1932

Abstract

Termites have long been studied for their symbiotic associations with gut microbes. In the late nineteenth century, this relationship was poorly understood and captured the interest of parasitologists such as Joseph Leidy; this research led to that of twentieth-century biologists and entomologists including Cleveland, Hungate, Trager, and Lüscher. Early insights came via microscopy, organismal, and defaunation studies, which led to descriptions of microbes present, descriptions of the roles of symbionts in lignocellulose digestion, and early insights into energy gas utilization by the host termite. Focus then progressed to culture-dependent microbiology and biochemical studies of host–symbiont complementarity, which revealed specific microhabitat requirements for symbionts and noncellulosic mechanisms of symbiosis (e.g., N fixation). Today, knowledge on termite symbiosis has accrued exponentially thanks to omic technologies that reveal symbiont identities, functions, and interdependence, as well as intricacies of host–symbiont complementarity. Moving forward, the merging of classical twentieth-century approaches with evolving omic tools should provide even deeper insights into host–symbiont interplay.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-ento-022420-074746
2021-01-07
2024-06-19
Loading full text...

Full text loading...

/deliver/fulltext/en/66/1/annurev-ento-022420-074746.html?itemId=/content/journals/10.1146/annurev-ento-022420-074746&mimeType=html&fmt=ahah

Literature Cited

  1. 1. 
    Beckwith TD, Rose EJ. 1929. Cellulose digestion by organisms from the termite gut. Proc. Soc. Exp. Biol. Med. 27:4–6
    [Google Scholar]
  2. 2. 
    Benjamino J, Graf J. 2016. Characterization of the core and caste-specific microbiota in the termite. Reticulitermes flavipes. Front. Microbiol. 7:171
    [Google Scholar]
  3. 3. 
    Benneman JR. 1973. Nitrogen fixation in termites. Science 181:164–65
    [Google Scholar]
  4. 4. 
    Berchtold M, Ludwig W, König H 1994. 16S rDNA sequence and phylogenetic position of an uncultivated spirochete from the hindgut of the termite Mastotermes darwiniensis Froggatt. FEMS Microbiol. Lett. 123:269–77
    [Google Scholar]
  5. 5. 
    Berlanga M, Paster BJ, Grandcolas P, Guerrero R 2011. Comparison of the gut microbiota from soldier and worker castes of the termite Reticulitermes grassei. Int. Microbiol 14:83–93
    [Google Scholar]
  6. 6. 
    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
    [Google Scholar]
  7. 7. 
    Brauman A, Bignell DE, Tayasu I 2000. Soil-feeding termites: biology, microbial associations, and digestive mechanisms. Termites: Evolution, Sociality, Symbioses, Ecology T Abe, DE Bignell, M Higashi 211–43 Berlin: Springer
    [Google Scholar]
  8. 8. 
    Brauman A, Doré J, Eggleton P, Bignell D, Breznak JA, Kane MD 2001. Molecular phylogenetic profiling of prokaryotic communities in guts of termites with different feeding habits. FEMS Microbiol. Ecol. 35:127–36
    [Google Scholar]
  9. 9. 
    Brauman A, Kane MD, Labat M, Breznak JA 1992. Genesis of acetate and methane by gut bacteria of nutritionally diverse termites. Science 257:1384–87
    [Google Scholar]
  10. 10. 
    Breznak JA, Brill JW, Mertins JW, Coppel HC 1973. Nitrogen fixation in termites. Nature 244:577–79
    [Google Scholar]
  11. 11. 
    Brune A. 2014. Symbiotic digestion of lignocellulose in termite guts. Nat. Rev. Microbiol. 12:168–80
    [Google Scholar]
  12. 12. 
    Brune A, Dietrich C. 2015. The gut microbiota of termites: digesting the diversity in the light of ecology and evolution. Annu. Rev. Microbiol. 69:145–66
    [Google Scholar]
  13. 13. 
    Brune A, Ohkuma M. 2011. Role of the termite gut microbiota in symbiotic digestion. Biology of Termites: A Modern Synthesis DE Bignell, Y Roisin, N Lo 439–75 Berlin: Springer
    [Google Scholar]
  14. 14. 
    Bucek A, Šobotník J, He S, Shi M, McMahon DP et al. 2019. Evolution of termite symbiosis informed by transcriptome-based phylogenies. Curr. Biol. 29:3728–34
    [Google Scholar]
  15. 15. 
    Bulmer MS, Bachelet I, Raman R, Rosengaus RB, Sasisekharan R 2009. Targeting an antimicrobial effector function in insect immunity as a pest control strategy. PNAS 106:12652–57
    [Google Scholar]
  16. 16. 
