The Gut Microbiota of Termites: Digesting the Diversity in the Light of Ecology and Evolution

Annual Review of Microbiology

Volumn 69, Issue 1, 2015, Pages 145-166

  Brune, Andreas ^a   Dietrich, Carsten ^a  

^a MAX PLANCK INSTITUTE FOR TERRESTRIAL MICROBIOLOGY   (Germany)

Author keywords

Coevolution; Cospeciation; Insects; Lignocellulose; Symbionts

Indexed keywords

HYDROGEN; NITROGEN; OXYGEN; POLYMER;

ARCHAEON; BACTERIUM; BACTEROIDETES; COEVOLUTION; COMMUNITY STRUCTURE; ENVIRONMENTAL FACTOR; FLAGELLATE; HABITAT SELECTION; INTESTINE; INTESTINE FLORA; ISOPTERA; LACHNOSPIRACEAE; MICROBIAL COMMUNITY; MICROBIAL DEGRADATION; MICROBIAL DIVERSITY; MICROBIAL METABOLISM; MICROHABITAT; MOLECULAR ECOLOGY; MOLECULAR EVOLUTION; NITROGEN METABOLISM; NONHUMAN; OXYGEN CONSUMPTION; PRIORITY JOURNAL; REVIEW; RUMINOCOCCACEAE; SPECIES DIFFERENTIATION; SPECIES HABITAT; SPIROCHETE; SYMBIOSIS; ANIMAL; CLASSIFICATION; EUKARYOTE; MICROBIOLOGY; PHYSIOLOGY;

ANIMALS; ARCHAEA; BACTERIA; EUKARYOTA; GASTROINTESTINAL MICROBIOME; ISOPTERA; SYMBIOSIS;

EID: 84944148857     PISSN: 00664227     EISSN: 15453251     Source Type: Book Series    
DOI: 10.1146/annurev-micro-092412-155715     Document Type: Review

References (130)

1. Ballor NR, Leadbetter JR. 2012. Patterns of [FeFe] hydrogenase diversity in the gut communities of lignocellulose-feeding higher termites. Appl. Environ. Microbiol. 78: 5368-74
2. Bauer E, Lampert N, Mikaelyan A, Köhler T, Maekawa K, Brune A. 2015. Physicochemical conditions, metabolites, and community structure of the bacterial microbiota in the gut of wood-feeding cockroaches (Blaberidae: Panesthiinae). FEMS Microbiol. Ecol. 91. doi: 10. 1093/femsec/fiu028
3. Bertino-Grimaldi D, Medeiros MN, Vieira RP, Cardoso AM, Turque AS, et al. 2013. Bacterial community composition shifts in the gut of Periplaneta americana fed on different lignocellulosic materials. SpringerPlus 2: 609
4. BignellDE, Eggleton P. 2000. Termites in ecosystems. In Termites: Evolution, Sociality, Symbioses, Ecology, Vol. 1, ed. T Abe, DE Bignell, M Higashi, pp. 363-87. Dordrecht, Neth.: Kluwer Acad.
5. Bignell DE, Oskarsson H, Anderson JM. 1980. Distribution and abundance of bacteria in the gut of a soil-feeding termite Procubitermes aburiensis (Termitidae, Termitinae). J. Gen. Microbiol. 117: 393-403
6. Bignell DE, Oskarsson H, Anderson JM, Ineson P. 1983. Structure, microbial associations and function of the so-called "mixed segment" of the gut in two soil-feeding termites, Procubitermes aburiensis and Cubitermes severus (Termitidae, Termitinae). J. Zool. Lond. 201: 445-480
7. Boucias DG, Cai Y, Sun Y, Lietze VU, Sen R, et al. 2013. The hindgut lumen prokaryotic microbiota of the termite Reticulitermes flavipes and its responses to dietary lignocellulose composition. Mol. Ecol. 22: 1836-53
8. Bourguignon T, Lo N, Cameron SL, Sobotnk J, Hayashi Y, Shigenobu S, et al. 2015. The evolutionary history of termites as inferred from 66 mitochondrial genomes. Mol. Biol. Evol. 32: 406-21
9. Breznak JA, Leadbetter JR. 2006. Termite gut spirochetes. In The Prokaryotes, Vol. 7: Proteobacteria: Delta and Epsilon Subclasses. Deeply Rooting Bacteria, ed. M Dworkin, S Falkow, E Rosenberg, K-H Schleifer, E Stackebrandt, pp. 318-29. New York: Springer. 3rd ed.
