Towards an integrated understanding of the consequences of fungus domestication on the fungus-growing termite gut microbiota

Environmental Microbiology

Volumn 17, Issue 8, 2015, Pages 2562-2572

  Poulsen, Michael ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA (MICROORGANISMS); FUNGI; ISOPTERA; MACROTERMITINAE; TERMITIDAE; TERMITOMYCES;

ANIMAL; EVOLUTION; INTESTINE FLORA; ISOPTERA; METABOLISM; MICROBIOLOGY; PHYLOGENY; PHYSIOLOGY; PLANT; SYMBIOSIS; TERMITOMYCES;

ANIMALS; BIOLOGICAL EVOLUTION; GASTROINTESTINAL MICROBIOME; ISOPTERA; PHYLOGENY; PLANTS; SYMBIOSIS; TERMITOMYCES;

EID: 84939268290     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/1462-2920.12765     Document Type: Short Survey

References (71)

1. Aanen, D.K., Eggleton, P., Rouland-Lefèvre, C., Guldberg-Frøslev, T., Rosendahl, S., and Boomsma, J.J. (2002) The evolution of fungus-growing termites and their mutualistic fungal symbionts. Proc Natl Acad Sci USA 99: 14887-14892.
2. Aanen, D.K., de Fine Licht, H.H., Debets, A.J.M., Kerstes, N.A.G., Hoekstra, R.F., and Boomsma, J.J. (2009) High symbiont relatedness stabilizes mutualistic cooperation in fungus-growing termites. Science 326: 1103-1106.
3. Abo-Khatwa, N. (1978) Cellulase of fungus-growing termites: a new hypothesis on its origin. Cell Mol Life Sci 34: 559-560.
4. Baumann, P., Baumann, L., Lai, C.-Y., Rouhbakhsh, D., Moran, N.A., and Clark, M.A. (1995) Genetics, physiology, and evolutionary relationships of the genus Buchnera: intracellular symbionts of aphids. Annu Rev Microbiol 49: 55-94.
5. Bignell, D.E. (2000) Introduction to symbiosis. In Termites: Evolution, Sociality, Symbiosis, Ecology. Abe, T., Bignell, D.E., and Higashi, M. (eds). Dordrecht, The Netherlands: Kluwer Academic Publishers, pp. 189-208.
6. Bignell, D.E., Slaytor, M., Veivers, P.C., Muhlemann, R., and Leuthold, R.H. (1994) Functions of symbiotic fungus gardens in higher termites of the genus Macrotermes: evidence against the acquired enzyme hypothesis. Acta Microbiol Immunol Hung 41: 391-401.
7. Bourguignon, T., Lo, N., Cameron, S.L., Šobotník, J., Hayashi, Y., Shigenobu, S., etal. (2014) The evolutionary history of termites as inferred from 66 mitochondrial genomes. Mol Biol Evol 32: 406-421.
8. Brugerolle, G., and Radek, R. (2006) Symbiotic protozoa of termites. In Intestinal Microorganisms of Termites and Other Invertebrates. König, H., and Varma, A. (eds). Berlin, Germany: Springer-Verlag, pp. 243-269.
9. Brune, A., and Ohkuma, M. (2011) Role of the termite gut microbiota in symbiotic digestion. In Biology of Termites: A Modern Synthesis. Bignell, D., Roisin, Y., and Lo, N. (eds). Dordrecht, The Netherlands: Springer, pp. 439-475.
10. Brune, A. (2014) Symbiotic digestion of lignocellulose in termite guts. Nature Rev Microbiol 12: 168-180.
11. Cairns, T., Minuzzi, F., and Bignell, E. (2011) The host-infecting fungal transcriptome. FEMS Microbiol Lett 307: 1-11.
12. Carr, G., Poulsen, M., Klassen, J.L., Hou, Y., Wyche, T.P., Bugni, T.S., etal. (2012) Microtermolides A and B from termite-associated Streptomyces sp. and structural revision of Vinylamycin. Org Lett 14: 2822-2825.
13. 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.
14. Cleveland, L.R. (1923) Symbiosis between termites and their intestinal protozoa. Proc Natl Acad Sci USA 9: 424-428.
15. Darlington, J. (1994) Nutrition and evolution in fungus-growing termites. In Nourishment and Evolution in Insect Societies. Hunt, J.H., and Nalepa, C.A. (eds). Boulder, CO, USA: Westview Press, pp. 105-130.