    Buscalioni L, Comes S. 1910. La digestion delle membrane vegetali per oper dei Flagellati contenuti nell'intestino dei Termitidi e il problema della simbiosi. Atti Acad. Gioenia Sci. Nat. Catania 3:1–16
    [Google Scholar]
  17. 17. 
    Chiu C-I, Ou J-H, Chen C-Y, Li H-F 2019. Fungal nutrition allocation enhances mutualism with fungus-growing termite. Fungal Ecol 41:92–100
    [Google Scholar]
  18. 18. 
    Chouvenc T, Efstathion CA, Elliott ML, Su NY 2013. Extended disease resistance emerging from the faecal nest of a subterranean termite. Proc. Biol. Sci. 280:20131885
    [Google Scholar]
  19. 19. 
    Chouvenc T, Elliott ML, Šobotník J, Efstathion CA, Su NY 2018. The termite fecal nest: a framework for the opportunistic acquisition of beneficial soil Streptomyces (Actinomycetales: Streptomycetaceae). Environ. Entomol. 47:1431–39
    [Google Scholar]
  20. 20. 
    Chouvenc T, Su NY, Robert A 2009. Inhibition of Metarhizium anisopliae in the alimentary tract of the eastern subterranean termite Reticulitermes flavipes. J. Invertebr. Pathol. 101:130–36
    [Google Scholar]
  21. 21. 
    Chung KT, Bryant MP. 1997. Robert E. Hungate: Pioneer of Anaerobic Microbial Ecology. Anaerobe 3:213–17
    [Google Scholar]
  22. 22. 
    Cleveland L. 1959. Sex induced with ecdysone. PNAS 45:747–53
    [Google Scholar]
  23. 23. 
    Cleveland LR. 1923. Correlation between the food and morphology of termites and the presence of intestinal protozoa. Am. J. Hyg. 3:444–61
    [Google Scholar]
  24. 24. 
    Cleveland LR. 1923. Symbiosis between termites and their intestinal protozoa. PNAS 9:424–28
    [Google Scholar]
  25. 25. 
    Cleveland LR. 1924. The physiological and symbiotic relationships between the intestinal protozoa of termites and their host, with special reference to Reticulitermes flavipes. Kollar. Biol. Bull. Mar. Biol. Lab 46:117–227
    [Google Scholar]
  26. 26. 
    Cleveland LR. 1925. The ability of termites to perhaps live indefinitely on a diet of pure cellulose. Biol. Bull. 48:289–93
    [Google Scholar]
  27. 27. 
    Cleveland LR. 1925. The effects of oxygenation and starvation on the symbiosis between the termite, Termopsis, and its intestinal flagellates. Biol. Bull. 48:309–26
    [Google Scholar]
  28. 28. 
    Cleveland LR. 1925. The feeding habit of termite castes and its relation to their intestinal flagellates. Biol. Bull. 48:295–310
    [Google Scholar]
  29. 29. 
    Cleveland LR. 1957. Correlation between the molting period of Cryptocercus and sexuality in its protozoa. J. Eukaryot. Microbiol. 4:168–175
    [Google Scholar]
  30. 30. 
    Cleveland LR, Burke AWJ, Karlson P 1960. Ecdysone induced modifications in the sexual cycles of the protozoa of Cryptocercus. J. Protozool 7:229–39
    [Google Scholar]
  31. 31. 
    Cleveland LR, Hall SR, Sanders EP, Collier J 1934. The wood feeding roach Cryptocercus, its protozoa, and the symbiosis between protozoa and roach. Mem. Am. Acad. Arts Sci. 17:185–342
    [Google Scholar]
  32. 32. 
    Cleveland LR, Nutting WL. 1955. Suppression of sexual cycles and death of the protozoa of Cryptocercus resulting from change of hosts during molting period. J. Exp. Zool. 130:485–513
    [Google Scholar]
  33. 33. 
    Cook SF. 1932. The respiratory gas exchange in Termopsis nevadensis. Biol. Bull 63:246–57
    [Google Scholar]
  34. 34. 
    Cook SF. 1943. Non-symbiotic utilization of carbohydrates by the termite. Zootermopsis angusticollis. Physiol. Zool. 16:123–28
    [Google Scholar]
  35. 35. 
    Cook SF, Smith RE. 1942. Metabolic relations in the termite—protozoa symbiosis; temperature effects. J. Cell. Comp. Physiol. 19:211–19
    [Google Scholar]
  36. 36. 
