Multipartite symbioses in fungus-growing termites (Blattodea: Termitidae, Macrotermitinae) for the degradation of lignocellulose.
Farhan Ahmad, Gui-Ying Yang, Shi-You Liang, Qi-Huan Zhou, Hassan Ahmed Gaal, Jian-Chu Mo
Author Information
Farhan Ahmad: Ministry of Agriculture Key Lab of Molecular Biology of Crop Pathogens and Insect Pests, Institute of Insect Sciences, College of Agricultural and Biotechnology, Zhejiang University, Hangzhou, China. ORCID
Gui-Ying Yang: Ministry of Agriculture Key Lab of Molecular Biology of Crop Pathogens and Insect Pests, Institute of Insect Sciences, College of Agricultural and Biotechnology, Zhejiang University, Hangzhou, China.
Shi-You Liang: Ministry of Agriculture Key Lab of Molecular Biology of Crop Pathogens and Insect Pests, Institute of Insect Sciences, College of Agricultural and Biotechnology, Zhejiang University, Hangzhou, China.
Qi-Huan Zhou: Ministry of Agriculture Key Lab of Molecular Biology of Crop Pathogens and Insect Pests, Institute of Insect Sciences, College of Agricultural and Biotechnology, Zhejiang University, Hangzhou, China.
Hassan Ahmed Gaal: Ministry of Agriculture Key Lab of Molecular Biology of Crop Pathogens and Insect Pests, Institute of Insect Sciences, College of Agricultural and Biotechnology, Zhejiang University, Hangzhou, China.
Jian-Chu Mo: Ministry of Agriculture Key Lab of Molecular Biology of Crop Pathogens and Insect Pests, Institute of Insect Sciences, College of Agricultural and Biotechnology, Zhejiang University, Hangzhou, China. ORCID
Fungus-growing termites are among the most successful herbivorous animals and improve crop productivity and soil fertility. A range of symbiotic organisms can be found inside their nests. However, interactions of termites with these symbionts are poorly understood. This review provides detailed information on the role of multipartite symbioses (between termitophiles, termites, fungi, and bacteria) in fungus-growing termites for lignocellulose degradation. The specific functions of each component in the symbiotic system are also discussed. Based on previous studies, we argue that the enzymatic contribution from the host, fungus, and bacteria greatly facilitates the decomposition of complex polysaccharide plant materials. The host-termitophile interaction protects the termite nest from natural enemies and maintains the stability of the microenvironment inside the colony.
Aanen, D.K. (2006) As you reap, so shall you sow: Coupling of harvesting and inoculating stabilizes the mutualism between termites and fungi. Biology Letters, 2, 209-212.
Aanen, D.K. and Eggleton, P. (2005) Fungus-growing termites originated in African rain forest. Current Biology, 15, 851-855.
Aanen, D.K., Henrik, H., Debets, A.J., Kerstes, N.A., Hoekstra, R.F. and Boomsma, J.J. (2009) High symbiont relatedness stabilizes mutualistic cooperation in fungus-growing termites. Science, 326, 1103-1106.
Ahmad, F., Fouad, H., Liang, S., Hu, Y. and Mo, J.C. (2021) Termites and Chinese agricultural system: applications and advances in integrated termite management and chemical control. Insect Science, 28, 2-20.
Arantes, V., Jellison, J. and Goodell, B. (2012) Peculiarities of brown-rot fungi and biochemical Fenton reaction with regard to their potential as a model for bioprocessing biomass. Applied Microbiology and Biotechnology, 94, 323-338.
Auer, L., Lazuka, A., Sillam-Dussès, D., Miambi, E., O'Donohue, M. and Hernandez-Raquet, G. (2017) Uncovering the potential of termite gut microbiome for lignocellulose bioconversion in anaerobic batch bioreactors. Frontiers in Microbiology, 8, 2623.
Aylward, F.O., Suen, G., Biedermann, P.H., Adams, A.S., Scott, J.J., Malfatti, S.A. et al. (2014) Convergent bacterial microbiotas in the fungal agricultural systems of insects. mBio, 5, e02077-e02014.
Bagine, R.K., Brandl, R. and Kaib, M. (1994) Species delimitation in Macrotermes (Isoptera: Macrotermitidae): Evidence from epicuticular hydrocarbons, morphology, and ecology. Annals of the Entomological Society of America, 87, 498-506.
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. Biotechnology Biofuels, 6, 78.
Benndorf, R., Guo, H., Sommerwerk, E., Weigel, C., Garcia-Altares, M., Martin, K. et al. (2018) Natural products from Actinobacteria associated with fungus-growing termites. Antibiotics, 7, 83.
