Omic research in termites: An overview and a roadmap

Frontiers in Genetics

Volumn 6, Issue MAR, 2015, Pages

  Scharf, Michael E ^a  

^a PURDUE UNIVERSITY   (United States)

Author keywords

Digestome; DNA methylation; Holobiome; Metabolomics; Sociobiology; Socioevolution; Sociogenomics; Symbiosis

Indexed keywords

ISOPTERA;

EID: 84923652223     PISSN: None     EISSN: 16648021     Source Type: Journal    
DOI: 10.3389/fgene.2015.00076     Document Type: Review

References (107)

1. Bastien, G., Arnal, G., Bozonnet, S., Laguerre, S., Ferreira, F., Fauré, R.,et al. (2013). Mining for hemicellulases in the fungus-growing termite Pseudacanthotermes militaris using functional metagenomics. Biotechnol. Biofuels. 6:78. doi: 10.1186/1754-6834-6-78
2. Bauwens, J., Millet, C., Tarayre, C., Brasseur, C., Destain, J., Vandenbol, M.,et al. (2013). Symbiont diversity in Reticulitermes santonensis: investigation strategy through proteomics. Environ. Entomol. 42, 882-887. doi: 10.1603/EN13112
3. Boucias, D. G., Cai, Y., Sun, Y., Lietze, V. U., Sen, R., Raychoudhury, R.,et al. (2013). The hindgut lumen prokaryotic microbiota of the termite Reticulitermes flavipes and its responses to dietary lignocellulose composition. Mol. Ecol. 22, 1836-1853. doi: 10.1111/mec.12230
4. Brune, A. (2014). Symbiotic digestion of lignocellulose in termite guts. Nat. Rev. Microbiol. 12, 168-180. doi: 10.1038/nrmicro3182
5. Burnum, K. E., Callister, S. J., Nicora, C. D., Purvine, S. O., Hugenholtz, P., Warnecke, F.,et al. (2011). Proteome insights into the symbiotic relationship between a captive colony of Nasutitermes corniger and its hindgut microbiome. ISME J. 5, 161-164. doi: 10.1038/ismej.2010.97
6. Chouvenc, T., Efstathion, C. A., Elliott, M. L., and Su, N. Y. (2013). Extended disease resistance emerging from the faecal nest of a subterranean termite. Proc. Biol. Sci. 280:20131885. doi: 10.1098/rspb.2013.1885
7. Cornette, R., Koshikawa, S., Hojo, M., Matsumoto, T., and Miura T. (2006). Caste-specific cytochrome P450 in the damp-wood termite Hodotermopsis sjostedti. Insect Mol. Biol. 15, 235-244. doi: 10.1111/j.1365-2583.2006.00632.x
8. Cornette, R., Hayashi, Y., Koshikawa, S., and Miura, T. (2013). Differential gene expression in response to juvenile hormone analog treatment in the damp-wood termite Hodotermopsis sjostedti. J. Insect Physiol. 59, 509-518. doi: 10.1016/j.jinsphys.2013.02.002
9. Do, T. H., Nguyen, T. T., Nguyen, T. N., Le, Q. G., Nguyen, C., Kimura, K.,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. 6, 665-671. doi: 10.1016/j.jbiosc.2014.05.010
10. Engelbrektson, A., Kunin, V., Wrighton, K. C., Zvenigorodsky, N., Chen, F., Ochman, H., et al. (2010). Experimental factors affecting PCR-based estimates of microbial species richness and evenness. ISME J. 4, 642-647. doi: 10.1038/ismej.2009.153
11. Fall, S., Hamelin, J., Ndiaye, F., Assigbetse, K., Aragno, M., Chotte, J. L.,et al. (2007). Differences between bacterial communities in the gut of a soil-feeding termite (Cubitermes niokoloensis) and its mounds. Appl. Environ. Microbiol. 73, 5199-5208. doi: 10.1128/AEM.02616-06
