High-resolution analysis of gut environment and bacterial microbiota reveals functional compartmentation of the gut in wood-feeding higher termites (Nasutitermes spp.)

Applied and Environmental Microbiology

Volumn 78, Issue 13, 2012, Pages 4691-4701

  Köhler, Tim ^a   Dietrich, Carsten ^a   Scheffrahn, Rudolf H ^b   Brune, Andreas ^a  

^a MAX PLANCK INSTITUTE FOR TERRESTRIAL MICROBIOLOGY   (Germany)

^b UNIVERSITY OF FLORIDA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

16S RRNA GENE; BACTERIAL COMMUNITY; BACTERIAL LINEAGES; CELLULASE ACTIVITY; COMPARTMENTATION; COMPREHENSIVE STUDIES; FERMENTATION PRODUCTS; HIGH PARTIAL PRESSURE; HIGH RESOLUTION; HIGH RESOLUTION ANALYSIS; INTESTINAL TRACT; MICROBIAL COMMUNITIES; MICROBIOTAS; MOLECULAR HYDROGEN; PHYSICOCHEMICAL CONDITIONS; PHYSICOCHEMICAL PARAMETERS; REDOX POTENTIALS;

ALKALINITY; CROPS; FEEDING; GENES; IMPORTANCE SAMPLING; REDOX REACTIONS; RNA;

BACTERIA;

BACTERIAL DNA; HYDROGEN; OXYGEN; RIBOSOME DNA; RNA 16S;

BACTERIUM; BIOCHEMICAL COMPOSITION; DIET; HYDROGEN; MICROBIAL ACTIVITY; MICROBIAL COMMUNITY; OXYGEN; PH; PHYSICOCHEMICAL PROPERTY; REDOX POTENTIAL; STOMACH CONTENT; TERMITE; WOOD;

ANIMAL; ARTICLE; BACTERIUM; BIODIVERSITY; CHEMISTRY; CLASSIFICATION; DIET; DNA SEQUENCE; GASTROINTESTINAL TRACT; GENETICS; ISOPTERA; METABOLISM; MICROBIOLOGY; OXIDATION REDUCTION REACTION; PH; WOOD;

ANIMALS; BACTERIA; BIODIVERSITY; DIET; DNA, BACTERIAL; DNA, RIBOSOMAL; GASTROINTESTINAL TRACT; HYDROGEN; HYDROGEN-ION CONCENTRATION; ISOPTERA; OXIDATION-REDUCTION; OXYGEN; RNA, RIBOSOMAL, 16S; SEQUENCE ANALYSIS, DNA; WOOD;

BACTERIA (MICROORGANISMS); FIBROBACTERES; ISOPTERA; NASUTITERMES; NASUTITERMES CORNIGER; PROKARYOTA; SPIROCHAETES; TERMITIDAE;

EID: 84864076952     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.00683-12     Document Type: Article

References (75)