Benndorf, R., Schwitalla, J.W., Martin, K., de Beer, Z.W., Vollmers, J., Kaster, A.K. et al. (2020) Nocardia macrotermitis sp. nov. and Nocardia aurantia sp. nov., isolated from the gut of the fungus-growing termite Macrotermes natalensis. International Journal of Systematic and Evolutionary Microbiology, ijsem004398.
Boga, H.I., Ji, R., Ludwig, W. and Brune, A. (2007) Sporotalea propionica gen. nov. sp. nov., a hydrogen-oxidizing, oxygen-reducing, propionigenic firmicute from the intestinal tract of a soil-feeding termite. Archives of Microbiology, 187, 15-27.
Bonachela, J.A., Pringle, R.M., Sheffer, E., Coverdale, T.C., Guyton, J.A., Caylor, K.K. et al. (2015) Termite mounds can increase the robustness of dryland ecosystems to climatic change. Science, 347, 651-655.
Boone, C.K., Keefover-Ring, K., Mapes, A.C., Adams, A.S., Bohlmann, J. and Raffa, K.F. (2013) Bacteria associated with a tree-killing insect reduce concentrations of plant defense compounds. Journal of Chemical Ecology, 39, 1003-1006.
Bourguignon, T., Lo, N., Cameron, S.L., Šobotník, J., Hayashi, Y., Shigenobu, S. et al. (2014) The evolutionary history of termites as inferred from 66 mitochondrial genomes. Molecular Biology and Evolution, 32, 406-421.
Bourguignon, T., Lo, N., Dietrich, C., Šobotník, J., Sidek, S., Roisin, Y. et al. (2018) Rampant host switching shaped the termite gut microbiome. Current Biology, 28, 649-654.
Brauman, A., Majeed, M.Z., Buatois, B., Robert, A., Pablo, A.L. and Miambi, E. (2015) Nitrous oxide (N2O) emissions by termites: Does the feeding guild matter ? PLoS ONE, 10, e0144340.
Brune, A. (1998) Termite guts: The world's smallest bioreactors. Trends in Biotechnology, 16, 16-21.
Brune, A. (2014) Symbiotic digestion of lignocellulose in termite guts. Nature Reviews Microbiology, 12, 168.
Brune, A. (2018) Methanogens in the digestive tract of termites. (Endo)symbiotic Methanogenic Archaea (ed. J. Hackstein), pp. 81-101. Springer, Cham.
Brune, A. and Ohkuma, M. (2011) Role of the termite gut microbiota in symbiotic digestion. Biology of Termites: A Modern Synthesis (eds. D. Bignell, Y. Roisin & N. Lo), pp. 439-475. Springer, Dordrecht.
Cai, C., Huang, D., Newton, A.F., Eldredge, K.T. and Engel, M.S. (2017) Early evolution of specialized termitophily in Cretaceous rove beetles. Current Biology, 27, 1229-1235.
Carrijo, T., Gonçalves, R. and Santos, R. (2012) Review of bees as guests in termite nests, with a new record of the communal bee, Gaesochira obscura (Smith, 1879) (Hymenoptera, Apidae), in nests of Anoplotermes banksi Emerson, 1925 (Isoptera, Termitidae, Apicotermitinae). Insectes Sociaux, 59, 141-149.
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. Proceedings of the Royal Society B: Biological Sciences, 280, 20131885.
Costa, C. and Vanin, S.A. (2010) Coleoptera larval fauna associated with termite nests (Isoptera) with emphasis on the “bioluminescent termite nests” from Central Brazil. Psyche: A Journal of Entomology, 2010, 12.
Coy, M., Salem, T., Denton, J., Kovaleva, E., Liu, Z., Barber, D. et al. (2010) Phenol-oxidizing laccases from the termite gut. Insect Biochemistry and Molecular Biology, 40, 723-732.
Cremer, S., Pull, C.D. and Fuerst, M.A. (2018) Social immunity: Emergence and evolution of colony-level disease protection. Annual Review of Entomology, 63, 105-123.
Cristaldo, P., Rosa, C., Florencio, D., Marins, A. and DeSouza, O. (2012) Termitarium volume as a determinant of invasion by obligatory termitophiles and inquilines in the nests of Constrictotermes cyphergaster (Termitidae, Nasutitermitinae). Insectes Sociaux, 59, 541-548.
da Costa, R.R. and Poulsen, M. (2018) Mixed-mode transmission shapes termite gut community assemblies. Trends in Microbiology, 26, 557-559.
da Costa, R.R., Hu, H., Li, H. and Poulsen, M. (2019) Symbiotic plant biomass decomposition in fungus-growing termites. Insects, 10, 87.
da Costa, R.R., Hu, H., Pilgaard, B., Vreeburg, S.M., Schückel, J., Pedersen, K.S. et al. (2018) Enzyme activities at different stages of plant biomass decomposition in three species of fungus-growing termites. Applied and Environmental Microbiology, 84, e01815-e01817.
da Cunha, H.F. and Morais, P.P.A.M. (2010) Relação espécie-área em cupinzeiros de pastagem, Goiânia-GO, Brasil. EntomoBrasilis, 3, 60-63.
