in a new window]

  		TABLE 1. Respiration rates and methane emission rates of termites incubated under air and under N2a

 

   In vivo incubation with 14CH4.
Top
 Abstract
 Introduction
 Influence of oxygen on...
 In vivo incubation with...
Screening for methane-oxidizing...
 Ammonia as a potential...
 References
 
The absence of methane oxidation was further supported by the results of a radiotracer study with Reticulitermes flavipes and Cubitermes orthognathus, representing lower and higher termites, respectively. Living termites were incubated for several days under an atmosphere of air supplemented with 14CH4, using the same setup as above. Shifts in the amounts of 14CH4 and 14CO2 were monitored over time by a gas chromatograph equipped with a methanizer and a radioactivity monitor (44). For both termite species, neither a decrease of 14CH4 nor a formation of 14CO2 was observed (Fig. 2), in the case of R. flavipes not even after 1 week of incubation, which provides sound evidence that methane oxidation is not taking place. The successful application of this strategy in a similar experiment with Nasutitermes walkeri (Hill), where 14CO2 supplemented to the headspace was subsequently converted to [14C]acetate in the hindgut (49), documents that a diffusion limitation of tracheal gas transport into the hindgut can be excluded.


Figure 2
View larger version (13K):
[in this window]
[in a new window]

  		FIG. 2. Incubation of living termites under an atmosphere of air supplemented with 14CH4. Data shown for Cubitermes orthognathus (closed symbols) represent means of two independent assays; the bars showing mean deviation are covered by the symbols. Data shown for Reticulitermes flavipes (open symbols) stem from a single experiment.

 

   Screening for methane-oxidizing microorganisms.
Top
 Abstract
 Introduction
 Influence of oxygen on...
 In vivo incubation with...
 Screening for methane-oxidizing...
Ammonia as a potential...
 References
 
Evidence for the absence of methane oxidation in living termites was corroborated by testing all termites studied for the presence of methanotrophs, using the pmoA gene, encoding the {alpha} subunit of the particulate methane monooxygenase, as a molecular marker. Primers targeting the pmoA gene of most methanotrophs (14) readily amplified pmoA genes from littoral lake sediment and the pmoA clones obtained from a previous study (34). However, they did not yield PCR products of the expected length (531 bp) with DNA extracted from termite hindgut contents (33), using the same protocol. In the case of Reticulitermes santonensis, a product of similar length was obtained, but cloning and sequencing revealed that it did not represent pmoA genes. Control experiments, where the same DNA extracts and amplification reagents were used to amplify 16S rRNA genes or fhs genes (PCR conditions were as described in references 50 and 33, respectively) always resulted in PCR products of the expected length, proving that a general inhibition of the PCRs can be excluded.

The absence of methane-oxidizing bacteria from termite guts is further supported by the extensive bacterial 16S rRNA gene clone libraries obtained from several Reticulitermes and Microcerotermes species (15, 16, 50). Among a total of 2,500 clones obtained from these termites, only a single clone (clone RS-K73 from Reticulitermes speratus) showed a loose phylogenetic affiliation with methanotrophic isolates (96 to 97% sequence identity with Methylocella species). In addition, none of the transmission electron micrographs of hindgut thin sections of lower and higher termites shows bacterial cells with structures resembling the typical internal membrane systems of methanotrophs (5, 10, 46, 51).

To exclude also the possibility of anaerobic methane oxidation, we conducted two PCR assays that specifically amplify the mcrA genes of ANME-1 or ANME-2 archaea (M. Krüger and M. W. Friedrich, unpublished data). Although DNA extracts of microbial mats, which showed anaerobic methane oxidation activity (25), always resulted in a specific PCR product, no mcrA genes were amplified from termite hindgut contents. Again, support for the absence of ANME archaea is provided by numerous archaeal 16S rRNA gene clone libraries obtained for various lower and higher termites (11, 13, 28-31, 39, 47). None of the clones in these libraries clusters with ANME-1, ANME-2, or ANME-3 archaea (phylogeny is summarized by Meyerdierks et al. [24]) or ANME archaea involved in anaerobic methane oxidation coupled to denitrification (35).


