TERMITE GUT: HOME TO MICROBIOME

Main Article Content

AMIT KUMAR
ASHA POONIA
RADHIKA SHARMA
MONIKA JANGRA
RAKESH SEHRAWAT
REKHA SANSANWAL

Abstract

Present manuscript reviews of microbial diversities present in termites’ gut. Microbial communities are the essential players of the termite gut due to several benefits arising from them which are useful for their host survival. The termites gut consists of one to several compartments, which harbor predominantly bacteria, protists (only in lower termites), some archaeal species (methanogenic or nonmethanogenic lineages), few species of fungi and bacteriophages which live in mutualistic relationship and provide nutrition by degrading the tough plant biomass. These microbiomes convert the cellulose/hemicellulose into long chain fatty acid to be later converted into short chain fatty acid which is finally absorbed by termites. Digestive enzymes such as carbohydrate active enzymes (CAZymes), proteases, lysozymes, chitinases, peroxidases amongst others play essential role in termites’ gut for converting the cellulose or other plant parts into nutrients. Environmental biotic factors, abiotic factors and diet also affect the physicochemical condition of gut compartments and the diversity of microbes in their gut. Supply of methanogenic substrates decides the archaeal diversities in the gut. First part of the review provides details of termite gut compartments and enzymes involved while the later part enlists the microbiome which makes termites “ecosystem engineers”. Lot of research is going on based on metagenome- assembled genomes for termite gut microbiota. Since, most of such studies reveal higher ranks such as phylum, class etc. only. Present manuscript is the first attempt to enlist all species of microbes obtained from termite gut and reviews present research and future prospects of this research.

 

Keywords:
Termites, termite gut, microbiome, isopteran, protists, termite gut enzymes, archaea, gut bacteria, gut archaea, methanogenic bacteria, chitinases, gut environment, gut pH, gut protists, insect gut.

Article Details

How to Cite
KUMAR, A., POONIA, A., SHARMA, R., JANGRA, M., SEHRAWAT, R., & SANSANWAL, R. (2020). TERMITE GUT: HOME TO MICROBIOME. UTTAR PRADESH JOURNAL OF ZOOLOGY, 41(22), 9-23. Retrieved from https://mbimph.com/index.php/UPJOZ/article/view/1750
Section
Review Article

References

Krishna K, Grimaldi DA, Engel MS. Treatise on the isoptera of the world: Vol. 1. Bull Am Museum Nat Hist. 2013;377:1–196.

Aanen DK, Eggleton P. Fungus-growing termites originated in African rain forest. Curr Biol. 2005;15:851–855.

Poonia A. Termites (Insecta: Isoptera) of Haryana present state of knowledge- A review. Agricultural Reviews. 2019;40(1):59-64.

Hongoh Y. Toward the functional analysis of uncultivable, symbiotic microorganisms in the termite gut. Cell Mol Life Sci. 2011;68:1311–1325.

Ebert A, Brune A. Hydrogen concentration profiles at the oxic-anoxic interface: A microsensor study of the hindgut of the wood-feeding lower termite Reticulitermes flavipes (Kollar). Appl. Environ. Microbiol. 1997;63:4039–4046.

Brune A, Emerson, Breznak JA. The termite gut microflora as an oxygen sink: Microelectrode determination of oxygen and pH gradients in guts of lower and higher termites. Appl. Environ. Microbiol. 1995;61:2681-2687.

Brune A, Kuhl M. pH profiles of the extremely alkaline hindguts of soil-feeding termites (Isoptera: Termitidae) determined with microelectrodes. J. Insect Physiol. 1996;42:1121-1127.

Kohler T, Dietrich C, Scheffrahn RH, Brune A. 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. 2012;78:4691–4701.

Schauer C, Thompson CL, Brune A. The bacterial community in the gut of the cockroach Shelfordella lateralis reflects the close evolutionary relatedness of cockroaches and termites. Appl. Environ. Microbiol. 2012;78:2758–67.