12. Fisher, M., Miller, D., Brewster, C., Husseneder, C., and Dickerman, A. (2007). Diversity of gut bacteria of Reticulitermes flavipes as examined by 16S rRNA gene sequencing and amplified rDNA restriction analysis. Curr. Microbiol. 55, 254-259. doi: 10.1007/s00284-007-0136-8
13. Gao, Q., Tancredi, S. E., and Thompson, G. J. (2012). Identification of mycosis-related genes in the eastern subterranean termite by suppression subtractive hybridization. Arch. Insect Biochem. Physiol. 80, 63-76. doi: 10.1002/arch.21026
14. Geib, S. M., Filley, T. R., Hatcher, P. G., Hoover, K., Carlson, J. E., Jimenez-Gasco Mdel, M.,et al. (2008). Lignin degradation in wood-feeding insects. Proc. Natl. Acad. Sci. U.S.A. 105, 12932-12937. doi: 10.1073/pnas.0805257105
15. Glastad, K. M., Hunt, B. G., and Goodisman, M. A. D. (2013). Evidence of a conserved functional role for DNA methylation in termites. Insect Mol. Biol. 22, 143-154. doi: 10.1111/imb.12010
16. Grieco, M. A., Cavalcante, J. J., Cardoso, A. M., Vieira, R. P., Machado, E. A., Clementino, M. M.,et al. (2013). Microbial community diversity in the gut of the South American termite Cornitermes cumulans. Microb. Ecol. 65, 197-204. doi: 10.1007/s00248-012-0119-6
17. Harmon-Smith, M., Celia, L., Chertkov, O., Lapidus, A., Copeland, A., Glavina Del Rio, T.,et al. (2010). Complete genome sequence of Sebaldella termitidis type strain (NCTC 11300). Stand. Genomic Sci. 2, 220-227. doi: 10.4056/sigs.811799
18. Hayashi, Y., Shigenobu, S., Watanabe, D., Toga, K., Saiki, R., Shimada, K.,et al. (2013). Construction and characterization of normalized cDNA libraries by 454 pyrosequencing and estimation of DNA methylation levels in three distantly related termite species. PLoS ONE 8:e76678. doi: 10.1371/journal.pone.0076678
19. He, S., Ivanova, N., Kirton, E., Allgaier, M., Bergin, C., Scheffrahn, R. H.,et al. (2013). Comparative metagenomic and metatranscriptomic analysis of hindgut paunch microbiota in wood- and dung-feeding higher termites. PLoS ONE 8:e61126. doi: 10.1371/journal.pone.0061126
20. Hojo, M., Maekawa, K., Saitoh, S., Shigenobu, S., Miura, T., Hayashi, Y.,et al. (2012). Exploration and characterization of genes involved in the synthesis of diterpene defence secretion in nasute termite soldiers. Insect Mol. Biol. 21, 545-557. doi: 10.1111/j.1365-2583.2012.01162.x
21. Honey Bee Genome Sequencing Consortium. (2006). Insights into social insects from the genome of the honeybee Apis mellifera. Nature 443, 931-949. doi: 10.1038/nature05260
22. Hongoh, Y., Ohkuma, M., and Kudo, T. (2003). Molecular analysis of bacterial microbiota in the gut of the termite Reticulitermes speratus. FEMS Microbiol. Ecol. 44, 231-242. doi: 10.1016/S0168-6496(03)00026-6
23. Hongoh, Y., Sharma, V. K., Prakash, T., Noda, S., Toh, H., Taylor, T. D.,et al. (2008a). Genome of an endosymbiont coupling N2 fixation to cellulolysis within protist cells in termite gut. Science 322, 1108-1109. doi: 10.1126/science.1165578
24. Hongoh, Y., Sharma, V. K., Prakash, T., Noda, S., Taylor, T. D., Kudo, T.,et al. (2008b). Complete genome of the uncultured Termite Group 1 bacteria in a single host protist cell. Proc. Natl. Acad. Sci. U.S.A. 105, 5555-5560. doi: 10.1073/pnas.0801389105
25. Huang, Q., Sun, P., Zhou, X., and Lei, C. (2012). Characterization of head transcriptome and analysis of gene expression involved in caste differentiation and aggression in Odontotermes formosanus. PLoS ONE 7:e50383. doi: 10.1371/journal.pone.0050383