    Cragg SM, Beckham GT, Bruce NC, Bugg TD, Distel DL et al. 2015. Lignocellulose degradation mechanisms across the Tree of Life. Curr. Opin. Chem. Biol. 29:108–19
    [Google Scholar]
  37. 37. 
    Dedeine F, Weinert LA, Bigot D, Josse T, Ballenghien M et al. 2015. Comparative analysis of transcriptomes from secondary reproductives of three Reticulitermes termite species. PLOS ONE 10:e0145596
    [Google Scholar]
  38. 38. 
    Desai MS, Brune A. 2012. Bacteroidales ectosymbionts of gut flagellates shape the nitrogen-fixing community in dry-wood termites. ISME J 6:1302–13
    [Google Scholar]
  39. 39. 
    Do TH, Nguyen TT, Nguyen TN, Le QG, Nguyen C et al. 2014. Mining biomass-degrading genes through Illumina-based de novo sequencing and metagenomics analysis of free-living bacteria in the gut of the lower termite Coptotermes gestroi harvested in Vietnam. J. Biosci. Bioeng. 118:665–71
    [Google Scholar]
  40. 40. 
    Donia MS, Fischbach MA. 2015. Small molecules from the human microbiota. Science 349:1254766
    [Google Scholar]
  41. 41. 
    Du X, Li X, Wang Y, Peng J, Hong H, Yang H 2012. Phylogenetic diversity of nitrogen fixation genes in the intestinal tract of Reticulitermes chinensis Snyder. Curr. Microbiol. 65:547–51
    [Google Scholar]
  42. 42. 
    Friedrich M, Schmitt-Wagner D, Lueders T, Brune A 2001. Axial differences in community structure of Crenarchaeota and Euryarcheaota in the highly compartmentalized gut of the soil feeding termite Cubitermes orthognathus. Appl. Environ. Microbiol 67:104880–90
    [Google Scholar]
  43. 43. 
    Gile GH, James ER, Tai V, Harper JT, Merrell TL et al. 2018. New species of Spirotrichonympha from Reticulitermes and the relationships among genera in Spirotrichonymphea (Parabasalia). J. Eukaryot. Microbiol. 65:159–69
    [Google Scholar]
  44. 44. 
    Grassi B, Sandias A. 1893. Constituzione e sviluppo della società dei termitidi. Atti Accad. Gioenia Sci. Nat. Catania 6:1–75
    [Google Scholar]
  45. 45. 
    Grieco MA, Cavalcante JJ, 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
    [Google Scholar]
  46. 46. 
    Hammer TJ, Moran NA. 2019. Links between metamorphosis and symbiosis in holometabolous insects. Philos. Trans. R. Soc. Lond. B 374:178320190068
    [Google Scholar]
  47. 47. 
    Harper JT, Gile GH, James ER, Carpenter KJ, Keeling PJ 2009. The inadequacy of morphology for species and genus delineation in microbial eukaryotes: an example from the parasbasalian termite symbiont Coronympha. PLOS ONE 4:8e6577
    [Google Scholar]
  48. 48. 
    Harrison MC, Jongepier E, Robertson HM, Arning N, Bitard-Feildel T et al. 2018. Hemimetabolous genomes reveal molecular basis of termite eusociality. Nat. Ecol. Evol. 3:557–66
    [Google Scholar]
  49. 49. 
    He S, Ivanova N, Kirton E, Allgaier M, 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
    [Google Scholar]
  50. 50. 
    Hongoh Y, Sharma VK, Prakash T, Noda S, Taylor TD et al. 2008. Complete genome of the uncultured Termite Group 1 bacteria in a single host protist cell. PNAS 105:5555–60
    [Google Scholar]
  51. 51. 
    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
    [Google Scholar]
  52. 52. 
    Hungate RE. 1938. Studies on the nutrition of Zootermopsis. II. The relative importance of the termite and the protozoa in wood digestion. Ecology 19:1–25
    [Google Scholar]
  53. 53. 
    Hungate RE. 1939. Experiments on the nutrition of Zootermopsis. III. The anaerobic carbohydrate dissimilation by the intestinal protozoa. Ecology 20:230–45
    [Google Scholar]
  54. 54. 
    Hungate RE. 1941. Experiments on the nitrogen economy of termites. Ann. Entomol. Soc. Am. 34:467–89
    [Google Scholar]
  55. 55. 
    Hungate RE. 1945. Studies on cellulose fermentation II: an anaerobic cellulose-decomposing actinomycete, Micromonospora propionici, N. sp. J. Bacteriol. 54:151–56
    [Google Scholar]
  56. 56. 
    Hungate RE. 1979. Evolution of a microbial ecologist. Annu. Rev. Microbiol. 33:1–20
    [Google Scholar]
  57. 57. 