Radek R, Strassert JFH, Kruger J, Meuser K, Scheffrahn RH, Brune A. Phylogeny and ultrastructure of Oxymonas jouteli, a rostellum-free species, and Opisthomitus longiflagellatus sp. nov., oxymonadid flagellates from the gut of Neotermes jouteli. Protist. 2014;165:384–99.

Brune A, Dietrich C. The gut microbiota of termites: Digesting the diversity in the light of ecology and evolution. Annu. Rev. Microbiol. 2015;69:145–166.

Tokuda G, Tsuboi Y, Kihara K, Saitou S, Moriya S, Lo N, Kikuchi J. Metabolomic profiling of 13C-labelled cellulose digestion in a lower termite: Insights into gut symbiont function. Proc. R. Soc. B. 2014;281:20140990.

Breznak JA. Ecology of prokaryotic microbes in the guts of wood- and litter-feeding termites. Termites: Evolution, Sociality, Symbioses, Ecology. 2000;209–231.

Brune A. Symbiotic associations between termites and prokaryotes. The Prokaryotes. 2013;545–577.

Dexter SV, Boopathy R. Biodegradation of phenol by Acinetobacter tandoii isolated from the gut of the termite. Environmental Science and Pollution Research. 2019;26(33).

Hu H, Costa RRD, Pilgaard B, Schiøtt M, Lange L, Poulsen M. Fungiculture in termites is associated with a mycolytic gut bacterial community. 2019;4(3):e00165-19.

Wheeler MM, Tarver MR, Coy MR, Scharf ME. Characterization of four esterase genes and esterase activity from the gut of the termite Reticulitermes flavipes. Archives of Insect Biochemistry and Physiology. 2009;73(1):30–48.

Fujita A, Miura T, Matsumoto T. Differences in cellulose digestive systems among castes in two termites lineages. Physiol. Entomol. 2009;33:73–82.

Lima T de. A, Pontual EV, Dornelles LP, Amorim PK, Sá RA, Coelho LC, Napoleão TH, Paiva PM. Digestive enzymes from workers and soldiers of termite Nasutitermes corniger. Comp Biochem Physiol B Biochem Mol Biol. 2014;176:1-8.

Rouland C, Lenoir-Rousseaux JJ, Mora P, Renoux. Origin of the exo-cellulase and the β-glucosidase purified from the digestive tract of the fungus-growing termite Macrotermes muelleri. Sociobiology. 1989;15:237–246.

Inoue T, Moriya S, Ohkuma M, Kudo T. Molecular cloning and characterization of a cellulase gene from a symbiotic protist of the lower termite, Coptotermes formosanus. Gene. 2005;349:67–75.

Leadbetter JR, Schmidt TM, Graber JR, Breznak JA. Acetogenesis from H2 plus CO2 by spirochetes from termite guts. Science. 1999;283:686–9.

Boga HI, Brune A. Hydrogen-dependent oxygen reduction by homoacetogenic bacteria isolated from termite guts. Appl Environ Microbiol. 2003;69:779–786.

Graber JR, Leadbetter JR, Breznak JA. Description of Treponema azotonutricium sp. nov. and Treponema primitia sp. nov., the first spirochaetes isolated from termite guts. Appl Environ Microbiol. 2004;70:1315–1320.

Duarte S, Nunes L, Borges PAV, Fossdal CG, Nobre T. Living inside termites - an overview of symbiotic interactions, with emphasis on flagellate protists. Arquipélago Life and Marine Sciences. 2017;34:21-43.

Lespes C. Recherches sur l’organisation et les moeurs du termite Lucifuge. Annales des Sciences Naturelles, Zoologie. 1856;4:227–282.

Cleveland LR. The effects of oxygenation and starvation on the symbiosis between the termite, Termopsis and its intestinal flagellates. Biol Bull. 1925;48:309–327.

Cleveland LR. Symbiosis among animals with special reference to termites and their intestinal flagellates. Q. Rev. Biol. 1926;1:51–60.

Katzin LI, Kirby H. The relative weights of termites and their protozoa. J Parasitology. 1939;25:444–445.

Nalepa CA. Origin of mutualism between termites and flagellated gut protists: Transition from horizontal to vertical transmission. Frontiers in Ecology and Evolution. 2020;8.