26. Hussain, A., Li, Y. F., Cheng, Y., Liu, Y., Chen, C. C., and Wen, S. Y. (2013). Immune-related transcriptome of Coptotermes formosanus Shiraki workers: the defense mechanism. PLoS ONE 8:e69543. doi: 10.1371/journal.pone.0069543
27. Husseneder, C., Ho, H. Y., and Blackwell, M. (2010a). Comparison of the bacterial symbiont composition of the Formosan subterranean termite from its native and introduced range. Open Microbiol. J. 4, 53-66. doi: 10.2174/1874285801004010053
28. Husseneder, C., Simms, D. M., Aluko, G. K., and Delatte, J. (2010b). Colony breeding system influences cuticular bacterial load of Formosan subterranean termite workers. Environ. Entomol. 39, 1715-1723. doi: 10.1603/EN09238
29. Husseneder, C., McGregor, C., Lang, R. P., Collier, R., and Delatte, J. (2012). Transcriptome profiling of female alates and egg-laying queens of the Formosan subterranean termite. Comp. Biochem. Physiol. D. 7, 14-27.
30. Husseneder, C., and Simms, D. M. (2014). Effects of caste on the expression of genes associated with septic injury and xenobiotic exposure in the Formosan subterranean termite. PLoS ONE 9:e105582. doi: 10.1371/journal.pone.0105582
31. Isanapong, J., Goodwin, L., Bruce, D., Chen, A., Detter, C., Han, J.,et al. (2012). High-quality draft genome sequence of the Opitutaceae bacterium strain TAV1, a symbiont of the wood-feeding termite Reticulitermes flavipes. J. Bacteriol. 194, 2744-2745. doi: 10.1128/JB.00264-12
32. Ishikawa, Y., Okada, Y., Ishikawa, A., Miyakawa, H., Koshikawa, S., and Miura, T. (2010). Gene expression changes during caste-specific neuronal development in the damp-wood termite Hodotermopsis sjostedti. BMC Genomics 11:314. doi: 10.1186/1471-2164-11-314
33. James, E. R., Tai, V., Scheffrahn, R. H., and Keeling, P. J. (2013). Trichonympha burlesquei n. sp. from Reticulitermes virginicus and evidence against a cosmopolitan distribution of Trichonympha agilis in many termite hosts. Int. J. Syst. Evol. Microbiol. 63, 3873-3876. doi: 10.1099/ijs.0.054874-0
34. Johjima, T., Taprab, Y., Noparatnaraporn, N., Kudo, T., and Ohkuma, M. (2006). Large-scale identification of transcripts expressed in a symbiotic fungus (Termitomyces) during plant biomass degradation. Appl. Microbiol. Biotechnol. 73, 195-203. doi: 10.1007/s00253-006-0570-8
35. Ke, J., Laskar, D. D., and Chen, S. (2013). Tetramethylammonium hydroxide (TMAH) thermochemolysis for probing in situ softwood lignin modification in each gut segment of the termite. J. Agric. Food Chem. 61, 1299-1308. doi: 10.1021/jf3048548
36. Ke, J., Laskar, D. D., Singh, D., and Chen, S. (2011). In situ lignocellulosic unlocking mechanism for carbohydrate hydrolysis in termites: crucial lignin modification. Biotechnol. Biofuels 4:17. doi: 10.1186/1754-6834-4-17
37. Köhler, T., Dietrich, C., Scheffrahn, R. H., and 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. doi: 10.1128/AEM.00683-12
38. König, H., Li, L., and Fröhlich, J. (2013). The cellulolytic system of the termite gut. Appl. Microbiol. Biotechnol. 97, 7943-7962. doi: 10.1007/s00253-013-5119-z