Darlington, J. (2012) Termites (Isoptera) as secondary occupants in mounds of Macrotermes michaelseni (Sjöstedt) in Kenya. Insectes Sociaux, 59, 159-165.
DeVisser, S.N., Freymann, B.P. and Schnyder, H. (2008) Trophic interactions among invertebrates in termitaria in the African savanna: A stable isotope approach. Ecological Entomology, 33, 758-764.
Diehl, E., Junqueira, L. and Berti-Filho, E. (2005) Ant and termite mound coinhabitants in the wetlands of Santo Antonio da Patrulha, Rio Grande do Sul, Brazil. Brazilian Journal of Biology, 65, 431-437.
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. Applied and Environmental Microbiology, 80, 2261-2269.
Du, X., Li, X., Wang, Y., Peng, J., Hong, H. and Yang, H. (2012) Phylogenetic diversity of nitrogen fixation genes in the intestinal tract of Reticulitermes chinensis Snyder. Current Microbiology, 65, 547-551.
Eggleton, P. (2011) An introduction to termites: Biology, taxonomy and functional morphology. Biology of Termites: A Modern Synthesis (eds. D. Bignell, Y. Roisin & N. Lo), pp. 1-26. Springer, Dordrecht.
Erens, H., Mujinya, B.B., Mees, F., Baert, G., Boeckx, P., Malaisse, F. et al. (2015) The origin and implications of variations in soil-related properties within Macrotermes falciger mounds. Geoderma, 249, 40-50.
Evans, T.A., Dawes, T.Z., Ward, P.R. and Lo, N. (2011) Ants and termites increase crop yield in a dry climate. Nature Communications, 2, 262.
Floudas, D., Binder, M., Riley, R., Barry, K., Blanchette, R.A., Henrissat, B. et al. (2012) The Paleozoic origin of enzymatic lignin decomposition reconstructed from 31 fungal genomes. Science, 336, 1715-1719.
Grassé, P.P. and Noirot, C. (1955) La fondation de nouvelles sociétés par Bellicositermes natalensis Hav. Insectes Sociaux, 2, 213-220.
Cranston, P.J.G. (2010) The Insects: An Outline of Entomology/Penny J. Gullan, Peter S. Cranston. London, U.K: Chapman and Hall.
Hammel, K.E. and Cullen, D. (2008) Role of fungal peroxidases in biological ligninolysis. Current Opinion in Plant Biology, 11, 349-355.
Hansen, A.K. and Moran, N.A. (2011) Aphid genome expression reveals host-symbiont cooperation in the production of amino acids. Proceedings of the National Academy of Sciences USA, 108, 2849-2854.
Hansen, A.K. and Moran, N.A. (2014) The impact of microbial symbionts on host plant utilization by herbivorous insects. Molecular Ecology, 23, 1473-1496.
Hata, H. and Kato, M. (2006) A novel obligate cultivation mutualism between damselfish and Polysiphonia algae. Biology Letters, 2, 593-596.
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.
Helms, K.R. and Vinson, S.B. (2002) Widespread association of the invasive ant Solenopsis invicta with an invasive mealybug. Ecology, 83, 2425-2438.
Henrik, H., Boomsma, J.J. and Tunlid, A. (2014) Symbiotic adaptations in the fungal cultivar of leaf-cutting ants. Nature Communications, 5, 5675.
Hongoh, Y. (2011) Toward the functional analysis of uncultivable, symbiotic microorganisms in the termite gut. Cellular and Molecular Life Sciences, 68, 1311-1325.
Hongoh, Y. and Ohkuma, M. (2018) Termite gut flagellates and their methanogenic and eubacterial symbionts. (Endo)symbiotic Methanogenic Archaea (ed. J. Hackstein), pp. 55-80. Springer, Cham.
Hu, H., da Costa, R.R., Pilgaard, B., Schiøtt, M., Lange, L. and Poulsen, M. (2019) Fungiculture in termites is associated with a mycolytic gut bacterial community. Msphere, 4, e00165-e00119.
Izawa, K., Kuwahara, H., Kihara, K., Yuki, M., Lo, N., Itoh, T. et al. (2016) Comparison of intracellular “Ca. Endomicrobium trichonymphae” genomovars illuminates the requirement and decay of defense systems against foreign DNA. Genome Biology and Evolution, 8, 3099-3107.