    Hussin NA, Zarkasi KZ, Ab Majid AH 2018. Characterization of gut bacterial community associated with worker and soldier castes of Globitermes sulphureus Haviland (Blattodea: Termitidae) using 16S rRNA metagenomics. J. Asia-Pac. Entomol. 21:1268–74
    [Google Scholar]
  58. 58. 
    Imms AD. 1920. On the structure and biology of Archotermopsis, together with descriptions of new species of intestinal protozoa, and general observations on the Isoptera. Philos. Trans. R. Soc. Lond. B 209:75–180
    [Google Scholar]
  59. 59. 
    Inoue T, Murashima K, Azuma JI, Sugimoto A, Slaytor M 1997. Cellulose and xylan utilization in the lower termite Reticulitermes speratus. J. Insect Physiol 43:235–42
    [Google Scholar]
  60. 60. 
    James ER, Tai V, Scheffrahn RH, Keeling PJ 2013. Trichnympha 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
    [Google Scholar]
  61. 61. 
    Karlson P, Lüscher M. 1959. “Pheromones”: a new term for a class of biologically active substances. Nature 183:55–56
    [Google Scholar]
  62. 62. 
    Koidzumi M. 1921. Studies of the intestinal protozoa of the termite of Japan. Parasitology 13:3235–309
    [Google Scholar]
  63. 63. 
    Kudo T, Ohkuma M, Moriya S, Noda S, Ohtoko K 1998. Molecular phylogenetic identification of the intestinal anaerobic microbial community in the hindgut of the termite, Reticulitermes speratus, without cultivation. Extremophiles 2:155–61
    [Google Scholar]
  64. 64. 
    Lamberty M, Zachary D, Lanot R, Bordereau C, Robert A et al. 2001. Insect immunity: constitutive expression of a cysteine-rich antifungal and a linear antibacterial peptide in a termite insect. J. Biol. Chem. 276:4085–92
    [Google Scholar]
  65. 65. 
    Leadbetter JR, Breznak JA. 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 62:3620–21
    [Google Scholar]
  66. 66. 
    Leadbetter JR, Schmidt TM, Graber JR, Breznak JA 1999. Acetogenesis from H2 plus CO2 by spirochetes from termite guts. Science 283:636–89
    [Google Scholar]
  67. 67. 
    Lespès C. 1856. Recherches sur l'organization et les moeurs du Termite lucifuge. Ann. Sci. Nat. Zool 5:227–82
    [Google Scholar]
  68. 68. 
    Leidy J. 1877. On the intestinal parasites of Termes flavipes. PNAS 29:146–49
    [Google Scholar]
  69. 69. 
    Leidy J. 1881. The parasites of termites. J. Acad. Phila. 2:425–27
    [Google Scholar]
  70. 70. 
    Leuthold R. 1980. Obituary of Martin Lüscher. Nature 284:197–98
    [Google Scholar]
  71. 71. 
    Liu XJ, Xie L, Liu N, Zhan S, Zhou XG, Wang Q 2017. RNA interference unveils the importance of Pseudotrichonympha grassii cellobiohydrolase, a protozoan exoglucanase, in termite cellulose degradation. Insect Mol. Biol. 26:233–42
    [Google Scholar]
  72. 72. 
    Lüscher M. 1949. Continuous observation of termites in laboratory cultures. Acta Trop 6:161–65
    [Google Scholar]
  73. 73. 
    Lüscher M. 1951. Significance of “fungus gardens” in termite nests. Nature 167:34–35
    [Google Scholar]
  74. 74. 
    Lüscher M. 1952. New evidence for an ectohormonal control of caste determination in termites. Transactions of the 9th International Congress of Entomology, Amsterdam, Aug. 17–24289–94 Amsterdam: Congr. Entomol.
    [Google Scholar]
  75. 75. 
    Lüscher M. 1953. The termite and the cell. Sci. Am. 188:574–78
    [Google Scholar]
  76. 76. 
    Lüscher M. 1960. Hormonal control of caste differentiation in termites. Ann. N. Y. Acad. Sci. 89:549–63
    [Google Scholar]
  77. 77. 
    Lüscher M. 1961. Air-conditioned termite nests. Sci. Am. 205:138–47
    [Google Scholar]
  78. 78. 
    Lüscher M. 1972. Environmental control of juvenile hormone (JH) secretion and caste differentiation in termites. Gen. Comp. Endocrinol. 3:509–14
    [Google Scholar]
  79. 79. 