16. Deng, T.F., Chen, C.R., Cheng, M.L., Pan, C.Y., Zhou, Y., and Mo, J.C. (2008) Differences in cellulase activity among different castes of Odontotermes formosanus (Isoptera: Termitidae) and the symbiotic fungus Termitomyces albuminosus. Sociobiology 51: 697-704.
17. Dietrich, C., Köhler, T., and Brune, A. (2014) The cockroach origin of the termite gut microbiota: patterns in bacterial community structure reflect major evolutionary events. Appl Environ Microbiol 80: 2261-2269.
18. Dillon, R.J., and Charnley, A.K. (1995) Chemical barriers to gut infection in the desert locust - in-vivo production of antimicrobial phenols associated with the bacterium Pantoea agglomerans. J Invertebr Pathol 66: 72-75.
19. Donovan, S.E., Eggleton, P., and Bignell, D.E. (2001) Gut content analysis and a new feeding group classification of termites. Ecol Entomol 26: 356-366.
20. Eggleton, P. (2000) Global patterns of termite diversity. In Termites: Evolution, Sociality, Symbiosis, Ecology. Abe, T., Bignell, D.E., and Higashi, M. (eds). Dordrecht, The Netherlands: Kluwer Academic Publishers, pp. 25-51.
21. Eggleton, P. (2006) The termite gut habitat: its evolution and co-evolution. In Intestinal Microorganisms of Termites and Other Invertebrates. König, H., and Varma, A. (eds). Berlin, Germany: Springer-Verlag, pp. 373-404.
22. Engel, M.S., Grimaldi, D.A., and Krishna, K. (2009) Termites (Isoptera): their phylogeny, classification, and rise to ecological dominance. Am Mus Novit 3650: 1-27.
23. Forsgren, E., Olofsson, T.C., Vasquez, A., and Fries, I. (2010) Novel lactic acid bacteria inhibiting Paenibacillus larvae in honeybee larvae. Apidologie 41: 99-108.
24. Frøslev, T.G., Aanen, D.K., Læssøe, T., and Rosendahl, S. (2003) Phylogenetic relationships of Termitomyces and related taxa. Mycol Res 107: 1277-1286.
25. Ghosh, A.K., Banerjee, P.C., and Sengupta, S. (1980) Purification and properties of xylan hydrolase from mushroom Termitomyces clypeatus. Biochim Biophys Acta 612: 143-152.
26. Gilbert, S.F., Sapp, J., and Tauber, A.I. (2012) A symbiotic view of life: we have never been individuals. Q Rev Biol 87: 325-341.
27. Grassé, P.-P., and Noirot, C. (1958) Le meule des termites champignonnistes et sa signification symbiotique. Ann Sci Nat Zool Biol Animale 11: 113-128.
28. Hansen, A.K., and Moran, N.A. (2011) Aphid genome expression reveals host-symbiont cooperation in the production of amino acids. Proc Natl Acad Sci USA 108: 2849-2854.
29. Hess, M., Sczyrba, A., Egan, R., Kim, T.-W., Chokhawala, H., Schroth, G., etal. (2011) Metagenomic discovery of biomass-degrading genes and genomes from cow rumen. Science 331: 463-467.
30. Hongoh, Y., Ekpornprasit, L., Inoue, T., Moriya, S., Trakulnaleamsai, S., Ohkuma, M., etal. (2006) Intracolony variation of bacterial gut microbiota among castes and ages in the fungus-growing termite Macrotermes gilvus. Mol Ecol 15: 505-516.
31. Hyodo, F., Inoue, T., Azuma, J.I., Tayasu, I., and Abe, T. (2000) Role of the mutualistic fungus in lignin degradation in the fungus-growing termite Macrotermes gilvus (Isoptera; Macrotermitinae). Soil Biol Biochem 32: 653-658.
32. Hyodo, F., Tayasu, I., Inoue, T., Azuma, J.I., Kudo, T., and Abe, T. (2003) Differential role of symbiotic fungi in lignin degradation and food provision for fungus-growing termites (Macrotermitinae: Isoptera). Funct Ecol 17: 186-193.
33. Inward, D., Beccaloni, G., and Eggleton, P. (2007) Death of an order: a comprehensive molecular phylogenetic study confirms that termites are eusocial cockroaches. Biol Lett 22: 331-335.
34. Kaltenpoth, M., and Engl, T. (2014) Defensive microbial symbionts in Hymenoptera. Funct Ecol 28: 315-327.