1. Ballor NR, Leadbetter JR. 2012. Analysis of extensive [FeFe] hydrogenase gene diversity within the gut microbiota of insects representing five families of Dictyoptera. Microb. Ecol. 63:586-595.
2. 2-rich termite gut. Microb. Ecol. 63:282-294.
3. Baughn AD, Malamy MH. 2004. The strict anaerobe Bacteroides fragilis grows in and benefits from nanomolar concentrations of oxygen. Nature 427:441-444.
4. Bignell DE. 2011. Morphology, physiology, biochemistry and functional design of the termite gut: an evolutionary wonderland, p 375-412. In Bignell DE, Roisin Y, Lo N (ed), Biology of termites: a modern synthesis. Springer, Dordrecht, Netherlands.
5. Bignell DE, Eggleton P. 1995. On the elevated intestinal pH of higher termites (Isoptera: Termitidae). Insect Soc. 42:57-69.
6. Bosshard PP, Zbinden R, Altwegg M. 2002. Turicibacter sanguinis gen. nov., sp. nov., a novel anaerobic, Gram-positive bacterium. Int. J. Syst. Evol. Microbiol. 52:1263-1266.
7. Brauman A, Kane MD, Labat M, Breznak JA. 1992. Genesis of acetate and methane by gut bacteria of nutritionally diverse termites. Science 257:1384-1387.
8. Bray JR, Curtis JT. 1957. An ordination of the upland forest communities of southern Wisconsin. Ecol. Monogr. 27:325-349.
9. Brune A, Emerson D, Breznak JA. 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.
10. Brune A. 1998. Termite guts: the world's smallest bioreactors. Trends Biotechnol. 16:16-21.
11. Brune A. 2010. Methanogenesis in the digestive tracts of insects, p 707-728. In Timmis KN (ed), Handbook of hydrocarbon and lipid microbiology, vol 8. Springer, Heidelberg, Germany.
12. Brune A, Kühl M. 1996. pH profiles of the extremely alkaline hindguts of soil-feeding termites (Isoptera: Termitidae) determined with microelectrodes. J. Insect Physiol. 42:1121-1127.
13. Brune A, Ohkuma M. 2011. Role of the termite gut microbiota in symbiotic digestion, p 439-475. In Bignell DE, Roisin Y, LoN(ed), Biology of termites: a modern synthesis. Springer, Dordrecht, Netherlands.
14. Chao A. 1984. Nonparametric estimation of the number of classes in a population. Scand. J. Stat. 11:265-270.
15. Chao A, Shen TJ. 2003. Nonparametric estimation of Shannon's index of diversity when there are unseen species in sample. Environ. Ecol. Stat. 10:429-443.
16. Cotta M, Forster R. 2006. The family Lachnospiraceae, including the genera Butyrivibrio, Lachnospira and Roseburia, p 1002-1021. In Dworkin M, Falkow S, Rosenberg E, Schleifer K-H, Stackebrandt E (ed), The prokaryotes, 3rd ed, vol 4. Springer, New York, NY.
17. Czolij R, Slaytor M, O'Brien RW. 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.
18. Ebert A, Brune A. 1997. Hydrogen concentration profiles at the oxicanoxic interface: a microsensor study of the hindgut of the wood-feeding lower termite Reticulitermes flavipes (Kollar). Appl. Environ. Microbiol. 63:4039-4046.
19. 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. Microbiol. 69:6659-6668.
20. Engelbrektson A, et al. 2010. Experimental factors affecting PCR-based estimates of microbial species richness and evenness. Environ. Microbiol. 4:642-647.
21. Friedrich MW, Schmitt-Wagner D, Lueders T, Brune A. 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.
22. Fröhlich J, et al. 1999. Isolation of Desulfovibrio intestinalis sp. nov. from the hindgut of the lower termite Mastotermes darwiniensis. Can. J. Microbiol. 45:145-152.
23. Fujita A, Abe T. 2002. Amino acid concentration and distribution of lysozyme and protease activities in the guts of higher termites. Physiol. Entomol. 27:76-78.
24. Graber JR, Leadbetter JR, Breznak JA. 2004. Description of Treponema azotonutricium sp. nov. and Treponema primitia sp. nov., the first spirochetes isolated from termite guts. Appl. Environ. Microbiol. 70:1315-1320.
25. Henckel T, Friedrich M, Conrad R. 1999. Molecular analyses of the methane-oxidizing microbial community in rice field soil by targeting the genes of the 16S rRNA, particulate methane monooxygenase, and methanol dehydrogenase. Appl. Environ. Microbiol. 65:1980-1990.
26. Hongoh Y, et al. 2006. Phylogenetic diversity, localization and cell morphologies of the candidate phylum TG3 and a subphylum in the phylum Fibrobacteres, recently found bacterial groups dominant in termite guts. Appl. Environ. Microbiol. 72:6780-6788.