Ji, R. and Brune, A. (2005) Digestion of peptidic residues in humic substances by an alkali-stable and humic-acid-tolerant proteolytic activity in the gut of soil-feeding termites. Soil Biology and Biochemistry, 37, 1648-1655.
Jiang, S., Li, J., Cao, C., Shen, Y. and Ni, J. (2018) Molecular modification of β-glucosidase from the midgut of Macrotermes barneyi. Chinese Journal of Biotechnology, 34, 1081-1090.
Joseph, G.S., Seymour, C.L., Cumming, G.S., Cumming, D.H. and Mahlangu, Z. (2013) Termite mounds as islands: Woody plant assemblages relative to termitarium size and soil properties. Journal of Vegetation Science, 24, 702-711.
Jouquet, P., Traoré, S., Choosai, C., Hartmann, C. and Bignell, D. (2011) Influence of termites on ecosystem functioning. Ecosystem services provided by termites. European Journal of Soil Biology, 47, 215-222.
Kanzaki, N., Liang, W.R., Chiu, C.I., Yang, C.T., Hsueh, Y.P. and Li, H.F. (2019) Nematode-free agricultural system of a fungus-growing termite. Scientific Reports, 9, 8917.
Ke, J., Singh, D. and Chen, S. (2011) Aromatic compound degradation by the wood-feeding termiteCoptotermes formosanus (Shiraki). International Biodeterioration & Biodegradation, 65, 744-756.
Ke, J., Sun, J.Z., Nguyen, H.D., Singh, D., Lee, K.C., Beyenal, H. et al. (2010) In situ oxygen profiling and lignin modification in guts of wood-feeding termites. Insect Science, 17, 277-290.
Khadempour, L. (2018) Microbial mediation of herbivory in leaf-cutter ant fungus gardens. The University of Wisconsin-Madison. https://search.proquest.com/openview/ead8a61a1ff379109d9b1e609cb8d4de/1?pq-origsite=gscholar&cbl=18750&diss=y.
Khadempour, L., Burnum-Johnson, K.E., Baker, E.S., Nicora, C.D., Webb-Robertson, B.J.M., White III, R.A. et al. (2016) The fungal cultivar of leaf-cutter ants produces specific enzymes in response to different plant substrates. Molecular Ecology, 25, 5795-5805.
Kistner, D.H. (1990) The integration of foreign insects into termite societies or why do termites tolerate foreign insects in their societies? Sociobiology, (USA).
Kitade, O. (2004) Comparison of symbiotic flagellate faunae between termites and a wood-feeding cockroach of the genus Cryptocercus. Microbes and Environments, 19, 215-220.
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.). Applied and Environmental Microbiology, 78, 4691-4701.
Köhler, T., Stingl, U., Meuser, K. and Brune, A. (2008) Novel lineages of Planctomycetes densely colonize the alkaline gut of soil-feeding termites (Cubitermes spp.). Environmental Microbiology, 10, 1260-1270.
Korb, J. (2003) Thermoregulation and ventilation of termite mounds. Naturwissenschaften, 90, 212-219.
Korb, J. and Aanen, D.K. (2003) The evolution of uniparental transmission of fungal symbionts in fungus-growing termites (Macrotermitinae). Behavioral Ecology and Sociobiology, 53, 65-71.
Krikken, J. (2008) Blind, flightless termitophiles of the genus Termitotrox in East Africa: Three new species with a generic review (Coleoptera: Scarabaeidae: Termitotroginae). Tijdschrift Voor Entomologie, 151, 65-75.
Leuthold, R., Badertscher, S. and Imboden, H. (1989) The inoculation of newly formed fungus comb with Termitomyces inMacrotermes colonies (Isoptera, Macrotermitinae). Insectes Sociaux, 36, 328-338.
Li, H., Dietrich, C., Zhu, N., Mikaelyan, A., Ma, B., Pi, R.et al. (2016) Age polyethism drives community structure of the bacterial gut microbiota in the fungus-cultivating termite Odontotermes formosanus. Environmental Microbiology, 18, 1440-1451.
Li, H., Lu, J. and Mo, J.C. (2012a) Physiochemical lignocellulose modification in the formosan subterranean termite Coptotermes formosanus Shiraki (Isoptera: Rhinotermitidae) and potential uses in the production of biofuels. BioResources, 7. https://doi.org/10.15376/biores.7.1.0675-0685.
Li, H., Sun, J., Zhao, J., Deng, T., Lu, J., Dong, Y. et al. (2012b) Physicochemical conditions and metal ion profiles in the gut of the fungus-growing termite Odontotermes formosanus. Journal of Insect Physiology, 58, 1368-1375.