10. Breznak JA, Pankratz HS. 1977. In situ morphology of the gut microbiota of wood-eating termites [Reticulitermes flavipes (Kollar) and Coptotermes formosanus Shiraki]. Appl. Environ. Microbiol. 33: 406-26
11. Brune A. 1998. Termite guts: The world's smallest bioreactors. Trends Biotechnol. 16: 16-21
12. Brune A. 2006. Symbiotic associations between termites and prokaryotes. In The Prokaryotes, Vol. 1: Symbiotic Associations, Biotechnology, Applied Microbiology, ed. M Dworkin, S Falkow, E Rosenberg, K-H Schleifer, E Stackebrandt, pp. 439-74. New York: Springer. 3rd ed.
13. Brune A. 2010. Methanogens in the digestive tract of termites. In (Endo)symbiotic Methanogenic Archaea, ed. JHP Hackstein, pp. 81-100. Heidelberg, Ger.: Springer
14. Brune A. 2012. Endomicrobia: intracellular symbionts of termite gut flagellates. J. Endocytobiosis Cell Res. 23: 11-15
15. Brune A. 2014. Symbiotic digestion of lignocellulose in termite guts. Nat. Rev. Microbiol. 12: 168-80
16. Brune A, Ohkuma M. 2011. Role of the termite gut microbiota in symbiotic digestion. In Biology of Termites: A Modern Synthesis, ed. DE Bignell, Y Roisin, N Lo, pp. 439-75. Dordrecht, Neth.: Springer
17. Chapman RF, Simpson SJ, Douglas AE. 2013. The Insects: Structure and Function. Cambridge, UK: Cambridge Univ. Press. 5th ed.
18. Colman DR, Toolson EC, Takacs-Vesbach CD. 2012. Do diet and taxonomy influence insect gut bacterial communities? Mol. Ecol. 21: 5124-37
19. Czolij R, SlaytorM, O'BrienRW. 1985. Bacterial flora of themixed segment and the hindgut of the higher termite Nasutitermes exitiosus Hill (Termitidae, Nasutitermitinae). Appl. Environ. Microbiol. 49: 1226-36
20. Desai MS, Brune A. 2012. Bacteroidales ectosymbionts of gut flagellates shape the nitrogen-fixing community in dry-wood termites. ISME J. 6: 1302-13
21. Desai MS, Strassert JFH, Meuser K, Hertel H, Ikeda-Ohtsubo W, et al. 2010. Strict cospeciation of devescovinid flagellates and Bacteroidales ectosymbionts in the gut of dry-wood termites (Kalotermitidae). Environ. Microbiol. 12: 2120-32
22. Dietrich C, Köhler T, Brune A. 2014. The cockroach origin of the termite gut microbiota: Patterns in bacterial community structure reflect major evolutionary events. Appl. Environ. Microbiol. 80: 2261-69
23. Do TH, Nguyen TT, Nguyen TN, Le QG, Nguyen C, et al. 2014. Mining biomass-degrading genes through Illumina-based de novo sequencing and metagenomic analysis of free-living bacteria in the gut of the lower termite Coptotermes gestroi harvested in Vietnam. J. Biosci. Bioeng. 118: 665-71
24. Douglas AE. 2014. The molecular basis of bacterial-insect symbiosis. J. Mol. Biol. 426: 3830-37
25. Douglas AE. 2015. Multiorganismal insects: diversity and function of resident microorganisms. Annu. Rev. Entomol. 60: 17-34
26. Dröge S, Rachel R, Radek R, König H. 2008. Treponema isoptericolens sp. Nov. , a novel spirochaete from the hindgut of the termite Incisitermes tabogae. Int. J. Syst. Evol. Microbiol. 58: 1079-83
27. Eggleton P. 2011. An introduction to termites: biology, taxonomy and functionalmorphology. In Biology of Termites: A Modern Synthesis, ed. DE Bignell, Y Roisin, N Lo, pp. 1-26. Dordrecht, Neth.: Springer
28. Engel P, Moran NA. 2013. The gut microbiota of insects-diversity in structure and function. FEMS Microbiol. Rev. 37: 699-735