    Lüscher M, Springhetti A. 1960. Untersuchungen uber die bedeutung der corpora allata fur die differenzierung der kasten bei der termite Kalotermes-flavicollis. J. Insect Physiol. 5:190–212
    [Google Scholar]
  80. 80. 
    Manjula A, Pushpanathan M, Sathyavathi S, Gunasekaran P, Rajendhran J 2016. Comparative analysis of microbial diversity in termite gut and termite nest using ion sequencing. Curr. Microbiol. 72:267–75
    [Google Scholar]
  81. 81. 
    Marynowska M, Goux X, Sillam-Dussès D, Rouland-Lefèvre C, Roisin Y et al. 2017. Optimization of a metatranscriptomic approach to study the lignocellulolytic potential of the higher termite gut microbiome. BMC Genom 18:681
    [Google Scholar]
  82. 82. 
    Masuoka Y, Toga K, Nalepa CA, Maekawa K 2018. A crucial caste regulation gene detected by comparing termites and sister group cockroaches. Genetics 209:1225–34
    [Google Scholar]
  83. 83. 
    Mevers E, Chouvenc T, Su NY, Clardy J 2017. Chemical interaction among termite-associated microbes. J. Chem. Ecol. 43:1078–85
    [Google Scholar]
  84. 84. 
    Misra JN, Vijayaraghavan PK. 1956. Ethylmalonate—an inhibitor of termite cellulase. Curr. Sci. 25:229–30
    [Google Scholar]
  85. 85. 
    Nakashima K, Watanabe H, Saitoh H, Tokuda G, Azuma JI 2002. Dual cellulose-digesting system of the wood-feeding termite, Coptotermes formosanus Shiraki. Insect Biochem. Mol. Biol. 32:777–84
    [Google Scholar]
  86. 86. 
    Nalepa CA. 2017. What kills the hindgut flagellates of lower termites during the host molting cycle. Microorganisms 5:82
    [Google Scholar]
  87. 87. 
    Nauer PA, Hutley LB, Arndt SK 2018. Termite mounds mitigate half of termite methane emissions. PNAS 115:13306–11
    [Google Scholar]
  88. 88. 
    Noda S, Ohkuma M, Usami R, Horikoshi K, Kudo T 1999. Culture-independent characterization of a gene responsible for nitrogen fixation in the symbiotic microbial community in the gut of the termite Neotermes koshunensis. Appl. Environ. Microbiol 65:4935–42
    [Google Scholar]
  89. 89. 
    Nutting WL. 1956. Reciprocal protozoan transfaunations between the roach, Cryptocercus, and the termite. Zootermopsis. Biol. Bull. 110:83–90
    [Google Scholar]
  90. 90. 
    Nutting WL, Cleveland LR. 1954. Effects of reciprocal transfaunations on protozoa of the roach Cryptocercus and the termite Zootermopsis. Anat. Rec 120:786
    [Google Scholar]
  91. 91. 
    Ohkuma M, Noda S, Kudo T 1999. Phylogenetic diversity of nitrogen fixation genes in the symbiotic microbial community in the gut of diverse termites. Appl. Environ. Microbiol. 65:4926–34
    [Google Scholar]
  92. 92. 
    Ohkuma M, Noda S, Usami R, Horikoshi K, Kudo T 1996. Diversity of nitrogen fixation genes in the symbiotic intestinal microflora of the termite Reticulitermes speratus. Appl. Environ. Microbiol 62:2747–52
    [Google Scholar]
  93. 93. 
    Oransky I. 2005. Obituary of William Trager. Lancet 365:748
    [Google Scholar]
  94. 94. 
    Otani S, Zhukova M, Koné NA, da Costa RR, Mikaelyan A et al. 2019. Gut microbial compositions mirror caste-specific diets in a major lineage of social insects. Environ. Microbiol. Rep. 11:2196–205
    [Google Scholar]
  95. 95. 
    Pester M, Brune A. 2007. Hydrogen is the central free intermediate during lignocellulose degradation by termite gut symbionts. ISME J 1:551–65
    [Google Scholar]
  96. 96. 
    Peterson BF, Scharf ME. 2016. Lower termite associations with microbes: synergy, protection, and interplay. Front. Microbiol. 7:422
    [Google Scholar]
  97. 97. 
    Peterson BF, Scharf ME. 2016. Metatranscriptome analysis reveals bacterial symbiont contributions to lower termite physiology and potential immune functions. BMC Genom 17:772
    [Google Scholar]
  98. 98. 
    Peterson BF, Stewart HL, Scharf ME 2015. Quantification of symbiotic contributions to lower termite lignocellulose digestion using antimicrobial treatments. Insect Biochem. Mol. Biol. 59:80–88
    [Google Scholar]
  99. 99. 