Li, H., Yelle, D.J., Li, C., Yang, M., Ke, J., Zhang, R.et al. (2017) Lignocellulose pretreatment in a fungus-cultivating termite. Proceedings of the National Academy of Sciences USA, 114, 4709-4714.
Liang, S., Wang, C., Ahmad, F., Yin, X., Hu, Y. and Mo, J.C. (2020) Exploring the effect of plant substrates on bacterial community structure in termite fungus-combs. PLoS ONE, 15, e0232329.
Liu, L., Zhao, X.Y., Tang, Q.B., Lei, C.L. and Huang, Q.Y. (2019a) The mechanisms of social immunity against fungal infections in eusocial insects. Toxins, 11, 244.
Liu, N., Li, H., Chevrette, M.G., Zhang, L., Cao, L., Zhou, H.et al. (2019b) Functional metagenomics reveals abundant polysaccharide-degrading gene clusters and cellobiose utilization pathways within gut microbiota of a wood-feeding higher termite. The ISME Journal, 13, 104.
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.
Lo, N. and Eggleton, P. (2010) Termite phylogenetics and co-cladogenesis with symbionts. Biology of Termites: A Modern Synthesis (eds. D.Bignell, Y. Roisin & N. Lo), pp. 27-50. Springer, Dordrecht.
Long, Y.H., Xie, L., Liu, N., Yan, X., Li, M.H., Fan, M.Z. et al. (2010) Comparison of gut-associated and nest-associated microbial communities of a fungus-growing termite (Odontotermes yunnanensis). Insect Science, 17, 265-276.
Lucey, K.S. and Leadbetter, J.R. (2014) Catechol 2, 3-dioxygenase and other meta-cleavage catabolic pathway genes in the ‘anaerobic'termite gut spirochete Treponema primitia. Molecular Ecology, 23, 1531-1543.
Makonde, H.M., Boga, H.I., Osiemo, Z., Mwirichia, R., Stielow, J.B., Göker, M. et al. (2013) Diversity of Termitomyces associated with fungus-farming termites assessed by cultural and culture-independent methods. PLoS ONE, 8, e56464.
Marins, A., Costa, D., Russo, L., Campbell, C., Desouza, O., Bjørnstad, O.N. et al. (2016) Termite cohabitation: The relative effect of biotic and abiotic factors on mound biodiversity. Ecological Entomology, 41, 532-541.
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.
Martin, M.M. and Martin, J.S. (1979) The distribution and origins of the cellulolytic enzymes of the higher termite, Macrotermes natalensis. Physiological Zoology, 52, 11-21.
Mathew, G.M., Ju, Y.M., Lai, C.Y., Mathew, D.C. and Huang, C.C. (2012) Microbial community analysis in the termite gut and fungus comb of Odontotermes formosanus: The implication of Bacillus as mutualists. FEMS Microbiology Ecology, 79, 504-517.
Mathews, A.A. (1977) Studies on Termites from the Mato Grosso state, Brazil. Academia brasileira de Ciências Rio de Janeiro. https://www.worldcat.org/title/studies-on-termites-from-the-mato-grosso-state-brazil/oclc/4595010.
Mattéotti, C., Thonart, P., Francis, F., Haubruge, E., Destain, J., Brasseur, C.et al. (2011) New glucosidase activities identified by functional screening of a genomic DNA library from the gut microbiota of the termite Reticulitermes santonensis. Microbiological Research, 166, 629-642.
Mattila, H.K., Mäkinen, M. and Lundell, T. (2020) Hypoxia is regulating enzymatic wood decomposition and intracellular carbohydrate metabolism in filamentous white rot fungus. Biotechnology Biofuels, 13, 1-17.
Maurice, N. and Erdei, L. (2018) Termite gut microbiome. Termites and Sustainable Management (eds. M. Khan & W. Ahmad), pp. 69-99. Springer, Cham.
Mo, J., Yang, T., Song, X. and Cheng, J. (2004) Cellulase activity in five species of important termites in China. Applied Entomology and Zoology, 39, 635-641.
Monteiro, I., Viana-Junior, A.B., de Castro Solar, R.R., de Siqueira Neves, F. and DeSouza, O. (2017) Disturbance-modulated symbioses in termitophily. Ecology and Evolution, 7, 10829-10838.
Mueller, U.G. and Gerardo, N. (2002) Fungus-farming insects: Multiple origins and diverse evolutionary histories. Proceedings of the National Academy of Sciences USA, 99, 15247-15249.
Mueller, U.G., Gerardo, N.M., Aanen, D.K., Six, D.L. and Schultz, T.R. (2005) The evolution of agriculture in insects. Annual Review of Ecology, Evolution, and Systematics, 36, 563-595.