Embley TM, Martin W. Eukaryotic evolution, changes and challenges. Nature. 2006;440:623–630.

Radek R, Meuser K, Altinay S, Lo N, Brune A. Novel lineages of oxymonad flagellates from the termite Porotermes adamsoni (Stolotermitidae): The Genera Oxynympha and Termitimonas. Protist. 2019;125683.

Bourguignon T, Lo N, Cameron SL, Šobotník J, Hayashi Y, Shigenobu S, Watanabe D, Roisin Y, Miura T, Evans TA. The evolutionary history of termites as inferred from 66 mitochondrial genomes. Mol Biol Evol. 2015;32(2):406-21.

Ohtsubo WI, Brune A. Cospeciation of termite gut flagellates and their bacterial endosymbionts: Trichonympha species and ‘Candidatus Endomicrobium trichonymphae’. Molecular Ecology. 2009;18:332–342.

Muller M. The hydrogenosome. J Gen Microbiol. 1993;139:2879–2889.

Hackstein JH, Akhmanova A, Voncken F, van Hoek A, van Alen T, Boxma B, Moon-van der Staay SY, van der Staay G, Leunissen J, Huynen M, Rosenberg J, Veenhuis M. Hydrogenosomes: Convergent adaptations of mitochondria to anaerobic environments. Zoology. 2001;104:290–302.

Husseneder C. Symbiosis in subterranean termites: A review of insights from molecular studies. Environmental Entomology. 2010;39(2):378–388.

Ohkuma M, Noda S, Hongoh Y, Nalepa CA, Inoue T. Inheritance and diversification of symbiotic trichonymphid flagellates from a common ancestor of termites and the cockroach Cryptocercus. Proc R Soc B. 2009;276:239–245.

Ohkuma M, Brune A. Diversity, structure and evolution of the termite gut microbial community. In Biology of Termites: A Modern Synthesis Ed. D E Bignell, Y Roisin, N Lo. Dordrecht, Neth.: Springer. 2011;413–38.

Tamschick S, Radek R. Colonization of termite hindgut walls by oxymonad flagellates and prokaryotes in Incisitermes tabogae, I. marginipennis and Reticulitermes flavipes. European Journal of Protistology. 2013;49(1):1–14.

Leidy J. On intestinal parasites of Termes flavipes. Proc. Acad. Nat. Sci. Phila. 1877;29:146-149.

Yamin MA. Flagellates of the orders Trichomonadida Kirby, Oxymonadida Grasse´, and Hypermastigida Grassi & Foa` reported from lower termites (Isoptera families Mastotermitidae, Kalotermitidae, Hodotermitidae, Termopsidae, Rhinotermitidae, and Serritermitidae) and from the wood-feeding roach Cryptocercus (Dictyoptera: Cryptocercidae). Sociobiology. 1979;4:5–119.

Brugerolle G, Radek R. Symbiotic protozoa of termites. In: Intestinal Microorganisms of Termites and Other Invertebrates (Eds König H, Varma A). Springer-Verlag, Berlin. 2006;243–269.

Kitade O, Matsumoto T. Characteristics of the symbiotic flagellate composition within the termite. Family Rhinotermitidae (Isoptera). Symbiosis. 1998;25:271-278.

Stingl U, Brune A. Phylogenetic diversity and whole-cell hybridization of oxymonad flagellates from the hindgut of the wood-feeding lower termite Reticulitermes flavipes. Protist. 2003;154:147–155.

Dietrich C, Kohler T, Brune A. The cockroach origin of the termite gut microbiota: Patterns in bacterial community structure reflect major evolutionary events. Appl. Environ. Microbiol. 2014;80:2261–2269.

Tai V, James ER, Nalepa CA, Scheffrahn RH, Perlman SJ, Keeling PJ. The role of host phylogeny varies in shaping microbial diversity in the hindguts of lower termites. Applied and Environmental Microbiology. 2015;81(3): 1059–1070.

Rossmassler K, Dietrich C, Thompson C, Mikaelyan A, Nonoh JO, Scheffrahn RH, Sillam-Dussès D, Brune A. Metagenomic analysis of the microbiota in the highly compartmented hindguts of six wood- or soil-feeding higher termites. Microbiome. 2015;3:56.