29. FriedrichMW, 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: 4880-90
30. Fujita A. 2004. Lysozymes in insects: What role do they play in nitrogen metabolism? Physiol. Entomol. 299: 305-10
31. Gile GH, Carpenter KJ, James ER, Scheffrahn RH, Keeling PJ. 2013. Morphology and molecular phylogeny of Staurojoenina mulleri sp. Nov. (Trichonymphida, Parabasalia) from the hindgut of the kalotermitid Neotermes jouteli. J. Eukaryot. Microbiol. 60: 203-13
32. Gile GH, James ER, Scheffrahn RH, Carpenter KJ, Harper JT, Keeling PJ. 2011. Molecular and morphological analysis of the Calonymphidae with a description of Calonympha chia sp. Nov. , Snyderella kirbyi sp. Nov. , Snyderella swezyae sp. Nov. , and Snyderella yamini sp. Nov. Int. J. Syst. Evol. Microbiol. 61: 2547-58
33. Grieco MAB, Cavalcante JJV, Cardoso AM, Vieira RP, Machado EA, et al. 2013. Microbial community diversity in the gut of the South American termite Cornitermes cumulans (Isoptera: Termitidae). Microb. Ecol. 65: 197-204
34. Hamilton C, Bulmer MS. 2012. Molecular antifungal defenses in subterranean termites: RNA interference reveals in vivo roles of termicins and GNBPs against a naturally encountered pathogen. Dev. Comp. Immunol. 36: 372-77
35. He S, Ivanova N, Kirton E, AllgaierM, Bergin C, et al. 2013. Comparative metagenomic and metatranscriptomic analysis of hindgut paunch microbiota in wood-and dung-feeding higher termites. PLOS ONE 8: e61126
36. Hongoh Y. 2010. Diversity and genomes of uncultured microbial symbionts in the termite gut. Biosci. Biotechnol. Biochem. 74: 1145-51
37. Hongoh Y. 2011. Toward the functional analysis of uncultivable, symbiotic microorganisms in the termite gut. Cell. Mol. Life Sci. 68: 1311-25
38. Hongoh Y, Deevong P, Hattori S, Inoue T, Noda S, 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: 6780-88
39. Hongoh Y, Deevong P, Inoue T, Moriya S, Trakulnaleamsai, 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: 6590-99
40. Hongoh Y, Ohkuma M. 2010. Termite gut flagellates and their methanogenic and eubacterial symbionts. In (Endo)symbiotic Methanogenic Archaea, ed. JHP Hackstein, pp. 55-79. Heidelberg, Ger.: Springer
41. Hongoh Y, Sato T, Dolan M, Noda S, Ui S, et al. 2007. The motility symbiont of the termite gut flagellate Caduceia versatilis is a member of the "Synergistes" group. Appl. Environ. Microbiol. 73: 6270-76
42. Hongoh Y, SharmaVK, PrakashT, Noda S, Taylor TD, et al. 2009. Complete genome of the uncultured Termite Group 1 bacteria in a single host protist cell. PNAS 105: 5555-60
43. Hongoh Y, Sharma VK, Prakash T, Noda S, Toh H, et al. 2008. Genome of an endosymbiont coupling N2 fixation to cellulolysis within protist cells in termite gut. Science 322: 1108-9
44. HuangXF, BakkerMG, JuddTM, Reardon KF, Vivanco JM. 2013. Variations in diversity and richness of gut bacterial communities of termites (Reticulitermes flavipes) fed with grassy and woody plant substrates. Microb. Ecol. 65: 531-36
45. Ikeda-Ohtsubo W, Brune A. 2009. Cospeciation of termite gut flagellates and their bacterial endosymbionts: Trichonympha species and 'Candidatus Endomicrobium trichonymphae. ' Mol. Ecol. 18: 332-42
46. Ikeda-Ohtsubo W, Faivre N, Brune A. 2010. Putatively free-living 'Endomicrobia'-ancestors of the intracellular symbionts of termite gut flagellates? Environ. Microbiol. Rep. 2: 554-59