   Ammonia as a potential inhibitor.
Top
 Abstract
 Introduction
 Influence of oxygen on...
 In vivo incubation with...
 Screening for methane-oxidizing...
 Ammonia as a potential...
References
 
There may be numerous reasons for the absence of methanotrophs from termite hindguts, e.g., the high nutrient concentrations (27, 45), which are unfavorable for many methanotrophs (48), or even the presence of specific inhibitors. A concrete factor responsible for this phenomenon, however, may be ammonia, which is readily cooxidized by methane monooxygenase (1) and is thought to affect methane oxidation by competitive inhibition (2).

Ammonia concentrations in termite hindguts were found to correlate with the feeding guild of the respective termite (Table 2). In the hindgut paunch of all wood-feeding termites, total ammonia concentrations were in the lower millimolar range, which is reported to partially inhibit methane oxidation even at high concentrations of methane (3, 9, 19, 20, 32, 48).


View this table:
[in this window]
[in a new window]

  		TABLE 2. Total ammonia concentrations in the hindgut paunch of wood-feeding termites and the major hindgut compartments of fungus-cultivating and soil-feeding termites

 
In the fungus-cultivating termite Macrotermes michaelseni and the soil-feeding termite Cubitermes orthognathus, total ammonia concentrations in the individual gut sections were well above the concentrations found with wood-feeding termites (Table 2), with the highest values in the methane-producing posterior hindgut sections of C. orthognathus (37). Such concentrations completely inhibited methanotrophs in other studies (48). Curiously, the nest material of soil-feeding termites also contains high ammonia concentrations (17), and the determination of stable carbon isotope fractionation indicated that about 70% of the methane produced in the nest is oxidized within the mound wall (41).

In summary, the comprehensive evidence provided in this study documents (i) that methane is not oxidized in the termite hindgut and (ii) that methane-oxidizing bacteria are absent, irrespective of the phylogenetic status and feeding guild of the host. The results eliminate the gut itself as a potential sink of this important greenhouse gas and add robustness to our concept of the degradation network in the termite hindgut.


   ACKNOWLEDGMENTS
 
We thank Judith Korb, Roland Brandl, and Horst Hertel for providing termites, and we thank David Kamanda Ngugi, Hamadi Boga, Sybille Frankenberg, and Mahesh Desai for DNA preparations. The excellent technical assistance of Katja Meuser is gratefully acknowledged.


   FOOTNOTES
 
* Corresponding author. Mailing address: Max Planck Institute for Terrestrial Microbiology, Karl-von-Frisch-Strasse, 35043 Marburg, Germany. Phone: (49) 6421 178701. Fax: (49) 6421 178709. E-mail: brune{at}mpi-marburg.mpg.de. Back

{triangledown} Published ahead of print on 19 January 2007. Back

{dagger} Present address: Altana Pharma Deutschland GmbH, Moltkestrasse 4, 78467 Konstanz, Germany. Back


   REFERENCES
Top
 Abstract
 Introduction
 Influence of oxygen on...
 In vivo incubation with...
 Screening for methane-oxidizing...
 Ammonia as a potential...
 References
 