27. Hongoh Y, et al. 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.
28. Huang Y, et al. 2005. Sanguibacter marinus sp. nov., isolated from coastal sediment. Int. J. Syst. Evol. Microbiol. 55:1755-1758.
29. Hugenholtz P, Goebel BM. 2001. The polymerase chain reaction as a tool to investigate microbial diversity in environmental samples, p 31-41. In Rochelle PA (ed), Environmental molecular microbiology: protocols and applications. Horizon Press Inc., New York, NY.
30. Jouquet P, Traoré S, Choosai C, Hartmann C, Bignell D. 2011. Influence of termites on ecosystem functioning. Ecosystem services provided by termites. Eur. J. Soil Biol. 47:215-222.
31. Kuhnigk T, Branke J, Krekeler D, Cypionka H, König H. 1996. A feasible role of sulfate-reducing bacteria in the termite gut. Syst. Appl. Microbiol. 19:139-149.
32. 2 by spirochetes from termite guts. Science 283:686-689.
33. Leaphart AB, Lovell CR. 2001. Recovery and analysis of formyltetrahydrofolate synthetase gene sequences from natural populations of acetogenic bacteria. Appl. Environ. Microbiol. 67:1392-1395.
34. Legendre P, Legendre L. 1998. Numerical ecology, 2nd ed. Elsevier, Amsterdam, Netherlands.
35. Leschine S, Paster B, Canale-Parola E. 2006. Free-living saccharolytic spirochetes: the genus Spirochaeta, p 195-210. In Dworkin M, Falkow S, Rosenberg E, Schleifer K-H, Stackebrandt E (ed) The prokaryotes, 3rd ed, vol 7. Springer, New York, NY.
36. Ley RE, et al. 2008. Evolution of mammals and their gut microbes. Science 320:1647-1651.
37. Liesack W, Bak F, Kreft JU, Stackebrandt E. 1994. Holophaga foetida gen. nov., sp. nov., a new, homoacetogenic bacterium degrading methoxylated aromatic compounds. Arch. Microbiol. 162:85-90.
38. Lo N, Bandi C, Watanabe H, Nalepa C, Beninati T. 2003. Evidence for co-cladogenesis between diverse dictyopteran lineages and their intracellular endosymbionts. Mol. Biol. Evol. 20:907-913.
39. Ludwig W, et al. 2004. ARB: a software environment for sequence data. Nucleic Acids Res. 32:1363-1371.
40. Muyzer G, de Waal EC, Uitterlinden AG. 1993. Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl. Environ. Microbiol. 59:695-700.
41. Nakajima H, Hongoh Y, Usamib R, Kudo T, Ohkuma M. 2005. Spatial distribution of bacterial phylotypes in the gut of the termite Reticulitermes speratus and the bacterial community colonizing the gut epithelium. FEMS Microbiol. Ecol. 54:247-255.
42. Nakajima H, et al. 2006. Phylogenetic and morphological diversity of Bacteroidales members associated with the gut wall of termites. Biosci. Biotechnol. Biochem. 70:211-218.
43. Noda S, et al. 2006. Identification and characterization of ectosymbionts of distinct lineages in Bacteroidales attached to flagellated protists in the gut of termites and a wood-feeding cockroach. Environ. Microbiol. 8:11-20.
44. Noirot C. 2001. The gut of termites (Isoptera). Comparative anatomy, systematics, phylogeny. II. Higher termites (Termitidae). Ann. Soc. Entomol. Fr. (N.S.) 37:431-471.
45. Ohkuma M, Brune A. 2011. Diversity, structure, and evolution of the termite gut microbial community, p 413-438. In Bignell DE, Roisin Y, Lo N (ed), Biology of termites: a modern synthesis. Springer, Dordrecht, Netherlands.
46. Ohkuma M, Iida T, Kudo T. 1999. Phylogenetic relationships of symbiotic spirochetes in the gut of diverse termites. FEMS Microbiol. Lett. 181: 123-129.
47. Ottesen EA, Leadbetter JR. 2011. Formyltetrahydrofolate synthetase gene diversity in the guts of higher termites with different diets and lifestyles. Appl. Environ. Microbiol. 77:3461-3467.
48. Paster BJ, et al. 1996. Phylogeny of not-yet-cultured spirochetes from termite guts. Appl. Environ. Microbiol. 62:347-352.
49. Pernthaler A, Pernthaler J, Amann R. 2004. Sensitive multi-color fluorescence in situ hybridization for the identification of environmental microorganisms, p 711-726. In Kowalchuk GA, de Brujin FJ, Head IM, Akkermans ADL, van Elsas JD (ed), Molecular microbial ecology manual, 2nd ed, vol 1. Kluwer Academic Publishers, Dordrecht, Netherlands.