Ley RE, Peterson DA, Gordon JI. Ecological and evolutionary forces shaping microbial diversity in the human intestine. Cell. 2006;124:837–848.

Brune A. Symbiotic digestion of lignocellulose in termite guts. Nat Rev Microbiol. 2014;168-80. DOI: 10.1038/nrmicro3182 Epub 2014 Feb 3 PMID: 24487819

Auer L, Lazuka A, Sillam-Dussès D, Miambi E, O’Donohue M, Hernandez-Raquet GH. Uncovering the potential of termite gut microbiome for lignocellulose bioconversion in anaerobic batch bioreactors. Front. Microbiol. 2017;8:2623. DOI: 10.3389/fmicb.2017.02623

Zhou J, Duan J, Gao M, Wang Y, Wang X, Zhao K. Diversity, roles and biotechnological applications of symbiotic microorganisms in the gut of termite. Curr Microbiol. 2018;76:755–761.

He C, Nan X, Zhang Z, Li M. Composition and diversity analysis of the gut bacterial community of the oriental armyworm, Mythimna separata, determined by culture-independent and culture-dependent techniques. Journal of Insect Science (Online). 2013;13:165.

Hongoh Y, Deevong P, Inoue T, Moriya S, Trakulnaleamsai S, Ohkuma M, Vongkaluang C, Noparatnaraporn N, Kudo T. Intra- and interspecific comparisons of bacterial diversity and community structure support coevolution of gut microbiota and termite host. Appl Environ Microbiol. 2005;71:6590–6599.

Hongoh Y, Deevong P, Hattori S, Inoue T, Noda S, Noparatnaraporn N, Kudo T, Ohkuma M. Phylogenetic diversity, localization and cell morphologies of members of the candidate phylum TG3 and a subphylum in the phylum Fibrobacteres, recently discovered bacterial groups dominant in termite guts. Appl Environ Microbiol. 2006;72:6780–6788.

Costa RRD, Hu H, Li H, Poulsen M. Symbiotic plant biomass decomposition in fungus-growing termites. Insects. 2019;10(4):87.

Warnecke F, Luginbuhl P, Ivanova N, Ghassemian M, Richardson TH, Stege JT, Cayouette M, McHardy AC, Djordjevic G, Aboushadi N, Sorek R, Tringe SU, Podar M, Maritn HG, Kunin V, Dalevi D, Madejska J, Kirton E, Platt D, Szeto E, Salamov A, Barry K, Mikhailova N, Kyrpides NV, Matson EG, Ottesen EA, Zhang X, Hernandez M, Murillo C, Acosta LG, Rigoutsos I, Tamayo G, Green BD, Chang C, Rubin EM, Mathur EJ, Rpbertspm DE, Hugenholtz P, Leadbetter JR. Metagenomic and functional analysis of hindgut microbiota of a wood-feeding higher termite. Nature. 2007;450:560-569.

Su L, Yang L, Huang S, Su X, Li Y, Wang F, Wang E, Kang N, Xu J, Song A. Comparative gut microbiomes of four species representing the higher and the lower termites. J Insect Sci. 2016;16(1):97.

Romero Victorica M, Soria MA, Batista-García RA, Ceja-Navarro JA, Vikram S, Ortiz M, Ontañon O, Ghio S, Martínez-Ávila L, Quintero, García OJ, Etcheverry C, Campos E, Cowan D, Arneodo J, Talia PM. Neotropical termite microbiomes as sources of novel plant cell wall degrading enzymes. Sci Rep. 2020;10:3864.

Butera G, Ferraro C, Alonzo G, Colazza S, Quatrini P. The gut microbiota of the wood-feeding termite Reticulitermes lucifugus (Isoptera; Rhinotermitidae). Ann Microbiol. 2016;66:253-260.

Sato T, Hongoh Y, Noda S, Hattori S, Ui S, Ohkuma M. Candidatus Desulfovibrio trichonymphae, a novel intracellular symbiont of the flagellate Trichonympha agilis in termite gut. Environ Microbiol. 2009;11:1007–15.