  1. Bedard, C., and R. Knowles. 1989. Physiology, biochemistry, and specific inhibitors of CH4, NH4+, and CO oxidation by methanotrophs and nitrifiers. Microbiol. Rev. 53:68-84.[Abstract/Free Full Text]
  2. Bodelier, P. L. E., and H. J. Laanbroek. 2004. Nitrogen as a regulatory factor of methane oxidation in soils and sediments. FEMS Microbiol. Ecol. 47:265-277.[CrossRef]
  3. Bosse, U., P. Frenzel, and R. Conrad. 1993. Inhibition of methane oxidation by ammonium in the surface layer of a littoral sediment. FEMS Microbiol. Ecol. 13:123-134.
  4. Brauman, A., M. D. Kane, M. Labat, and J. A. Breznak. 1992. Genesis of acetate and methane by gut bacteria of nutritionally diverse termites. Science 257:1384-1387.[Abstract/Free Full Text]
  5. Breznak, J. A., and H. S. Pankratz. 1977. In situ morphology of the gut microbiota of wood-eating termites [Reticulitermes flavipes (Kollar) and Coptotermes formosanus Shiraki]. Appl. Environ. Microbiol. 33:406-426.[Abstract/Free Full Text]
  6. Brune, A., and M. W. Friedrich. 2000. Microecology of the termite gut: structure and function on a microscale. Curr. Opin. Microbiol. 3:263-269.[CrossRef][Medline]
  7. Brune, A., D. Emerson, and J. A. Breznak. 1995. The termite gut microflora as an oxygen sink: microelectrode determination of oxygen and pH gradients in guts of lower and higher termites. Appl. Environ. Microbiol. 61:2681-2687.[Abstract]
  8. Brune, A., P. Frenzel, and H. Cypionka. 2000. Life at the oxic-anoxic interface: microbial activities and adaptations. FEMS Microbiol. Rev. 24:691-710.[Medline]
  9. Carlsen, H. N., L. Jørgensen, and H. Degn. 1991. Inhibition by ammonia of methane utilization of Methylococcus capsulatus (Bath). Appl. Microbiol. Biotechnol. 35:124-127.
  10. Czolij, R., M. Slaytor, and R. W. O'Brien. 1985. Bacterial flora of the mixed segment and the hindgut of the higher termite Nasutitermes exitiosus Hill (Termitidae, Nasutitermitinae). Appl. Environ. Microbiol. 49:1226-1236.
  11. Donovan, S. E., K. J. Purdy, M. D. Kane, and P. Eggleton. 2004. Comparison of Euryarchaea strains in the guts and food-soil of the soil-feeding termite Cubitermes fungifaber across different soil types. Appl. Environ. Microbiol. 70:3884-3892.[Abstract/Free Full Text]
  12. Ebert, A., and A. Brune. 1997. Hydrogen concentration profiles at the oxic-anoxic interface: a microsensor study of the hindgut of the wood-feeding lower termite Reticulitermes flavipes (Kollar). Appl. Environ. Microbiol. 63:4039-4046.[Abstract]
  13. Friedrich, M. W., D. Schmitt-Wagner, T. Lüders, and A. Brune. 2001. Axial differences in community structure of Crenarchaeota and Euryarchaeota in the highly compartmentalized gut of the soil-feeding termite Cubitermes orthognathus. Appl. Environ. Microbiol. 67:4880-4890.[Abstract/Free Full Text]
  14. Holmes, A. J., A. Costello, M. E. Lidstrom, and J. C. Murrell. 1995. Evidence that particulate methane monooxygenase and ammonia monooxygenase may be evolutionarily related. FEMS Microbiol. Lett. 132:203-208.[CrossRef][Medline]
  15. Hongoh, Y., M. Ohkuma, and T. Kudo. 2003. Molecular analysis of bacterial microbiota in the gut of the termite Reticulitermes speratus (Isoptera; Rhinotermitidae). FEMS Microbiol. Ecol. 44:231-242.
  16. Hongoh, Y., P. Deevong, T. Inoue, S. Moriya, S. Trakulnaleamsai, M. Ohkuma, C. Vongkaluang, N. Noparatnaraporn, and T. Kudo. 2005. Intra- and interspecific comparisons of bacterial diversity and community structure support coevolution of gut microbiota and termite host. Appl. Environ. Microbiol. 71:6590-6599.[Abstract/Free Full Text]
  17. Ji, R., and A. Brune. 2006. Nitrogen mineralization, ammonia accumulation, and emission of gaseous NH3 by soil-feeding termites. Biogeochemistry 78:267-283.