    Potrikus CA, Breznak JM. 1980. Uric acid-degrading bacteria in guts of termites. Appl. Environ. Microbiol. 40:117–24
    [Google Scholar]
  100. 100. 
    Potrikus CA, Breznak JM. 1981. Gut bacteria recycle uric acid nitrogen in termites: a strategy for nutrient conservation. PNAS 78:4601–5
    [Google Scholar]
  101. 101. 
    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
    [Google Scholar]
  102. 102. 
    Pramono AK, Kuwahara H, Itoh T, Toyoda A, Yamada A, Hongoh Y 2017. Discovery and complete genome sequence of a bacteriophage from an obligate intracellular symbiont of a cellulytic protist in the termite gut. Microb. Environ. 32:112–17
    [Google Scholar]
  103. 103. 
    Rahman NA, Parks DH, Willner DL, Engelbrektson AL, Goddrefi 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
    [Google Scholar]
  104. 104. 
    Rajarapu SP, Scharf ME. 2017. Saccharification of agricultural lignocellulose feedstocks and protein-level responses by a termite gut-microbe bioreactor. Front. Energy Res. 5:5
    [Google Scholar]
  105. 105. 
    Rajarapu SP, Shreve JT, Bhide KP, Thimmapuram J, Scharf ME 2015. Metatranscriptomic profiles of Eastern subterranean termites, Reticulitermes flavipes (Kollar) fed on second generation feedstocks. BMC Genom 16:332
    [Google Scholar]
  106. 106. 
    Raje K, Peterson BF, Scharf ME 2018. Screening of 57 candidate double-stranded RNAs for insecticidal activity against the pest termite Reticulitermes flavipes. J. Econ. Entomol 111:2782–87
    [Google Scholar]
  107. 107. 
    Rosengaus RB, Moustakas JE, Calleri DV, Traniello JF 2003. Nesting ecology and cuticular microbial loads in dampwood (Zootermopsis angusticollis) and drywood termites (Incisitermes minor, I. schwarzi, Cryptotermes cavifrons). J. Insect Sci 3:31
    [Google Scholar]
  108. 108. 
    Rosengaus RB, Schultheis KF, Yalonetskaya A, Bulmer MS, DuComb WS et al. 2014. Symbiont-derived β-1,3-glucanases in a social insect: mutualism beyond nutrition. Front. Microbiol. 5:607
    [Google Scholar]
  109. 109. 
    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 5:71100–42
    [Google Scholar]
  110. 110. 
    Saiki R, Gotoh H, Toga K, Miura T, Maekawa K 2015. High juvenile hormone titre and abdominal activation of JH signaling may induce reproduction of termite neotenics. Insect Mol. Biol. 24:432–41
    [Google Scholar]
  111. 111. 
    Sapountzis P, de Verges J, Rousk K, Cilliers M, Vorster BJ, Poulsen M 2016. Potential for nitrogen fixation in the fungus-growing termite symbiosis. Front. Microbiol. 7:1993
    [Google Scholar]
  112. 112. 
    Scharf ME. 2015. Omic research in termites: an overview and a roadmap. Front. Genet. 6:76
    [Google Scholar]
  113. 113. 
    Scharf ME. 2015. Termites as targets and models for biotechnology. Annu. Rev. Entomol. 60:77–102
    [Google Scholar]
  114. 114. 
    Scharf ME, Boucias DG. 2010. Potential of termite-based biomass pre-treatment strategies for use in bioethanol production. Insect Sci 17:166–74
    [Google Scholar]
  115. 115. 
    Scharf ME, Cai Y, Sun Y, Sen R, Raychoudhury R, Boucias DG 2017. A meta-analysis testing eusocial co-option theories in termite gut physiology and symbiosis. Commun. Integr. Biol. 10:e1295187
    [Google Scholar]
  116. 116. 
    Scharf ME, Karl ZJ, Sethi A, Boucias DG 2011. Multiple levels of synergistic collaboration in termite lignocellulose digestion. PLOS ONE 6:e21709
    [Google Scholar]
  117. 117. 
    Scharf ME, Tartar A. 2008. Termite digestomes as sources for novel lignocellulases. Biofuels Bioprod. Bioref. 2:540–52
    [Google Scholar]
  118. 118. 
    Scharf ME, Wu-Scharf D, Zhou X, Pittendrigh BR, Bennett GW 2005. Gene expression profiles among immature and adult reproductive castes of the termite Reticulitermes flavipes. Insect Mol. Biol 14:31–44
    [Google Scholar]
  119. 119. 