47. Inoue J, Noda S, Hongoh Y, Ui S, Ohkuma M. 2008. Identification of endosymbiotic methanogen and ectosymbiotic spirochetes of gut protists of the termite Coptotermes formosanus. Microb. Environ. 23: 94-97
48. Inoue JI, Oshim K, Suda W, Sakamoto M, Iino T, et al. 2015. Distribution and evolution of nitrogen fixation genes in the phylum Bacteroidetes. Microb. Environ. 30: 44-50
49. Isanapong J, Sealy-HambrightW, Willis AG, Boonmee A, Callister SJ, et al. 2013. Development of an ecophysiological model for Diplosphaera colotermitum TAV2, a termite hindgut verrucomicrobium. ISME J. 7: 1-11
50. James ER, OkamotoN, Burki F, Scheffrahn RH, Keeling PJ. 2013. Cthulhumacrofasciculumque n. g. , n. Sp. And Cthylla microfasciculumque n. g. , n. Sp. , a newly identified lineage of parabasalian termite symbionts. PLOS ONE 8: e58509
51. James ER, Tai V, Scheffrahn RH, Keeling PJ. 2013. Trichonympha burlesquei from Reticulitermes virginicus and evidence against a cosmopolitan distribution of Trichonympha agilis in many termite hosts. Int. J. Syst. Evol. Microbiol. 63: 3873-76
52. Kitade O. 2004. Comparison of symbiotic flagellate faunae between termites and a wood-feeding cockroach of the genus Cryptocercus. Microb. Environ. 19: 215-220
53. Klass KD, Nalepa C, Lo N. 2008. Wood-feeding cockroaches as models for termite evolution (Insecta: Dictyoptera): Cryptocercus versus Parasphaeria boleiriana. Mol. Phylogenet. Evol. 46: 809-17
54. Köhler T, Dietrich C, Scheffrahn RH, 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: 4691-701
55. Köhler T, Stingl U, Meuser K, Brune A. 2008. Novel lineages of Planctomycetes densely colonize the alkaline gut of soil-feeding termites (Cubitermes spp.). Environ. Microbiol. 10: 1260-70
56. Lang K, Schuldes J, Klingl A, Poehlein A, Daniel R, Brune A. 2015. New mode of energy metabolism in the seventh order of methanogens as indicated by comparative genome analysis of "Candidatus Methanoplasma termitum. " Appl. Environ. Microbiol. 81: 1338-52
57. Lemaitre B, Miguel-Aliaga I. 2013. The digestive tract of Drosophila melanogaster. Annu. Rev. Genet. 47: 377-404
58. Ley RE, Hamady M, Lozupone C, Turnbaugh PJ, Ramey RR, et al. 2008. Evolution of mammals and their gut microbes. Science 5883: 1647-51
59. Li H, Sun J, Zhao J, Deng T, Lu J, et al. 2012. Physiochemical conditions and metal ion profiles in the gut of the fungus-growing termite Odontotermes formosanus. J. Insect Physiol. 58: 1368-75
60. Liu N, Zhang L, Zhou H, ZhangM, Yan X, et al. 2013. Metagenomic insights into metabolic capacities of the gut microbiota in a fungus-cultivating termite (Odontotermes yunnanensis). PLOS ONE 8: e69184
61. Lo N, Eggleton P. 2011. Termite phylogenetics and co-cladogenesis with symbionts. In Biology of Termites: A Modern Synthesis, ed. DE Bignell, Y Roisin, N Lo, pp. 27-50. Dordrecht, Neth.: Springer
62. Lucey KS, Leadbetter JR. 2014. Catechol 2, 3-dioxygenase and other meta-cleavage catabolic pathway genes in the 'anaerobic' termite gut spirochete Treponema primitia. Mol. Ecol. 23: 1531-43
63. MakondeHM, Boga HI, Osiemo Z, Mwirichia R, Mackenzie LM, et al. 2013. 16S-rRNA-based analysis of bacterial diversity in the gut of fungus-cultivating termites (Microtermes and Odontotermes species). Antonie Leeuwenhoek 104: 869-83