  18. Kambhampati, S., and P. Eggleton. 2000. Taxonomy and phylogenetics of Isoptera, p. 1-23. In T. Abe, D. E. Bignell, and M. Higashi (ed.), Termites: evolution, sociality, symbiosis, ecology. Kluwer Academic Publishers, Dordrecht, The Netherlands.
  19. King, G. M., and S. Schnell. 1998. Effects of ammonium and non-ammonium salt additions on methane oxidation by Methylosinus trichosporium OB3b and Maine forest soils. Appl. Environ. Microbiol. 64:253-257.[Abstract/Free Full Text]
  20. King, G. M., and S. Schnell. 1994. Ammonium and nitrite inhibition of methane oxidation by Methylobacter albus BG8 and Methylosinus trichosporium OB3b at low methane concentrations. Appl. Environ. Microbiol. 60:3508-3513.[Abstract/Free Full Text]
  21. Leadbetter, J. R., and J. A. Breznak. 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.[Abstract]
  22. Leadbetter, J. R., L. D. Crosby, and J. A. Breznak. 1998. Methanobrevibacter filiformis sp. nov., a filamentous methanogen from termite hindguts. Arch. Microbiol. 169:287-292.[CrossRef][Medline]
  23. Lee, M. J., P. J. Schreurs, A. C. Messer, and S. H. Zinder. 1987. Association of methanogenic bacteria with flagellated protozoa from a termite hindgut. Curr. Microbiol. 15:337-341.
  24. Meyerdierks, A., M. Kube, T. Lombardot, K. Knittel, M. Bauer, F. O. Glöckner, R. Reinhardt, and R. Amann. 2005. Insights into the genomes of archaea mediating the anaerobic oxidation of methane. Environ. Microbiol. 7:1937-1951.[CrossRef][Medline]
  25. Michaelis, W., R. Seifert, K. Nauhaus, T. Treude, V. Thiel, M. Blumenberg, K. Knittel, A. Gieseke, K. Peterknecht, T. Pape, A. Boetius, R. Amann, B. B. Jörgensen, F. Widdel, J. Peckmann, N.V. Pimenov, and M. B. Gulin. 2002. Microbial reefs in the Black Sea fueled by anaerobic oxidation of methane. Science 297:1013-1015.[CrossRef][Medline]
  26. Nunes, L., D. E. Bignell, N. Lo, and P. Eggleton. 1997. On the respiratory quotient (RQ) of termites (Insecta: Isoptera). J. Insect Physiol. 43:749-758.[CrossRef][Medline]
  27. Odelson, D. A., and J. A. Breznak. 1983. Volatile fatty acid production by the hindgut microbiota of xylophagous termites. Appl. Environ. Microbiol. 45:1602-1613.[Abstract/Free Full Text]
  28. Ohkuma, M., and T. Kudo. 1998. Phylogenetic analysis of the symbiotic intestinal microflora of the termite Cryptotermes domesticus. FEMS Microbiol. Lett. 164:389-395.
  29. Ohkuma, M., K. Ohtoko, C. Grunau, S. Moriya, and T. Kudo. 1998. Phylogenetic identification of the symbiotic hypermastigote Trichonympha agilis in the hindgut of the termite Reticulitermes speratus based on small-subunit rRNA sequence. J. Eukaryot. Microbiol. 45:439-444.[Medline]
  30. Ohkuma, M., S. Noda, and T. Kudo. 1999. Phylogenetic relationships of symbiotic methanogens in diverse termites. FEMS Microbiol. Lett. 171:147-153.[CrossRef][Medline]
  31. Ohkuma, M., S. Noda, K. Horikoshi, and T. Kudo. 1995. Phylogeny of symbiotic methanogens in the gut of the termite Reticulitermes speratus. FEMS Microbiol. Lett. 134:45-50.[CrossRef][Medline]
  32. O'Neill, G. J., and J. F. Wilkinson. 1977. Oxidation of ammonia by methane oxidizing bacteria and the effects of ammonia on methane oxidation. J. Gen. Microbiol. 100:407-412.
  33. Pester, M., and A. Brune. 2006. Expression profiles of fhs (FTHFS) genes support the hypothesis that spirochaetes dominate reductive acetogenesis in the hindgut of lower termites. Environ. Microbiol. 8:1261-1270.[CrossRef][Medline]
  34. Pester, M., M. W. Friedrich, B. Schink, and A. Brune. 2004. pmoA-based analysis of methanotrophs in a littoral lake sediment reveals a diverse and stable community in a dynamic environment. Appl. Environ. Microbiol. 70:3138-3142.[Abstract/Free Full Text]
  35. Raghoebarsing, A. A., A. Pol, K. T. van de Pas-Schoonen, A. J. Smolders, K. F. Ettwig, W. I. Rijpstra, S. Schouten, J. S. Damste, H. J. Op den Camp, M. S. Jetten, and M. Strous. 2006. A microbial consortium couples anaerobic methane oxidation to denitrification. Nature 440:918-921.[CrossRef][Medline]