39. Koshikawa, S., Cornette, R., Hojo, M., Maekawa, K., Matsumoto, T., and Miura, T. (2005). Screening of genes expressed in developing mandibles during soldier differentiation in the termite Hodotermopsis sjostedti. FEBS Lett. 579, 1365-1370. doi: 10.1016/j.febslet.2005.01.031
40. Koshikawa, S., Miyazaki, S., Cornette, R., Matsumoto, T., and Miura, T. (2008). Genome size of termites (Insecta, Dictyoptera, Isoptera) and wood roaches (Insecta, Dictyoptera, Cryptocercidae). Naturwissenschaften 95, 859-867. doi: 10.1007/s00114-008-0395-7
41. Leonardo, F. C., da Cunha, A. F., da Silva, M. J., Carazzolle, M. F., Costa-Leonardo, A. M., Costa, F. F.,et al. (2011). Analysis of the workers head transcriptome of the Asian subterranean termite, Coptotermes gestroi. Bull. Entomol. Res. 101, 383-391. doi: 10.1017/S0007485310000556
42. Lilburn, T. G., Schmidt, T. M., and Breznak, J. A. (1999). Phylogenetic diversity of termite gut spirochaetes. Environ. Microbiol. 1, 331-345. doi: 10.1046/j.1462-2920.1999.00043.x
43. Liu, N., Yan, X., Zhang, M., Xie, L., Wang, Q., Huang, Y.,et al. (2011). Microbiome of fungus-growing termites: a new reservoir for lignocellulase genes. Appl. Environ. Microbiol. 77, 48-56. doi: 10.1128/AEM.01521-10
44. Liu, N., Zhang, L., Zhou, H., Zhang, M., Yan, X., Wang, Q.,et al. (2013). Metagenomic insights into metabolic capacities of the gut microbiota in a fungus-cultivating termite (Odontotermes yunnanensis). PLoS ONE 8:e69184. doi: 10.1371/journal.pone.0069184
45. Lo, N., Li, B., and Ujvari, B. (2012). DNA methylation in the termite Coptotermes lacteus. Insect Soc. 59, 257-261. doi: 10.1007/s00040-011-0213-7
46. Makonde, H. M., Boga, H. I., Osiemo, Z., Mwirichia, R., Mackenzie, L. M., Göker, M.,et al. (2013). 16S-rRNA-based analysis of bacterial diversity in the gut of fungus-cultivating termites (Microtermes and Odontotermes species). Antonie Van Leeuwenhoek 104, 869-883. doi: 10.1007/s10482-013-0001-7
47. Mattéotti, C., Bauwens, J., Brasseur, C., Tarayre, C., Thonart, P., Destain, J.,et al. (2012). Identification and characterization of a new xylanase from Gram-positive bacteria isolated from termite gut (Reticulitermes santonensis). Protein Expr. Purif. 83, 117-127. doi: 10.1016/j.pep.2012.03.009
48. Mattéotti, C., Haubruge, E., Thonart, P., Francis, F., De Pauw, E., Portetelle, D.,et al. (2011a). Characterization of a new ß-glucosidase/ß-xylosidase from the gut microbiota of the termite (Reticulitermes santonensis). FEMS Microbiol. Lett. 314, 147-157. doi: 10.1111/j.1574-6968.2010.02161.x
49. Mattéotti, C., Thonart, P., Francis, F., Haubruge, E., Destain, J., Brasseur, C.,et al. (2011b). New glucosidase activities identified by functional screening of a genomic DNA library from the gut microbiota of the termite Reticulitermes santonensis. Microbiol. Res. 166, 629-642. doi: 10.1016/j.micres.2011.01.001
50. Miura, T., Kamikouchi, A., Sawata, M., Takeuchi, H., Natori, S., Kubo, T.,et al. (1999). Soldier caste-specific gene expression in the mandibular glands of Hodotermopsis japonica. Proc. Natl. Acad. Sci. U.S.A. 96, 13874-13879. doi: 10.1073/pnas.96.24.13874
51. Miura, T., and Scharf, M. E. (2011). "Molecular mechanisms underlying caste differentiation in termites," in Biology of Termites: A Modern Synthesis, eds D. E. Bigness, Y. Roisin, and N. Lo (Dordrecht: Springer), 211-253.