64. Matson EG, Gora KG, Leadbetter JR. 2011. Anaerobic carbon monoxide dehydrogenase diversity in the homoacetogenic hindgut microbial communities of lower termites and the wood roach. PLOS ONE 6: e19316
65. Mikaelyan A, Strassert JFH, Tokuda G, Brune A. 2014. The fiber-associated cellulolytic bacterial community in the hindgut of wood-feeding higher termites (Nasutitermes spp.). Environ. Microbiol. 16: 2711-22
66. Miyata R, Noda N, Tamaki H, Kinjyo K, Aoyagi H, et al. 2007. Influence of feed components on symbiotic bacterial community structure in the gut of the wood-feeding higher termite Nasutitermes takasagoensis. Biosci. Biotechnol. Biochem. 71: 1244-51
67. Miyata R, Noda N, Tamaki H, Kinjyo K, Aoyagi H, et al. 2007. Phylogenetic relationship of symbiotic archaea in the gut of the higher termite Nasutitermes takasagoensis fed with various carbon sources. Microb. Environ. 22: 157-64
68. Nakajima H, Hongoh Y, Noda S, Yoshida Y, Usami R, et al. 2006. Phylogenetic and morphological diversity of Bacteroidales members associated with the gut wall of termites. Biosci. Biotechnol. Biochem. 70: 211-18
69. Nalepa CA. 2011. Altricial development in wood-feeding cockroaches: The key antecedent of termite eusociality. In Biology of Termites: A Modern Synthesis, ed. DE Bignell, Y Roisin, N Lo, pp. 69-95. Dordrecht, Neth.: Springer
70. Nalepa CA. 2015. Origin of termite eusociality: Trophallaxis integrates the social, nutritional, and microbial environments. Ecol. Entomol. 40: 323-35
71. Ngugi DK, Brune A. 2012. Nitrate reduction, nitrous oxide formation, and anaerobic ammonia oxidation to nitrite in the gut of soil-feeding termites (Cubitermes and Ophiotermes spp.). Environ. Microbiol. 14: 860-71
72. Ni J, Tokuda G. 2013. Lignocellulose-degrading enzymes from termites and their symbiotic microbiota. Biotechnol. Adv. 31: 838-50
73. Nobre T, Rouland-Lef èvre C, Aanen DK. 2011. Comparative biology of fungus cultivation in termites and ants. In Biology of Termites: A Modern Synthesis, ed. DE Bignell, Y Roisin, N Lo, pp. 193-210. Dordrecht, Neth.: Springer
74. Noda S, Hongoh Y, Sato T, Ohkuma M. 2009. Complex coevolutionary history of symbiotic Bacteroidales bacteria of various protists in the gut of termites. BMC Evol. Biol. 9: 158
75. Noda S, Inoue T, Hongoh Y, Nalepa CA, VongkaluangC, 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
76. Noda S, Kitade O, Inoue T, Kawai M, Kanuka M, et al. 2007. Cospeciation in the triplex symbiosis of termite gut protists (Pseudotrichonympha spp.), their hosts, and their bacterial endosymbionts. Mol. Ecol. 16: 1257-66
77. Noda S, Mantini C, Meloni D, Inoue J-I, Kitade O, et al. 2012. Molecular phylogeny and evolution of parabasalia with improved taxon sampling and new protein markers of actin and elongation factor-1. PLOS ONE 7: e29938
78. Noirot C. 1995. The gut of termites (Isoptera). Comparative anatomy, systematics, phylogeny. I. Lower termites. Ann. Soc. Entomol. Fr. 31: 197-226
79. Noirot C. 2001. The gut of termites (Isoptera). Comparative anatomy, systematics, phylogeny. II. Higher termites (Termitidae). Ann. Soc. Entomol. Fr. 37: 431-71
80. Ochman H, WorobeyM, Kuo CH, Ndjango JBN, PeetersM, et al. 2010. Evolutionary relationships of wild hominids recapitulated by gut microbial communities. PLOS Biol. 8: e1000546