  36. Sanderson, M. G. 1996. Biomass of termites and their emissions of methane and carbon dioxide: a global database. Global Biogeochem. Cycles 10:543-557.
  37. Schmitt-Wagner, D., and A. Brune. 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.[Abstract/Free Full Text]
  38. Seedorf, H., A. Dreisbach, R. Hedderich, S. Shima, and R. K. Thauer. 2004. F420H2 oxidase (FprA) from Methanobrevibacter arboriphilus, a coenzyme F420-dependent enzyme involved in O2 detoxification. Arch. Microbiol. 182:126-137.[Medline]
  39. Shinzato, N., T. Matsumoto, I. Yamaoka, T. Oshima, and A. Yamagishi. 1999. 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.[Abstract/Free Full Text]
  40. Slaytor, M., and D. J. Chappell. 1994. Nitrogen metabolism in termites. Comp. Biochem. Physiol. 107:1-10.
  41. Sugimoto, A., D. E. Bignell, and J. A. MacDonald. 2000. Global impact of termites on the carbon cycle and atmospheric trace gases, p. 409-435. In T. Abe, D. E. Bignell, and M. Higashi, (ed.), Termites: evolution, sociality, symbioses, ecology. Kluwer Academic Publishers, Dordrecht, The Netherlands.
  42. Sugimoto, A., T. Inoue, I. Tayasu, L. Miller, S. Takeichi, and T. Abe. 1998. Methane and hydrogen production in a termite-symbiont system. Ecol. Res. 13:241-257.
  43. Tholen, A. 1999. Der Termitendarm als strukturiertes Ökosystem: Untersuchung der Mikrobiota und der Stoffflüsse im Darm von Reticulitermes flavipes und Cubitermes spp. Ph.D. thesis. University of Constance, Constance, Germany.
  44. Tholen, A., and A. Brune. 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.[Abstract/Free Full Text]
  45. Tholen, A., and A. Brune. 2000. Impact of oxygen on metabolic fluxes and in situ rates of reductive acetogenesis in the hindgut of the wood-feeding termite Reticulitermes flavipes. Environ. Microbiol. 2:436-449.[CrossRef][Medline]
  46. To, L. P., L. Margulis, D. Chase, and W. L. Nutting. 1980. The symbiotic microbial community of the Sonoran desert termite: Pterotermes occidentis. Biosystems 13:109-137.[CrossRef][Medline]
  47. Tokura, M., M. Ohkuma, and T. Kudo. 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.[CrossRef][Medline]
  48. Whittenbury, R., K. C. Phillips, and J. F. Wilkinson. 1970. Enrichment, isolation, and some properties of methane-utilizing bacteria. J. Gen. Microbiol. 61:205-218.[Medline]
  49. Williams, C. M., P. C. Veivers, M. Slaytor, and S. V. Cleland. 1994. Atmospheric carbon dioxide and acetogenesis in the termite Nasutitermes walkeri (Hill). Comp. Biochem. Physiol. 107:113-118.
  50. Yang, H., D. Schmitt-Wagner, U. Stingl, and A. Brune. 2005. Niche heterogeneity determines bacterial community structure in the termite gut (Reticulitermes santonensis). Environ. Microbiol. 7:916-932.[CrossRef][Medline]
  51. Yara, K., K. Jahana, and H. Hayashi. 1989. In situ morphology of the gut microbiota of the fungus-growing termite Odontotermes formosanus (Termitidae Macrotermitinae). Sociobiology 15:247-260.

Applied and Environmental Microbiology, March 2007, p. 2024-2028, Vol. 73, No. 6
0099-2240/07/$08.00+0     doi:10.1128/AEM.02190-06
Copyright © 2007, American Society for Microbiology. All Rights Reserved.




This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Other Versions of this Article:
AEM.02190-06v1
73/6/2024    most recent
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Pester, M.
Right arrow Articles by Brune, A.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Pester, M.
Right arrow Articles by Brune, A.
Agricola
Right arrow Articles by Pester, M.
Right arrow Articles by Brune, A.

Home Help [Feedback] [For Subscribers] [Archive] [Search] [Contents]
J. Bacteriol. Microbiol. Mol. Biol. Rev. Eukaryot. Cell All ASM Journals