Ni, J. and Tokuda, G. (2013) Lignocellulose-degrading enzymes from termites and their symbiotic microbiota. Biotechnology Advances, 31, 838-850.
Ni, J., Wu, Y., Yun, C., Yu, M. and Shen, Y. (2014) cDNA cloning and heterologous expression of an endo-β-1,4-glucanase from the fungus-growing termite Macrotermes barneyi. Archives of Insect Biochemistry and Physiology, 86, 151-164.
Nobre, T. and Aanen, D.K. (2012) Fungiculture or termite husbandry? The ruminant hypothesis. Insects, 3, 307-323.
Nobre, T., Eggleton, P. and Aanen, D. (2009) Vertical transmission as the key to the colonization of Madagascar by fungus-growing termites? Proceedings of the Royal Society B: Biological Sciences, 277, 359-365.
Noda, S., Shimizu, D., Yuki, M., Kitade, O. and Ohkuma, M. (2018) Host-symbiont cospeciation of termite-gut cellulolytic protists of the genera Teranympha and Eucomonympha and their Treponema endosymbionts. Microbes and Environments, 33, 26-33.
Ohkuma, M. (2003) Termite symbiotic systems: Efficient bio-recycling of lignocellulose. Applied Microbiology and Biotechnology, 61, 1-9.
Ohkuma, M., Noda, S. and Kudo, T. (1999) Phylogenetic diversity of nitrogen fixation genes in the symbiotic microbial community in the gut of diverse termites. Applied and Environmental Microbiology, 65, 4926-4934.
Osiemo, Z., Marten, A., Kaib, M., Gitonga, L., Boga, H. and Brandl, R. (2010) Open relationships in the castles of clay: High diversity and low host specificity of Termitomyces fungi associated with fungus-growing termites in Africa. Insectes Sociaux, 57, 351-363.
Otani, S., Hansen, L.H., Sørensen, S.J. and Poulsen, M. (2016) Bacterial communities in termite fungus combs are comprised of consistent gut deposits and contributions from the environment. Microbial Ecology, 71, 207-220.
Otani, S., Mikaelyan, A., Nobre, T., Hansen, L.H., Koné, N.G.A., Sørensen, S.J.et al. (2014) Identifying the core microbial community in the gut of fungus-growing termites. Molecular Ecology, 23, 4631-4644.
Otani, S., Zhukova, M., Koné, N.G.A., da Costa, R.R., Mikaelyan, A., Sapountzis, P. et al. (2019) Gut microbial compositions mirror caste-specific diets in a major lineage of social insects. Environmental Microbiology Reports, 11, 196-205.
Paul, K., Nonoh, J.O., Mikulski, L. and Brune, A. (2012) “Methanoplasmatales,” Thermoplasmatales-related archaea in termite guts and other environments, are the seventh order of methanogens. Applied and Environmental Microbiology, 78, 8245-8253.
Pennisi, E. (2015) Africa's soil engineers: Termites. Science, 347, 596-597.
Pester, M. and Brune, A. (2007) Hydrogen is the central free intermediate during lignocellulose degradation by termite gut symbionts. The ISME Journal, 1, 551-565.
Pisno, R.M., Salazar, K., Lino-Neto, J., Serrão, J.E. and DeSouza, O. (2019) Termitariophily: Expanding the concept of termitophily in a physogastric rove beetle (Coleoptera: Staphylinidae). Ecological Entomology, 44, 305-314.
Poulsen, M. (2015) Towards an integrated understanding of the consequences of fungus domestication on the fungus-growing termite gut microbiota. Environmental Microbiology, 17, 2562-2572.
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. Proceedings of the National Academy of Sciences USA, 111, 14500-14505.
Presley, G.N., Panisko, E., Purvine, S.O. and Schilling, J.S. (2018) Coupling secretomics with enzyme activities to compare the temporal processes of wood metabolism among white and brown rot fungi. Applied and Environmental Microbiology, 84, e00159-e00118.
Quinet, Y., Tekule, N. and De Biseau, J. (2005) Behavioural interactions between Crematogaster brevispinosa rochai Forel (Hymenoptera: Formicidae) and two Nasutitermes species (Isoptera: Termitidae). Journal of Insect Behavior, 18, 1-17. https://doi.org/10.1007/s10905-005-9343-y.
Rahman, N.A., Parks, D.H., Vanwonterghem, I., Morrison, M., Tyson, G.W. and Hugenholtz, P. (2016) A phylogenomic analysis of the bacterial phylum Fibrobacteres. Frontiers in Microbiology, 6, 1469.
Rahman, N.A., Parks, D.H., Willner, D.L., Engelbrektson, A.L., Goffredi, S.K., Warnecke, F.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.