81. Ohkuma M, Brune A. 2011. Diversity, structure, and evolution of the termite gut microbial community. In Biology of Termites: AModern Synthesis, ed. DE Bignell, Y Roisin, NLo, pp. 413-38. Dordrecht, Neth.: Springer
82. Ohkuma M, Noda S, Hattori S, Iida T, Yuki M, et al. 2015. Acetogenesis from H2 plus CO2 and nitrogen fixation by an endosymbiotic spirochete of a termite-gut cellulolytic protist. PNAS. In press. doi: 10. 1073/pnas. 1423979112
83. Otani S, Mikaelyan A, Nobre T, Hansen LH, Koné NA, et al. 2014. Identifying the core microbial community in the gut of fungus-growing termites. Mol. Ecol. 23(18): 4631-44
84. Ottesen EA, Leadbetter JR. 2011. Formyltetrahydrofolate synthetase gene diversity in the guts of higher termites with different diets and lifestyles. Appl. Environ. Microbiol. 77: 3461-67
85. 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. Microbiol. 78: 8245-53
86. Pérez-Cobas AE, Maiques E, Angelova A, Carrasco P, Moya A, Latorre A. 2015. Diet shapes the gut microbiota of the omnivorous cockroach Blatella germanica. FEMS Microbiol. Ecol. 91. doi: 10. 1093/ femsec/fiv022
87. Pester M, Brune A. 2007. Hydrogen is the central free intermediate during lignocellulose degradation by termite gut symbionts. ISME J. 1: 551-65
88. PoulsenM. 2015. Towards an integrated understanding of the consequences of fungus domestication on the fungus-growing termite gut microbiota. Environ. Microbiol. In press. doi: 10. 1111/1462-2920. 12765
89. Poulsen M, Hu H, Li C, Chen Z, Xu L, et al. 2014. Complementary symbiont contributions to plant decomposition in a fungus-farming termite. PNAS 111: 14500-5
90. Pramono AK, Sakamoto M, Iino T, Hongoh Y, Ohkuma M. 2015. Dysgonomonas termitidis sp. Nov. , isolated from the gut of the subterranean termite Reticulitermes speratus. Int. J. Syst. Evol. Microbiol. 65: 681-685
91. Radek R, Strassert JFH, Krüger J, Meuser K, Scheffrahn RH, Brune A. 2014. Phylogeny and ultrastructure of Oxymonas jouteli, a rostellum-free species, and Opisthomitus longiflagellatus sp. Nov. , oxymonadid flagellates from the gut of Neotermes jouteli. Protist 165: 384-99
92. Rahman NA, Parks DH, Willner DL, Engelbrektson AL, Goffredi SK, et al. 2015. A molecular survey of Australian and North American termite genera indicates that vertical inheritance is the primary force shaping termite gut microbiomes. Microbiome 3: 5
93. Rawls JF, Mahowald MA, Ley RE, Gordon JI. 2006. Reciprocal gut microbiota transplants from zebrafish and mice to germ-free recipients reveal host habitat selection. Cell 127: 423-33
94. Raychoudhury R, Sen R, Cai Y, Sun Y, Lietze V-U, et al. 2013. Comparative metatranscriptomic signatures ofwood and paper feeding in the gut of the termite Reticulitermes flavipes (Isoptera: Rhinotermitidae). Insect Mol. Biol. 22: 155-71
95. Reid NM, Addison SL, West MA, Lloyd-Jones G. 2014. The bacterial microbiota of Stolotermes ruficeps (Stolotermitidae), a phylogenetically basal termite endemic toNew Zealand. FEMS Microbiol. Ecol. 90: 678-88
96. Rosengaus RB, Schultheis KF, Yalonetskaya A, Bulmer MS, du CombW, et al. 2014. Symbiont-derived-1, 3-glucanases in a social insect: mutualism beyond nutrition. Front. Microbiol. 5: 607
97. Rosenthal AZ, Matson EG, Eldar A, Leadbetter JR. 2011. RNA-seq reveals cooperative metabolic interactions between two termite-gut spirochete species in co-culture. ISME J. 5: 1133-42