Mathew GM, Ju YM, Lai CY, Mathew DC, Huang CC. Microbial community analysis in the termite gut and fungus comb of Odontotermes formosanus: The implication of Bacillus as mutualists. FEMS Microbiol Ecol. 2012;79(2):504–517.

Shinzato N, Muramatsu M, Matsui T, Watanabe Y. Molecular phylogenetic diversity of the bacterial community in the gut of the termite Coptotermes formosanus. Biosci Biotechnol Biochem. 2005;69:1145–1155.

Ali HRK, Hemeda NF, Abdelaliem YF. Symbiotic cellulolytic bacteria from the gut of the subterranean termite Psammotermes hypostoma Desneux and their role in cellulose digestion. AMB Express. 2019;9(1):111.

Ohkuma M, Kudo T. Phylogenetic diversisity of the intestinal bacterial community in the termite Reticuliterrmes speratus. Appl Environ Microbiol. 1996;62(2):461–468.

Poulsen M, Hu H, Li C, Chen Z, Xu L, Otani S, Nygaard S, Korb J, Aanen DK, Wang J, Boomsma JJ, Zhang G. Complementary symbiont contributions to plant decomposition in a fungus-farming termite. Proc Natl Acad Sci USA. 2014;40:14500–14505.

Shinzato N, Muramatsu M, Matsui T, Watanabe Y. Phylogenetic analysis of the gut bacterial microflora of the fungus-growing termite Odontotermes formosanus. Biosci Biotechnol Biochem. 2007;71:906–915.

Konig H. Bacillus species in the intestine of termites and other soil invertebrates. Journal of Applied Microbiology. 2006;101(3):620–627. DOI: 10.1111/j.1365-2672.2006.02914.x

Hussin NA, Majid AH. Inter and intra termites colonies comparisons of gut microbial diversity from worker and soldier caste of Globitermes sulphureus (Blattodea: Termitidae) using 16S rRNA gene. Malaysian Journal of Microbiology. 2017;13:228-234.

Nidhi K, Gupta KG, Bura A, Gandhi A. Diversity of cellulose hydrolyzing bacteria from the gut of Coptotermes heimi (Rhinotermitidae). Asian J. Biol. Life Sci. 2018;7(1).

Schultz JE, Breznak JA. Cross-feeding of lactate between Streptococcus lactis and Bacteroides sp. isolated from termite hindguts. Appl. Environ. Microbiol. 1979;37:1206-10.

Kohler T, Stingl U, Meuser K, Brune A. Novel lineages of planctomycetes densely colonize the alkaline gut of soil-feeding termites (Cubitermes spp.). Environ Microbiol. 2008;10:1260–70.

Kappler A, Brune A. Influence of gut alkalinity and oxygen status on mobilization and sizeclass distribution of humic acids in the hindgut of soil-feeding termites. Appl Soil Ecol. 1999;13:219–229.

Noda S, Inoue T, Hongoh Y, Nalepa CA, Vongkaluang C, Kudo T, Ohkuma M. Identification and characterization of ectosymbionts of distinct lineages in Bacteroidales attached to flagellated protists in the gut of termites and a wood-feeding cockroach. Environ. Microbiol. 2006;8:11–20.

Iida T, Ohkuma M, Ohtoko K, Kudo T. Symbiotic spirochetes in the termite hindgut: Phylogenetic identification of ectosymbiotic spirochetes of oxymonad protists. FEMS Microbiol. Ecol. 2000;34:17–26.

Breznak JA, Leadbetter JR. Termite gut spirochetes. The Prokaryotes. 2006;318– 329.

Droge S, Rachel R, Radek R, Konig H. Treponema isoptericolens sp. nov., a novel spirochaete from the hindgut of the termite Incisitermes tabogae. Int J Syst Evol Microbiol. 2008;58:1079–1083.

Watanabe Y, Shunzato N, Fukatsu T. Isolation of Actinomycetes from termites’ guts. Bioscience, Biotechnology and Biochemistry. 2003;67(8):1797–1801.