Rashamuse, K., Ronneburg, T., Sanyika, W., Mathiba, K., Mmutlane, E. and Brady, D. (2014) Metagenomic mining of feruloyl esterases from termite enteric flora. Applied Microbiology and Biotechnology, 98, 727-737.
Roberts, E.M., Todd, C.N., Aanen, D.K., Nobre, T., Hilbert-Wolf, H.L., O'Connor, P.M.et al. (2016) Oligocene termite nests with in situ fungus gardens from the Rukwa Rift Basin, Tanzania, support a Paleogene African origin for insect agriculture. PloS ONE, 11, e0156847.
Rouland, C., Civas, A., Renoux, J. and Petek, F. (1988) Purification and properties of cellulases from the termite Macrotermes mülleri (Termitidae, Macrotermitinae) and its symbiotic fungus Termitomyces sp. Comparative Biochemistry and Physiology Part B: Comparative Biochemistry, 91, 449-458.
Rouland-Lefèvre, C. (2000) Symbiosis with fungi. Termites: Evolution, Sociality, Symbioses, Ecology (eds. T. Abe, D.E. Bignell & M. Higashi), pp. 289-306. Springer, Dordrecht.
Rouland-Lefèvre, C. and Bignell, D.E. (2001) Cultivation of symbiotic fungi by termites of the subfamily. Macrotermitinae. Symbiosis (ed. J. Seckbach), pp. 731-756. Springer, Dordrecht.
Santos, P.P., Vasconcellos, A., Jahyny, B. and Delabie, J.H.C. (2010) Ant fauna (Hymenoptera, Formicidae) associated to arboreal nests of Nasutitermes spp. (Isoptera, Termitidae) in a cacao plantation in southeastern Bahia, Brazil. Revista Brasileira de Entomologia, 54, 450-454.
Sapountzis, P., De Verges, J., Rousk, K., Cilliers, M., Vorster, B.J. and Poulsen, M. (2016) Potential for nitrogen fixation in the fungus-growing termite symbiosis. Frontiers in Microbiology, 7, 1993.
Sato, T., Kuwahara, H., Fujita, K., Noda, S., Kihara, K., Yamada, A. et al. (2014) Intranuclear verrucomicrobial symbionts and evidence of lateral gene transfer to the host protist in the termite gut. The ISME Journal, 8, 1008-1019.
Schnorr, S.L., Hofman, C.A., Netshifhefhe, S.R., Duncan, F.D., Honap, T.P., Lesnik, J. et al. (2019) Taxonomic features and comparisons of the gut microbiome from two edible fungus-farming termites (Macrotermes falciger; M. natalensis) harvested in the Vhembe district of Limpopo, South Africa. BMC microbiology, 19, 164.
Shi, Y., Huang, Z., Han, S., Fan, S. and Yang, H. (2015) Phylogenetic diversity of Archaea in the intestinal tract of termites from different lineages. Journal of Basic Microbiology, 55, 1021-1028.
Shimada, K. and Maekawa, K. (2014) Gene expression and molecular phylogenetic analyses of beta-glucosidase in the termiteReticulitermes speratus (Isoptera: Rhinotermitidae). Journal of Insect Physiology, 65, 63-69.
Shinzato, N., Muramatsu, M., Matsui, T. and Watanabe, Y. (2007) Phylogenetic analysis of the gut bacterial microflora of the fungus-growing termite Odontotermes formosanus. Bioscience, Biotechnology, and Biochemistry, 71, 906-915.
Slaytor, M. (2000) Energy metabolism in the termite and its gut microbiota. Termites: Evolution, Sociality, Symbioses, Ecology (eds. T. Abe, D.E. Bignell & M. Higashi), pp. 307-332. Springer, Dordrecht.
Suman, S.K., Dhawaria, M., Tripathi, D., Raturi, V., Adhikari, D.K. and Kanaujia, P.K. (2016) Investigation of lignin biodegradation by Trabulsiella sp. isolated from termite gut. International Biodeterioration & Biodegradation, 112, 12-17.
Tamschick, S. and Radek, R. (2013) Colonization of termite hindgut walls by oxymonad flagellates and prokaryotes in Incisitermes tabogae, I. marginipennis and Reticulitermes flavipes. European Journal of Protistology, 49, 1-14.
Thauer, R.K., Kaster, A.K., Seedorf, H., Buckel, W. and Hedderich, R. (2008) Methanogenic archaea: Ecologically relevant differences in energy conservation. Nature Reviews Microbiology, 6, 579-591.
Tholen, A. and Brune, A. (2000) Impact of oxygen on metabolic fluxes and in situ rates of reductive acetogenesis in the hindgut of the wood-feeding termite Reticulitermes flavipes. Environmental Microbiology, 2, 436-449.