98. Rosenthal AZ, Zhang X, Lucey KS, Ottesen EA, Trivedi V, et al. 2013. Localizing transcripts to single cells suggests an important role of uncultured deltaproteobacteria in the termite gut hydrogen economy. PNAS 110: 16163-68
99. Sabree ZL, Huang CY, Arakawa G, Tokuda G, Lo N, et al. 2012. Genome shrinkage and loss of nutrient-providing potential in the obligate symbiont of the primitive termite Mastotermes darwiniensis. Appl. Environ. Microbiol. 78: 204-10
100. Sabree ZL, Moran NA. 2014. Host-specific assemblages typify gut microbial communities of related insect species. SpringerPlus 3: 138
101. Sakamoto M, Ohkuma, M. 2013. Bacteroides reticulotermitis sp. Nov. , isolated from the gut of the subterranean termite (Reticulitermes speratus). Int. J. Syst. Evol. Microbiol. 63: 691-695
102. Sato T, Hongoh Y, Noda S, Hattori S, Ui S, Ohkuma M. 2009. Candidatus Desulfovibrio trichonymphae, a novel intracellular symbiont of the flagellate Trichonympha agilis in termite gut. Environ. Microbiol. 11: 1007-15
103. Sato T, Kuwahara H, Fujita K, Noda S, Kihara K, et al. 2014. Intranuclear verrucomicrobial symbionts and evidence of lateral gene transfer to the host protist in the termite gut. ISME J. 8: 1008-19
104. Schauer C, Thompson CL, Brune A. 2012. The bacterial community in the gut of the cockroach Shelfordella lateralis reflects the close evolutionary relatedness of cockroaches and termites. Appl. Environ. Microbiol. 78: 2758-67
105. Schauer C, Thompson CL, Brune A. 2014. Pyrotag sequencing of the gut microbiota of the cockroach Shelfordella lateralis reveals a highly dynamic core but only limited effects of diet on community structure. PLOS ONE 9: e85861
106. 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: 6007-17
107. Seedorf H, Griffin NW, Ridaura VK, Reyes A, Cheng J, et al. 2014. Bacteria from diverse habitats colonize and compete in the mouse gut. Cell 159: 254-66
108. Strassert JFH, Köhler T, Wienemann THG, Ikeda-Ohtsubo W, Faivre N, et al. 2012. 'Candidatus Ancillula trichonymphae', a novel lineage of endosymbiotic Actinobacteria in termite gut flagellates of the genus Trichonympha. Environ. Microbiol. 14: 3259-70
109. Tai V, Gile GH, Pan J, James ER, Carpenter KJ, et al. 2014. The phylogenetic position of Kofoidia loriculata (Parabasalia) and its implications for the evolution of the Cristamonadea. J. Eukaryot. Microbiol. 62: 255-59
110. Tai V, James ER, Nalepa CA, Scheffrahn RH, Perlman SJ, Keeling PJ. 2015. The role of host phylogeny varies in shaping microbial diversity in the hindguts of lower termites. Appl. Environ. Microbiol. 81: 1059-70
111. Tai V, James ER, Perlman SJ, Keeling PJ. 2013. Single-cell DNA barcoding using sequences from the small subunit rRNA and internal transcribed spacer region identifies new species of Trichonympha and Trichomitopsis from the hindgut of the termite Zootermopsis angusticollis. PLOS ONE 8: e58728
112. Tamschick S, RadekR. 2013. Colonization of termite hindgut walls by oxymonad flagellates and prokaryotes in Incisitermes tabogae, I. marginipennis and Reticulitermes flavipes. Eur. J. Protistol. 49: 1-14
113. Tanaka H, Aoyagi H, Shina S, Dodo Y, Yoshimura T, et al. 2006. Influence of the diet components on the symbiotic microorganisms community in hindgut of Coptotermes formosanus Shiraki. Appl. Microbiol. Biotechnol. 71: 907-17