Arango RA, Carlson CM, Currie CR, McDonald BR, Book AJ, Green F, Lebow NK, Raffa KF. Antimicrobial activity of actinobacteria isolated from the guts of subterranean termites. Environmental Entomology. 2016;45(6):1415–1423.

Strassert JFH, Desai MS, Radek R, Brune A. Identification and localization of the multiple bacterial symbionts of the termite gut flagellate Joenia annectens. Microbiology. 2010;156:2068– 2079.

Frohlich J, Konig H. Rapid isolation of single microbial cells from mixed natural and laboratory populations with the aid of a micromanipulator. Syst Appl Microbiol. 1999;22:249–257.

Hongoh Y, Ohkuma M, Kudo T. Molecular analysis of bacterial microbiota in the gut of the termite Reticulitermes speratus (Isoptera; Rhinotermitidae). FEMS Microbiol Ecol. 2003;44:231–242.

Hongoh Y, Ohkuma M. Termite gut flagellates and their methanogenic and eubacterial symbionts. Microbiology Monographs. 2010;55–79.

Brune A. Methanogens in the digestive tract of termites. Microbiology Monographs. 2018;81–101.

Paul K, Nonoh JO, Mikulski L, Brune A. “Methanoplasmatales,” Thermoplasmatales-related archaea in termite guts and other environments, are the seventh order of methanogens. Appl. Environ. Microbiol. 2012;78(23):8245–8253.

Yang J, Bordeaux FM, Smith PH. Isolation of methanogenic bacteria from termites. Abstr. In: Abstract of the 85th Annual Meeting of the American Society for Microbiology. Wash., D.C.1-83. 1985;160.

Leadbetter JR, Breznak JA. Physiological ecology of Methanobrevibacter cuticularis sp. nov. and Methanobrevibacter curvatus sp. nov., isolated from the hind gut of the termite Reticulitermes flavipes. Appl. Environ. Microbiol. 1996;62:3620–3631.

Leadbetter JR, Crosby LD, Breznak JA. Methanobrevibacter filiformis sp. nov., A filamentous methanogen from termite hindguts. Archives of Microbiology. 1998;169(4):287–92.

Donovan SE, Purdy KJ, Kane MD, Eggleton P. Comparison of Euryarchaea strains in the guts and food-soil of the soil-feeding termite Cubitermes fungifaber across different soil types. Appl Environ Microbiol. 2004;70:3884–3892.

Shi Y, Huang Z, Han S, Fan S, Yang H. Phylogenetic diversity of Archaea in the intestinal tract of termites from different lineages. Journal of Basic Microbiology. 2015;55(8):1021–1028.

Brauman A, Dore J, Eggleton P, Bignell D, Breznak JA, Kane MD. Molecular phylogenetic profiling of prokaryotic communities in guts of termites with different feeding habits. FEMS Microbiol Ecol. 2001;35(1):27–36.

Brune A. Methanogens in the digestive tract of termites. In: Hackstein JHP (Ed) (Endo) symbiotic methanogenic archaea, 1st Edn. Springer, Heidelberg. 2010;81–100.

Ohkuma M, Noda S, Horikoshi K, Kudo T. Phylogeny of symbiotic methanogens in the gut of the termite Reticulitermes speratus. FEMS Microbiology Letters. 1995;134:45–50.

Breznak JA, Brune A. Role of microorganisms in the digestion of lignocellulose by termites. Annu. Rev. Enford. 1994;39:433-487.

Wood TG, Thomas RJ. The mutualistic association between macrotermitinae and termitomyces. Insect-Fungus Interactions. 1989;69–92.

Radek R. Flagellates, bacteria and fungi associated with termites: Diversity and function in nutrition – a review. Ecotropica. 1999;5:183–196.

Moriya S, Inoue T, Ohkuma M, Yaovapa T, Johjima T, Suwanarit P, Sangwanit U, Vongkaluang C, Noparatnaraporn N, Kudo YT. Fungal community analysis of fungus gardens in termite nests. Microbes Environ. 2005;20:243-252.