Tholen, A., Pester, M. and Brune, A. (2007) Simultaneous methanogenesis and oxygen reduction byMethanobrevibacter cuticularis at low oxygen fluxes. FEMS Microbiology Ecology, 62, 303-312.
Tokuda, G., Lo, N., Watanabe, H., Arakawa, G., Matsumoto, T. and Noda, H. (2004) Major alteration of the expression site of endogenous cellulases in members of an apical termite lineage. Molecular Ecology, 13, 3219-3228.
Tokuda, G., Mikaelyan, A., Fukui, C., Matsuura, Y., Watanabe, H., Fujishima, M. et al. (2018) Fiber-associated spirochetes are major agents of hemicellulose degradation in the hindgut of wood-feeding higher termites. Proceedings of the National Academy of Sciences USA, 115, 11996-12004.
Tokuda, G., Watanabe, H., Hojo, M., Fujita, A., Makiya, H., Miyagi, M.et al. (2012) Cellulolytic environment in the midgut of the wood-feeding higher termite Nasutitermes takasagoensis. Journal of Insect Physiology, 58, 147-154.
Traoré, S., Tigabu, M., Jouquet, P., Ouédraogo, S.J., Guinko, S. and Lepage, M. (2015) Long-term effects of Macrotermes termites, herbivores and annual early fire on woody undergrowth community in Sudanian woodland, Burkina Faso. Flora-Morphology Distribution Functional Ecology of Plants, 211, 40-50.
Um, S., Fraimout, A., Sapountzis, P., Oh, D.-C. and Poulsen, M. (2013) The fungus-growing termite Macrotermes natalensis harbors bacillaene-producing Bacillus sp. that inhibit potentially antagonistic fungi. Scientific Reports, 3, 3250.
Vecherskii, M.V., Kostina, N.V., Gorlenko, M.V., Dobrovol'skaya, T.G. and Umarov, M.M. (2008) Specific features of nitrogen fixation in the termite Reticulitermes lucifugus. Biology Bulletin, 35, 446-451.
Veivers, P., Mühlemann, R., Slaytor, M., Leuthold, R. and Bignell, D. (1991) Digestion, diet and polyethism in two fungus-growing termites: Macrotermes subhyalinus Rambur and M. michaelseni Sjøstedt. Journal of Insect Physiology, 37, 675-682.
Vesala, R., Arppe, L. and Rikkinen, J. (2019) Caste-specific nutritional differences define carbon and nitrogen fluxes within symbiotic food webs in African termite mounds. Scientific Reports, 9, 1-11.
Wang, Y., Lim, L., DiGuistini, S., Robertson, G., Bohlmann, J. and Breuil, C. (2013) A specialized ABC efflux transporter GcABC-G1 confers monoterpene resistance to Grosmannia clavigera, a bark beetle-associated fungal pathogen of pine trees. New Phytologist, 197, 886-898.
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.
Wei, H., Donohoe, B.S., Vinzant, T.B., Ciesielski, P.N., Wang, W., Gedvilas, L.M. et al. (2011) Elucidating the role of ferrous ion cocatalyst in enhancing dilute acid pretreatment of lignocellulosic biomass. Biotechnology Biofuels, 4, 48.
Wertz, J.T., Kim, E., Breznak, J.A., Schmidt, T.M. and Rodrigues, J.L. (2012) Genomic and physiological characterization of the Verrucomicrobia isolate Diplosphaera colitermitum gen. nov., sp. nov., reveals microaerophily and nitrogen fixation genes. Applied and Environmental Microbiology, 78, 1544-1555.
Wu, Y., Chi, S., Yun, C., Shen, Y., Tokuda, G. and Ni, J. (2012) Molecular cloning and characterization of an endogenous digestive β-glucosidase from the midgut of the fungus-growing termite Macrotermes barneyi. Insect Molecular Biology, 21, 604-614.
Yanagawa, A., Yokohari, F. and Shimizu, S. (2008) Defense mechanism of the termite, Coptotermes formosanus Shiraki, to entomopathogenic fungi. Journal of Invertebrate Pathology, 97, 165-170.
Yang, G., Ahmad, F., Liang, S., Fouad, H., Guo, M. and Gaal, H.A. (2020) Termitomyces heimii associated with fungus-growing termite produces volatile organic compounds (VOCs) and lignocellulose-degrading enzymes. Applied Biochemistry and Biotechnology, 192, 1270-1283.
Zhang, M., Liu, N., Qian, C., Wang, Q., Wang, Q., Long, Y. 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 β-glucosidase genes. Microbial Ecology, 68, 416-425.
Grants
31770686/National Natural Science Foundation of China