52. Miyata, R., Noda, N., Tamaki, H., Kinjyo, K., Aoyagi, H., Uchiyama, 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, 1244-1251. doi: 10.1271/bbb.60672
53. Nelson, C. M., Ihle, K. E., Fondrk, M. K., Page, R. E., and Amdam, G. V. (2007). The gene vitellogenin has multiple coordinating effects on social organization. PLoS Biol. 5:e62. doi: 10.1371/journal.pbio.0050062
54. Nelson, L. J., Cool, L. G., Forschler, B. T., and Haverty, M. I. (2001). Correspondence of soldier defense secretion mixtures with cuticular hydrocarbon phenotypes for chemotaxonomy of the termite genus Reticulitermes in North America. J. Chem. Ecol. 27, 1449-1479. doi: 10.1023/A:1010325511844
55. Ni, J., and Tokuda, G. (2013). Lignocellulose-degrading enzymes from termites and their symbiotic microbiota. Biotechnol. Adv. 31, 838-850. doi: 10.1016/j.biotechadv.2013.04.005
56. Nimchua, T., Thongaram, T., Uengwetwanit, T., Pongpattanakitshote, S., and Eurwilaichitr, L. (2012). Metagenomic analysis of novel lignocellulose-degrading enzymes from higher termite guts inhabiting microbes. J. Microbiol. Biotechnol. 22, 462-469. doi: 10.4014/jmb.1108.08037
57. Otani, S., Mikaelyan, A., Nobre, T., Hansen, L. H., Koné, N. A., Sørensen, S. J.,et al. (2014). Identifying the core microbial community in the gut of fungus-growing termites. Mol. Ecol. 23, 4631-4644. doi: 10.1111/mec.12874
58. Poulsen, M., Hu, H., Li, C., Chen, Z., Xu, L., Otani, S.,et al. (2014). Complementary symbiont contributions to plant decomposition in a fungus-farming termite. Proc. Natl. Acad. Sci. U.S.A. 111, 14500-14505. doi: 10.1073/pnas.1319718111
59. Prestwich, G. D. (1984). Defense mechanisms of termites. Ann. Rev. Entomol. 29, 201-232. doi: 10.1146/annurev.en.29.010184.001221
60. Rashamuse, K., Mabizela-Mokoena, N., Sanyika, T. W., Mabvakure, B., and Brady D. (2012). Accessing carboxylesterase diversity from termite hindgut symbionts through metagenomics. J. Mol. Microbiol. Biotechnol. 22, 277-286. doi: 10.1159/000342447
61. Rashamuse, K., Ronneburg, T., Sanyika, W., Mathiba, K., Mmutlane, E., and Brady, D. (2014). Metagenomic mining of feruloyl esterases from termite enteric flora. Appl. Microbiol. Biotechnol. 98, 727-737. doi: 10.1007/s00253-013-4909-7
62. Raychoudhury, R., Sen, R., Cai, Y., Sun, Y., Lietze, V. U., Boucias, D. G.,et al. (2013). Comparative metatranscriptomic signatures of wood and paper feeding in the gut of the termite Reticulitermes flavipes. Insect Mol. Biol. 22, 155-171. doi: 10.1111/imb.12011
63. Robinson, G. E., Grozinger, C. M., and Whitfield, C. W. (2005). Sociogenomics: social life in molecular terms. Nat. Rev. Genet. 6, 257-270. doi: 10.1038/nrg1575
64. Roose-Amsaleg, C., Brygoo, Y., and Harry, M. (2004). Ascomycete diversity in soil-feeding termite nests and soils from a tropical rainforest. Environ. Microbiol. 6, 462-469. doi: 10.1111/j.1462-2920.2004.00579.x