    Schmidlin K, Kraberger S, Fontenele RS, De Martini F, Chouvenc T et al. 2019. Genome sequences of microviruses associated with Coptotermes formosanus. Microbiol. Resour. Announc 8:16e00185–19
    [Google Scholar]
  120. 120. 
    Schultz JE, Breznak JA. 1978. Heterotrophic bacteria present in hindguts of wood-eating termites [Reticulitermes flavipes (Kollar)]. Appl. Environ. Microbiol. 35:5930–36
    [Google Scholar]
  121. 121. 
    Sen R, Raychoudhury R, Cai YP, Sun YJ, Lietze VU 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 Genom 14:491
    [Google Scholar]
  122. 122. 
    Sen R, Raychoudhury R, Cai YP, Sun YJ, Lietze VU et al. 2015. Molecular signatures of nicotinoid-pathogen synergy in the termite gut. PLOS ONE 10:e0123391
    [Google Scholar]
  123. 123. 
    Sethi A, Kovaleva ES, Slack JM, Brown S, Buchman GW, Scharf ME 2013. A GHF7 cellulase from the protist symbiont community of Reticulitermes flavipes enables more efficient lignocellulose processing by host enzymes. Arch. Insect. Biochem. Physiol. 84:175–93
    [Google Scholar]
  124. 124. 
    Sethi A, Slack JM, Kovaleva ES, Buchman GW, Scharf ME 2013. Lignin-associated metagene expression in a lignocellulose-digesting termite. Insect Biochem. Mol. Biol. 43:91–101
    [Google Scholar]
  125. 125. 
    Su NY, Monteagudo EJ. 2017. Hyperecdysonism in the Formosan subterranean termite and Eastern subterranean termite. J. Econ. Entomol. 110:1736–39
    [Google Scholar]
  126. 126. 
    Tai V, James ER, Nalepa CA, Scheffrahn RH, Perlman SJ, Keeling PJ 2015. The role of host phylogeny varies in structuring the microbial communities in the hindguts of lower termites. Appl. Environ. Microbiol. 81:1059–70
    [Google Scholar]
  127. 127. 
    Tai V, James ER, Perlman SJ, Keeling PJ 2013. Single-cell barcoding using sequences from the small subunit rRNA and internal transcribed spacer region identifies new species of Trichonympha and Trichmitopsis from the hindgut of the termite Zootermopsis angusticollis. PLOS ONE 8:e58728
    [Google Scholar]
  128. 128. 
    Tartar A, Wheeler MM, Zhou X, Coy MR, Boucias DG, Scharf ME 2009. Parallel metatranscriptome analyses of host and symbiont gene expression in the gut of the termite Reticulitermes flavipes. Biotechnol. Biofuels 2:25
    [Google Scholar]
  129. 129. 
    Terrapon N, Li C, Robertson HM, Ji L, Meng X et al. 2014. Molecular traces of alternative social organization in a termite genome. Nat. Commun. 5:3636
    [Google Scholar]
  130. 130. 
    Thong-On A, Suzuki K, Noda S, Inoue J, Kajiwara S, Ohkuma M 2012. Isolation and characterization of anaerobic bacteria for symbiotic recycling of uric acid nitrogen in the gut of various termites. Microbes Environ 27:186–92
    [Google Scholar]
  131. 131. 
    Tokuda G, Lo N, Watanabe H 2005. Marked variations in patterns of cellulase activity against crystalline- versus carboxymethyl-cellulose in the digestive systems of diverse, wood-feeding termites. Physiol. Entomol. 30:372–80
    [Google Scholar]
  132. 132. 
    Tokuda G, Mikaelyan A, Fukui C, Matsuura Y, Watanabe H et al. 2018. Fiber-associated spirochetes are major agents of hemicellulose degradation in the hindgut of wood-feeding higher termites. PNAS 115:E11996–2004
    [Google Scholar]
  133. 133. 
    Tokuda G, Watanabe H, Matsumoto T, Noda K 1997. Cellulose digestion in the wood-eating higher termite, Nasutitermes takasagoensis (Shiraki): distribution of cellulases and properties of endo-β-1,4-glucanases. Zool Sci 14:183–93
    [Google Scholar]
  134. 134. 
    Trager W. 1932. A cellulase from the symbiotic intestinal flagellates of termites and of the roach. Cryptocercus punctulatus. Biochem. J. 26:1762–71
    [Google Scholar]
  135. 135. 
    Trager W. 1934. The cultivation of a cellulose-digesting flagellate, Trichomonas termopsidis, and of certain other termite protozoa. Biol. Bull. 66:182–90
    [Google Scholar]
  136. 136. 