50. Pernthaler J, Glöckner FO, Schönhuber W, Amann R. 2001. Fluorescence in situ hybridization with rRNA-targeted oligonucleotide probes, p 207-226. In Paul J (ed), Methods in microbiology: marine microbiology, vol 30. Academic Press, London, United Kingdom.
51. Pester M, Brune A. 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.
52. Pester M, Brune A. 2007. Hydrogen is the central free intermediate during lignocellulose degradation by termite gut symbionts. ISME J. 1:551-565.
53. Pruesse E, et al. 2007. SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res. 35:7188-7196.
54. 2-using acetogenic bacterium from the rumen: description of Ruminococcus schinkii sp. nov. FEMS Microbiol. Lett. 140:281-286.
55. 2-reductive acetogenesis in cultivated spirochetes and the gut community of the termite Zootermopsis angusticollis. Microbiology 149:2529-2537.
56. Scheffrahn RH, Cabrera BJ, Kern WH, Jr, Su N-Y. 2002. Nasutitermes costalis (Isoptera: Termitidae) in Florida: first record of a non-endemic establishment by a higher termite. Florida Entomol. 85:273-275.
57. Scheffrahn RH, Krecek J, Szalanski AL, Austin JW. 2005. Synonymy of the neotropical arboreal termites Nasutitermes corniger and N. costalis (Isoptera: Termitidae: Nasutitermitinae), with evidence from morphology, genetics, and biogeography. Ann. Entomol. Soc. Am. 98:273-281.
58. Schloss PD, Gevers D, Westcott SL. 2011. Reducing the effects of PCR amplification and sequencing artifacts on 16S rRNA-based studies. PLoS One 6:e27310. doi:10.1371/journal.pone.0027310.
59. Schloss PD, et al. 2009. Introducing mothur: open-source, platformindependent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 75:7537-7541.
60. Schmitt-Wagner D, Brune A. 1999. Hydrogen profiles and localization of methanogenic activities in the highly compartmentalized hindgut of soilfeeding higher termites (Cubitermes spp.). Appl. Environ. Microbiol. 65: 4490-4496.
61. Schmitt-Wagner D, Friedrich MW, Wagner B, Brune A. 2003. Phylogenetic diversity, abundance, and axial distribution of bacteria in the intestinal tract of two soil-feeding termites (Cubitermes spp.). Appl. Environ. Microbiol. 69:6007-6017.
62. Schmitt-Wagner D, Friedrich MW, Wagner B, Brune A. 2003. Axial dynamics, stability, and interspecies similarity of bacterial community structure in the highly compartmentalized gut of soil-feeding termites (Cubitermes spp.). Appl. Environ. Microbiol. 69:6018-6024.
63. Sogin ML, et al. 2006. Microbial diversity in the deep sea and the underexplored "rare biosphere." Proc. Natl. Acad. Sci. U. S. A. 103:12115-12120.
64. Suen G, et al. 2011. The complete genome sequence of Fibrobacter succinogenes S85 reveals a cellulolytic and metabolic specialist. PLoS One 6:e18814. doi:10.1371/journal.pone.0018814.
65. Sugimoto A, et al. 1998. Methane and hydrogen production in a termitesymbiont system. Ecol. Res. 13:241-257.
66. Tholen A, Brune A. 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.
67. Tholen A, Pester M, Brune A. 2007. Simultaneous methanogenesis and oxygen reduction by Methanobrevibacter cuticularis at low oxygen fluxes. FEMS Microbiol. Ecol. 62:303-312.
68. Thongaram T, et al. 2005. Comparison of bacterial communities in the alkaline gut segment among various species of higher termites. Extremophiles 9:229-238.
69. Tokuda G, et al. 2012. Cellulolytic environment in the midgut of the wood-feeding higher termite Nasutitermes takasagoensis. J. Insect Physiol. 58:147-154.
70. Tokuda G, Watanabe H. 2007. Hidden cellulases in termites: revision of an old hypothesis. Biol. Lett. 3:336-339.
71. Tokuda G, Yamaoka I, Noda H. 2000. Localization of symbiotic clostridia in the mixed segment of the termite Nasutitermes takasagoensis (Shiraki). Appl. Environ. Microbiol. 66:2199-2207.
72. Wang Q, Garrity GM, Tiedje JM, Cole JR. 2007. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl. Environ. Microbiol. 73:5261-5267.
73. Warnecke F, et al. 2007. Metagenomic and functional analysis of hindgut microbiota of a wood-feeding higher termite. Nature 450:560-565.
74. Watanabe H, Tokuda G. 2010. Cellulolytic systems in insects. Annu. Rev. Entomol. 55:609-632.
75. Werner JJ, et al. 2012. Impact of training sets on classification of highthroughput bacterial 16S rRNA gene surveys. ISME J. 6:94-103.