35. Kashyap, P.C., Marcobal, A., Ursell, L.K., Larauche, M., Duboc, H., Earle, K.A., etal. (2013) Complex interactions among diet, gastrointestinal transit, and gut microbiota in humanized mice. Gastroenterology 144: 967-977.
36. Kirk, P.M., Cannon, P.F., David, J.C., and Stalpers, J.A. (2001) Ainsworth & Bigby's Dictionary of the Fungi. Wallingford, UK: CAB International.
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.
38. Korb, J., and Aanen, D.K. (2003) The evolution of uniparental transmission of fungal symbionts in fungus-growing termites (Macrotermitinae). Behav Ecol Sociobiol 53: 65-71.
39. Liu, N., Zhang, L., Zhou, H., Zhang, M., Yan, X., Wang, Q., etal. (2013) Metagenomic insights into metabolic capacities of the gut microbiota in a fungus-cultivating termite (Odontotermes yunnanensis). PLoS ONE 8: e69184.
40. Makonde, H.M., Boga, H.I., Osiemo, Z., Mwirichia, R., Mackenzie, L.M., Göker, M., and Klenk, H.P. (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.
41. Martin, M.M., and Martin, J.S. (1978) Cellulose digestion in the midgut of the fungus-growing termite Macrotermes natalensis: the role of acquired digestive enzymes. Science 199: 1453-1455.
42. Martin, M.M., and Martin, J.S. (1979) The distribution and origins of the cellulolytic enzymes of the higher termite, Macrotermes natalensis. Physiol Zool 52: 11-21.
43. Mathew, G.M., Ju, Y.-M., Lai, C.-Y., Mathew, D.C., and Huang, C.C. (2011) Microbial community analysis in the termite gut and fungus comb of Odontotermes formosanus: the implication of Bacillus as mutualists. FEMS Microbiol Ecol 79: 504-517.
44. Matoub, M., and Rouland, C. (1995) Purification and properties of the xylanases from the termite Macrotermes bellicosus and its symbiotic fungus Termitomyces sp. Comp Biochem Physiol Biochem Mol Biol 112: 629-635.
45. Nobre, T., and Aanen, D.K. (2012) Fungiculture or termite husbandry? The ruminant hypothesis. Insects 3: 307-323.
46. Nobre, T., Rouland-Lefèvre, C., and Aanen, D.K. (2011) Comparative biology of fungus cultivation in termites and ants. In Biology of Termites: A Modern Synthesis. Bignell, D., Roisin, Y., and Lo, N. (eds). Dordrecht, The Netherlands: Springer, pp. 193-210.
47. Ohkuma, M. (2008) Symbioses of flagellates and prokaryotes in the gut of lower termites. Trends Microbiol 16: 345-352.
48. Otani, S., Mikaelyan, A., Nobre, T., Hansen, L.H., Koné, N.G.A., Sørensen, S.J., etal. (2014) Identifying the core microbial community in the gut of fungus-growing termites. Mol Ecol 23: 4631-4644.
49. Poulsen, M., Hu, H., Li, C., Chen, Z., Xu, L., Otani, S., etal. (2014) Complementary symbiont contributions to plant decomposition in a fungus-farming termite. Proc Natl Acad Sci USA 111: 14500-14505.
50. Rohrmann, G. (1978) The origin, structure, and nutritional importance of the comb in two species of Macrotermitinae. Pedobiologia 18: 89-98.
51. Rouland, C., Civas, A., Renoux, J., and Petek, F. (1988) Purification and properties of cellulases from the termite Macrotermes mulleri (Termitidae, Macrotermitinae) and its symbiotic fungus Termitomyces sp. Comp Biochem Physiol 91: 449-458.
52. Rouland-Lefèvre, C. (2000) Symbiosis with fungi. In Termites: Evolution, Sociality, Symbioses, Ecology. Abe, T., Bignell, D.E., and Higashi, M. (eds). Dordrecht, The Netherlands: Kluwer Academic Publishers, pp. 289-306.
53. Rouland-Lefèvre, C., Lenoir, F., and Lepage, M. (1991) The role of the symbiotic fungus in the digestive metabolism of several species of fungus-growing termites. Comp Biochem Physiol A 99: 657-663.