114. Thompson CL, Vier R, Mikaelyan A, Wienemann T, Brune A. 2012. 'Candidatus Arthromitus' revised: Segmented filamentous bacteria in arthropod guts are members of Lachnospiraceae. Environ. Microbiol. 14: 1454-65
115. Thongaram T, Hongoh Y, Kosono S, Ohkuma M, Trakulnaleamsai S, et al. 2005. Comparison of bacterial communities in the alkaline gut segment among various species of higher termites. Extremophiles 9: 229-38
116. Tokuda G, Nakamura T, Murakami R, Yamaoka I. 2001. Morphology of the digestive system in the wood-feeding termite Nasutitermes takasagoensis (Shiraki) [Isoptera: Termitidae]. Zool. Sci. 18: 869-77
117. Tokuda G, Tsuboi Y, Kihara K, Saitou S, Moriya S, et al. 2014. Metabolomic profiling of 13C-labelled cellulose digestion in a lower termite: insights into gut symbiont function. Proc. R. Soc. B 281: 20140990
118. Ulyshen MD. 2014. Wood decomposition as influenced by invertebrates. Biol. Rev. In press. doi: 10. 1111/brv. 12158
119. Warnecke F, Luginbühl P, Ivanova N, Ghassemian M, Richardson TH, et al. 2007. Metagenomic and functional analysis of hindgut microbiota of a wood-feeding higher termite. Nature 450: 560-65
120. Watanabe H, Tokuda G. 2010. Cellulolytic systems in insects. Annu. Rev. Entomol. 55: 609-32
121. Wenzel M, Radek R, Brugerolle G, König H. 2003. Identification of the ectosymbiotic bacteria of Mixotricha paradoxa involved in movement symbiosis. Eur. J. Protistol. 39: 11-24
122. Wertz JT, Breznak JA. 2007. Physiological ecology of Stenoxybacter acetivorans, an obligate microaerophile in termite guts. Appl. Environ. Microbiol. 73: 6829-41
123. Wertz JT, Kim E, Breznak JA, Schmidt TM, Rodrigues JLM. 2012. Genomic and physiological characterization of the Verrucomicrobia isolate Diplosphaera colotermitum gen. Nov. , sp. Nov. reveals microaerophily and nitrogen fixation genes. Appl. Environ. Microbiol. 78: 1544-55
124. Yamada A, Inoue T, Noda Y, Hongoh H, Ohkuma M. 2007. Evolutionary trend of phylogenetic diversity of nitrogen fixation genes in the gut community of wood-feeding termites. Mol. Ecol. 16: 3768-77
125. Yang YJ, Zhang N, Ji SQ, Lan X, Zhang KD, et al. 2014. Dysgonomonas macrotermitis sp. Nov. , isolated from the hindgut of a fungus-growing termite. Int. J. Syst. Evol. Microbiol. 64: 2956-2961
126. Yun J-H, Roh SW, Whon TW, Jung M-J, Kim M-S, et al. 2014. Insects gut bacterial diversity determined by host environmental habitat, diet, developmental stage and phylogeny. Appl. Environ. Microbiol. 80: 5254-64
127. Zhang M, Liu N, Qian C, Wang Q, Wang Q, et al. 2014. Phylogenetic and functional analysis of gut microbiota of a fungus-growing higher termite: Bacteroidetes from higher termites are a rich source of-glucosidase genes. Microb. Ecol. 68: 416-25
128. Zhang X, Leadbetter JR. 2012. Evidence for cascades of perturbation and adaptation in the metabolic genes of higher termite gut symbionts. mBio 3: e00223-12
129. Zheng H, Bodington D, Zhang C, Miyanaga K, Tanji Y, et al. 2013. Comprehensive phylogenetic diversity of [FeFe]-hydrogenase genes in termite gut microbiota. Microb. Environ. 28: 491-94
130. Zheng H, Dietrich C, Thompson CL, Meuser K, Brune A. 2015. Population structure of Endomicrobia in single host cells of termite gut flagellates (Trichonympha spp.). Microb. Environ. 30: 92-98