65. Rosengaus, R. B., Schultheis, K. F., Yalonetskaya, A., Bulmer, M. S., DuComb, W. S., Benson, R. W.,et al. (2014). Symbiont-derived ß-1,3-glucanases in a social insect: mutualism beyond nutrition. Front. Microbiol. 5:607. doi: 10.3389/fmicb.2014.00607
66. Rosengaus, R. B., Zecher, C. N., Schultheis, K. F., Brucker, R. M., and Bordenstein, S. R. (2011). Disruption of the termite gut microbiota and its prolonged consequences for fitness. Appl. Environ. Microbiol. 77, 4303-4312. doi: 10.1128/AEM.01886-10
67. Rosenthal, A. Z., Matson, E. G., Eldar, A., and Leadbetter, J. R. (2011). RNA-seq reveals cooperative metabolic interactions between two termite-gut spirochete species in co-culture. ISME J. 5, 1133-1142. doi: 10.1038/ismej.2011.3
68. Sabree, Z. L., Huang, C. Y., Arakawa, G., Tokuda, G., Lo, N., Watanabe, H.,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, 204-210. doi: 10.1128/AEM.06540-11
69. Sanyika, T. W., Rashamuse, K. J., Hennesy, F., and Brady, D. (2012). Luminal hindgut bacterial diversities of the grass and sugarcane feeding termite Trinervitermes trinervoides. African J. Microbiol. Res. 6, 2639-2648.
70. Scharf, M. E. (2015). Termites as targets and models for biotechnology. Ann. Rev. Entomol. 60, 77-102. doi: 10.1146/annurev-ento-010814-020902
71. Scharf, M. E., Karl, Z. J., Sethi, A., and Boucias, D. G. (2011). Multiple levels of synergistic collaboration in termite lignocellulose digestion. PLoS ONE 6:e21709. doi: 10.1371/journal.pone.0021709
72. Scharf, M. E., Scharf, W. D., Pittendrigh, B. R., and Bennett, G. W. (2003). Caste- and development-associated gene expression in a lower termite. Genome Biol. 4:R62. doi: 10.1186/gb-2003-4-10-r62
73. Scharf, M. E., and Tartar, A. (2008). Termite digestomes as sources for novel lignocellulases. Biofuels Bioprod. Bioref. 2, 540-552. doi: 10.1002/bbb.107
74. Scharf, M. E., Wu-Scharf, D., Zhou, X., Pittendrigh, B. R., and Bennett, G. W. (2005). Gene expression profiles among immature and adult reproductive castes of the termite Reticulitermes flavipes. Insect Mol. Biol. 14, 31-44. doi: 10.1111/j.1365-2583.2004.00527.x
75. Schauer, C., Thompson, C., and 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. doi: 10.1371/journal.pone.0085861
76. Sen, R., Raychoudhury, R., Cai, Y., Sun, Y., Lietze, V. U., Boucias, D. G.,et al. (2013). Differential impacts of juvenile hormone, soldier head extract and alternate caste phenotypes on host and symbiont transcriptome composition in the gut of the termite Reticulitermes flavipes. BMC Genomics 14:491. doi: 10.1186/1471-2164-14-491
77. Sen, R., Raychoudhury, R., Cai, Y., Sun, Y., Lietze, V. U., Boucias, D. G.,et al. (2015). Metatranscriptomic signatures of nicotinoid-pathogen synergy in the termite gut. PLoS ONE (in press).