54. Sands, W.A. (1960) The initiation of fungus comb construction in laboratory colonies of Ancistrotermes guineensis (Silvestri). Insect Soc 7: 251-259.
55. Sapp, J. (1994) Evolution by Association: A History of Symbiosis. Oxford, UK: Oxford University Press.
56. Sengupta, S., Ghosh, A.K., and Sengupta, S. (1991) Purification and characterisation of a β-glucosidase (cellobiase) from a mushroom Termitomyces clypeatus. Biochim Biophys Acta 1076: 215-220.
57. Shinzato, N., Muramatsu, M., Matsui, T., and Watanabe, Y. (2007) Phylogenetic analysis of the gut bacterial microflora of the fungus-growing termite Odontotermes formosanus. Biosci Biotechnol Biochem 71: 906-915.
58. Sieber, R., and Leuthold, R.H. (1981) Behavioural elements and their meaning in incipient laboratory colonies of the fungus-growing termite Macrotermes michaelseni (Isoptera: Macrotermitinae). Insect Soc 28: 371-382.
59. Sinha, N., and Sengupta, S. (1995) Simultaneous production of α-arabinofuranosidase and xylanase by Termitomyces clypeatus. World J Microbiol Biotechnol 11: 359-360.
60. Slaytor, M. (1992) Cellulose digestion in termites and cockroaches: what role do symbionts play? Comp Biochem Physiol B 103: 775-784.
61. Um, S., Fraimout, A., Sapountzis, S., Oh, D.-C., and Poulsen, M. (2013) The fungus-growing termite Macrotermes natalensis harbors bacillaene-producing Bacillus sp. that inhibit potentially antagonistic fungi. Sci Rep 3: 3250.
62. Van Horn, D.J., Garcia, J.R., Loker, E.S., Mitchell, K.R., Mkoji, G.M., Adema, C.M., and Takacs-Vesbach, C.D. (2012) Complex intestinal bacterial communities in three species of planorbid snails. J Mollus Stud 78: 74-80.
63. Veivers, P.C., Mühlemann, R., Slaytor, M., Leuthold, R.H., and Bignell, D.E. (1991) Digestion, diet and polyethism in two fungus-growing termites: Macrotermes subhyalinus Rambur and M.michaelseni Sjøstedt. J Insect Physiol 37: 675-682.
64. Visser, A.A., Ros, V.I., De Beer, Z.W., Debets, A.J., Hartog, E., Kuyper, T.W., etal. (2009) Levels of specificity of Xylaria species associated with fungus-growing termites: a phylogenetic approach. Mol Ecol 18: 553-567.
65. Visser, A.A., Kooij, P.W., Debets, A.J.M., Kuyper, T.W., and Aanen, D.K. (2011) Pseudoxylaria as stowaway of the fungus-growing termite nest: interaction asymmetry between Pseudoxylaria, Termitomyces and free-living relatives. Fung Ecol 4: 322-332.
66. Visser, A.A., Nobre, T.M., Currie, C.R., Aanen, D.K., and Poulsen, M. (2012) Exploring the potential for Actinobacteria as defensive symbionts in fungus-growing termites. Microb Ecol 63: 975-985.
67. Warnecke, F., Luginbühl, P., Ivanova, N., Ghassemian, M., Richardson, T.H., Stege, J.T., etal. (2007) Metagenomic and functional analysis of hindgut microbiota of a wood-feeding higher termite. Nature 450: 560-565.
68. Wood, T.G., and Sands, W.A. (1978) The role of termites in ecosystems. In Production Ecology of Ants and Termites. Brian, M.V. (ed.). Cambridge, UK: Cambridge University Press, pp. 245-292.
69. Wymelenberg, A.V., Gaskell, J., Mozuch, M., Sabat, G., Ralph, J., Skyba, O., etal. (2010) Comparative transcriptome and secretome analysis of wood decay fungi Postia placenta and Phanerochaete chrysosporium. Appl Environ Microbiol 76: 3599-3610.
70. Yang, T., Mo, J.C., and Cheng, J. (2004) Purification and some properties of cellulase from Odontotermes formosanus (Isoptera: Termitidae). Entomol Sin 11: 1-10.
71. Zhu, Y., Li, J., Liu, H., Yang, H., Xin, S., Zhao, F., etal. (2012) Phylogenetic analysis of the gut bacterial microflora of the fungus-growing termite Macrotermes barneyi. Afr J Microbiol Res 6: 2071-2078.