    Tramontina R, Franco Cairo JP, Liberato MV, Mandelli F, Sousa A et al. 2017. The Coptotermes gestroi aldo-keto reductase: a multipurpose enzyme for biorefinery applications. Biotechnol. Biofuels 10:4
    [Google Scholar]
  137. 137. 
    Treitli SC, Kolisko M, Husník F, Keeling PJ, Hampl V 2019. Revealing the metabolic capacity of Streblomastix strix and its bacterial symbionts using single-cell metagenomics. PNAS 116:19675–84
    [Google Scholar]
  138. 138. 
    Warnecke F, Luginbuhl 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
    [Google Scholar]
  139. 139. 
    Warren L. 1998. Joseph Leidy: The Last Man Who Knew Everything New Haven, CT: Yale Univ. Press
    [Google Scholar]
  140. 140. 
    Watanabe H, Noda H, Tokuda G, Lo N 1998. A cellulase gene of termite origin. Nature 394:330–31
    [Google Scholar]
  141. 141. 
    Wheeler MM, Zhou XG, Scharf ME, Oi FM 2007. Molecular and biochemical markers for monitoring dynamic shifts of cellulolytic protozoa in Reticulitermes flavipes. Insect Biochem. Mol. Biol 37:1366–74
    [Google Scholar]
  142. 142. 
    Wilson EO, Bossert WH. 1963. Chemical communication among insects. Recent Prog. Horm. Res. 19:673–716
    [Google Scholar]
  143. 143. 
    Wu WJ, Gu DF, Yan SC, Li ZQ 2019. RNA interference of endoglucanases in the Formosan subterranean termite Coptotermes formosanus Shiraki by dsRNA injection or ingestion. J. Insect Physiol. 112:15–22
    [Google Scholar]
  144. 144. 
    Wu WJ, Li ZQ. 2018. dsRNA injection successfully inhibited two endogenous beta-glucosidases in Coptotermes formosanus. J. Econ. Entomol 111:860–67
    [Google Scholar]
  145. 145. 
    Wu WJ, Li ZQ, Zhang S, Ke Y, Hou Y 2016. Transcriptome response to elevated atmospheric CO(2) concentration in the Formosan subterranean termite, Coptotermes formosanus Shiraki (Isoptera: Rhinotermitidae). PeerJ 4:e2527
    [Google Scholar]
  146. 146. 
    Yaguchi H, Shigenobu S, Hayashi Y, Miyazaki S, Toga K et al. 2018. A lipocalin protein, Neural Lazarillo, is key to social interactions that promote termite soldier differentiation. Proc. Biol. Sci. 285:20180707
    [Google Scholar]
  147. 147. 
    Yang H, Schmitt-Wagner D, Stingl U, Brune A 2005. Niche heterogeneity determines bacterial community structure in the termite gut (Reticulitermes santonensis). Environ. Microbiol. 7:7916–32
    [Google Scholar]
  148. 148. 
    Yokoe Y. 1964. Cellulase activity in the termite, Leucotermes speratus, with new evidence in support of a cellulase produced by the termite itself. Sci. Pap. Coll. Gen. Educ. Univ. Tokyo 14:115–20
    [Google Scholar]
  149. 149. 
    Zhang D, Lax AR, Henrissat B, Coutinho P, Katiya N et al. 2012. Carbohydrate-active enzymes revealed in Coptotermes formosanus (Isoptera: Rhinotermitidae) transcriptome. Insect Mol. Biol. 21:235–45
    [Google Scholar]
  150. 150. 
    Zheng H, Dietrich C, Radek R, Brune A 2016. Endomicrobium proavitum, the first isolate of Endomicrobia class. nov. (phylum Elusimicrobia): an ultramicrobacterium with an unusual cell cycle that fixes nitrogen with a Group IV nitrogenase. Environ. Microbiol. 18:191–204
    [Google Scholar]
  151. 151. 
    Zhou J, Duan J, Gao M, Wang Y, Wang X, Zhao K 2019. Diversity, roles, and biotechnological applications of symbiotic microorganisms in the gut of termite. Curr. Microbiol. 76:755–61
    [Google Scholar]
  152. 152. 
    Zhou X, Smith JA, Oi FM, Koehler PG, Bennett GW, Scharf ME 2007. Correlation of cellulase gene expression and cellulolytic activity throughout the gut of the termite Reticulitermes flavipes. Gene 395:29–39
    [Google Scholar]
/content/journals/10.1146/annurev-ento-022420-074746
Loading
/content/journals/10.1146/annurev-ento-022420-074746
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error