78. Sethi, A., Slack, J. M., Kovaleva, E. S., Buchman, G. W., and Scharf, M. E. (2013a). Lignin-associated metagene expression in a lignocellulose-digesting termite. Insect Biochem. Mol. Biol. 43, 91-101. doi: 10.1016/j.ibmb.2012.10.001
79. Sethi, A., Kovaleva, E. S., Slack, J. M., Brown, S., Buchman, G. W., and Scharf, M. E. (2013b). A GHF7 cellulase from the protist symbiont community of Reticulitermes flavipes enables more efficient lignocellulose processing by host enzymes. Arch. Insect Biochem. Physiol. 84, 175-193. doi: 10.1002/arch.21135
80. Sillam-Dussès, D., Krasulová, J., Vrkoslav, V., Pytelková, J., Cvacka, J., Kutalová, K.,et al. (2012). Comparative study of the labial gland secretion in termites. PLoS ONE 7:e46431. doi: 10.1371/journal.pone.0046431
81. Steller, M. M., Kambhampati, S., and Caragea, D. (2010). Comparative analysis of expressed sequence tags from three castes and two life stages of the termite Reticulitermes flavipes. BMC Genomics 11:463. doi: 10.1186/1471-2164-11-463
82. Stingl, U., Radek, R., Yang, H., and Brune, A. (2005). "Endomicrobia": cytoplasmic symbionts of termite gut protozoa form a separate phylum of prokaryotes. Appl. Environ. Microbiol. 71, 1473-1479. doi: 10.1128/AEM.71.3.1473-1479.2005
83. Tai, V., James, E. R., Nalepa, C. A., Scheffrahn, R. H., Perlman, S. J., and Keeling, P. J. (2015). The role of host phylogeny varies in shaping microbial diversity in the hindguts of lower termites. Appl. Environ. Microbiol. 81, 1059-1070. doi: 10.1128/AEM.02945-14
84. Tai, V., James, E. R., Perlman, S. J., and Keeling, P. J. (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. doi: 10.1371/journal.pone.0058728
85. Tai, V., and Keeling, P. J. (2013). Termite hindguts and the ecology of microbial communities in the sequencing age. J. Eukaryot. Microbiol. 60, 421-428. doi: 10.1111/jeu.12048
86. Tartar, A., Wheeler, M. M., Zhou, X., Coy, M. R., Boucias, D. G., and Scharf, M. E. (2009). Parallel metatranscriptome analyses of host and symbiont gene expression in the gut of the termite R. flavipes. Biotechnol. Biofuels 2:25. doi: 10.1186/1754-6834-2-25
87. Tarver, M. R., Zhou, X., and Scharf, M. E. (2010). Socio-environmental and endocrine influences on developmental and caste-regulatory gene expression in the eusocial termite Reticulitermes flavipes. BMC Mol. Biol. 11:28. doi: 10.1186/1471-2199-11-28
88. Terrapon, N., Li, C., Robertson, H. M., Ji, L., Meng, X., Booth, W.,et al. (2014). Molecular traces of alternative social organization in a termite genome. Nat. Commun. 5:3636. doi: 10.1038/ncomms4636
89. Thompson, G. J., Crozier, Y. C., and Crozier, R. H. (2003). Isolation and characterization of a termite transferrin gene up-regulated on infection. Insect Mol. Biol. 12, 1-7. doi: 10.1046/j.1365-2583.2003.00381.x
90. Todaka, N., Inoue, T., Saita, K., Ohkuma, M., Nalepa, C. A., Lenz, M.,et al. (2010). Phylogenetic analysis of cellulolytic enzyme genes from representative lineages of termites and a related cockroach. PLoS ONE 5:e8636. doi: 10.1371/journal.pone.0008636
91. Todaka, N., Moriya, S., Saita, K., Hondo, T., Kiuchi, I., Takasu, H.,et al. (2007). Environmental cDNA analysis of the genes involved in lignocellulose digestion in the symbiotic protist community of Reticulitermes speratus. FEMS Microbiol. Ecol. 59, 592-599. doi: 10.1111/j.1574-6941.2006.00237.x
92. Tokuda, G., Tsuboi, Y., Kihara, K., Saitou, S., Moriya, S., Lo, N.,et al. (2014). Metabolomic profiling of 13C-labelled cellulose digestion in a lower termite: insights into gut symbiont function. Proc. Biol. Sci. 281, 1789. doi: 10.1098/rspb.2014.0990
93. Vargo, E. L., and Husseneder, C. (2009). Biology of subterranean termites: insights from molecular studies of Reticulitermes, and Coptotermes. Annu. Rev. Entomol. 54, 379-403. doi: 10.1146/annurev.ento.54.110807.090443
94. Wang, Q., Qian, C., Zhang, X. Z., Liu, N., Yan, X., and Zhou, Z. (2012). Characterization of a novel thermostable ß-glucosidase from a metagenomic library of termite gut. Enzyme Microb. Technol. 51, 319-324. doi: 10.1016/j.enzmictec.2012.07.015
95. Wang, Y., and Qian, P. Y. (2009). Conservative fragments in bacterial 16S rRNA genes and primer design for 16S ribosomal DNA amplicons in metagenomic studies. PLoS ONE 4:e7401. doi: 10.1371/journal.pone.0007401
96. Warnecke, F., Luginbühl, P., Ivanova, N., Ghassemian, M., Richardson, T. H., Stege, J. T.,et al. (2007). Metagenomic and functional analysis of hindgut microbiota of a wood-feeding higher termite. Nature 450, 560-565. doi: 10.1038/nature06269
97. Watanabe, H., Noda, H., Tokuda, G., and Lo, N. (1998). A cellulase gene of termite origin. Nature 394, 330-331. doi: 10.1038/28527
98. Watanabe, H., and Tokuda, G. (2010). Cellulolytic systems in insects. Annu. Rev. Entomol. 55, 609-632. doi: 10.1146/annurev-ento-112408-085319
99. Weil, T., Korb, J., and Rehli, M. (2009). Comparison of queen-specific gene expression in related lower termite species. Mol. Biol. Evol. 26, 1841-1850. doi: 10.1093/molbev/msp095
100. Weil, T., Rehli, M., and Korb, J. (2007). Molecular basis for the reproductive division of labour in a lower termite. BMC Genomics 8:198. doi: 10.1186/1471-2164-8-198
101. West-Eberhard, M. J. (2003). Developmental Plasticity and Evolution. Oxford: Oxford University Press.
102. Wu-Scharf, D., Scharf, M. E., Pittendrigh, B. R., and Bennett, G. W. (2003). Expressed sequence tags from a polyphenic Reticulitermes flavipes cDNA library. Sociobiology 41, 479-490.
103. Xie, L., Zhang, L., Zhong, Y., Liu, N., Long, Y., Wang, S.,et al. (2012). Profiling the metatranscriptome of the protistan community in Coptotermes formosanus with emphasis on the lignocellulolytic system. Genomics 99, 246-255. doi: 10.1016/j.ygeno.2012.01.009
104. Yang, H., Schmitt-Wagner, D., Stingl, U., and Brune, A. (2005). Niche heterogeneity determines bacterial community structure in the termite gut (Reticulitermes santonensis). Environ. Microbiol. 7, 916-932. doi: 10.1111/j.1462-2920.2005.00760.x
105. Yang, F., Xu, B., Li, J., and Huang, Z. (2012). Transcriptome analysis of Termitomyces albuminosus reveals the biodegradation of lignocellulose. Wei Sheng Wu Xue Bao 52, 466-477.
106. Yuki, M., Moriya, S., Inoue, T., and Kudo, T. (2008). Transcriptome analysis of the digestive organs of Hodotermopsis sjostedti, a lower termite that hosts mutualistic microorganisms in its hindgut. Zoolog. Sci. 25, 401-406. doi: 10.2108/zsj.25.401
107. Zhang, D., Lax, A. R., Henrissat, B., Coutinho, P., Katiya, N., Nierman, W. C.,et al. (2012). Carbohydrate-active enzymes revealed in Coptotermes formosanus transcriptome. Insect Mol. Biol. 21, 235-245. doi: 10.1111/j.1365-2583.2011.01130.x