Visser AA, Ros VID, De-Beer ZW, Debets AJM, Hartog E, Kuyper TW, Laessøe T, Slippers B, Aanen DK. Levels of specificity of Xylaria species associated with fungus-growing termites: A phylogenetic approach. Mol. Ecol. 2009;18:553-567.

Visser AA, Kooij PW, Debets AJM, Kuyper TW, Aanen DK. Pseudoxylaria as stowaway of the fungus-growing termite nest: Interaction asymmetry between Pseudoxylaria, Termitomyces and free-living relatives. Fungal Ecology. 2011;4:322–332.

Makonde HM, Boga HI, Osiemo Z, Mwirichia R, Stielow JB, Göker M, Klenk HP. Diversity of termitomyces associated with fungus-farming termites assessed by cultural and culture-independent methods. PLoS ONE. 2013;8(2):e56464.

Rogers JD, Ju YM, Lehmann J. Some Xylaria species on termite nests. Mycologia. 2005;97:914–923.

Lozupone CA, Hamady M, Kelley ST, Knight R. Quantitative and qualitative (beta) diversity measures lead to different insights into factors that structure microbial communities. Appl. Environ. Microbiol. 2007;73(5):1576-1585.

Makonde, Huxley. Fungal diversity and community structure in gut, mound and surrounding soil of fungus-cultivating termites. African Journal of Microbiology Research. 2017;11:504-515.

Wilhelm SW, Suttle CA. Viruses and nutrient cycles in the sea viruses play critical roles in the structure and function of aquatic food webs. Bioscience. 1999;49:781–788.

Rodriguez-Brito B, Li L, Wegley L, Furlan M, Angly F, Breitbart M, Buchanan J, Desnues C, Dinsdale E, Edwards R, Felts B, Haynes M, Liu H, Lipson D, Mahaffy J, Martin-Cuadrado AB, Mira A, Nulton J, Pasić L, Rayhawk S, Rodriguez-Mueller J, Rodriguez-Valera F, Salamon P, Srinagesh S, Thingstad TF, Tran T, Thurber RV, Willner D, Youle M, Rohwer F. Viral and microbial community dynamics in four aquatic environments. ISME J. 2010;4:739–751.

Jasna V, Parvathi A, Pradeep Ram AS, Balachandran KK, Madhu NV, Nair M, Jyothibabu R, Jayalakshmy KV, Revichandran C, Sime-Ngando T. Viral-induced mortality of prokaryotes in a tropical monsoonal estuary. Frontiers in Microbiology. 2017;8:895.

Tikhe CV, Martin TM, Gissendanner CR, Husseneder C. Complete genome sequence of Citrobacter phage CVT22 isolated from the gut of the Formosan subterranean termite, Coptotermes formosanus Shiraki. Genome Announc. 2015;3:e00408–00415.

Tikhe CV, Gissendanner CR, Husseneder C. Whole-genome sequence of the novel temperate Enterobacter bacteriophage Tyrion, isolated from the gut of the Formosan subterranean termite. Genome Announc. 2018;6:e00839-17.

Tikhe CV, Husseneder C. Metavirome sequencing of the termite gut reveals the presence of an unexplored bacteriophage community. Front. Microbiol. 2018;8:2548.

Minot S, Sinha R, Chen J, Li H, Keilbaugh SA, Wu GD, Lewis JD, Bushman FD. The human gut virome: Inter-individual variation and dynamic response to diet. Genome Research. 2011;21(10):1616–1625.

Santiago-Rodriguez TM, Ly M, Bonilla N, Pride DT. The human urine virome in association with urinary tract infections. Front. Microbiol. 2015;6:14.

Tangherlini M, Dell’anno A, Allen LZ, Riccioni G, Corinaldesi C. Assessing viral taxonomic composition in benthic marine ecosystems: Reliability and efficiency of different bioinformatic tools for viral metagenomic analyses. Sci. Rep. 2016;6:28428.

Brune A, Ohkuma M. Role of the termite gut microbiota in symbiotic digestion. In: Bignell, DE, Roisin, Y, and Lo, N (Eds.), Biology of Termites: A Modern Synthesis. Springer Science + Business Media B.V., Springer Dordrecht Heidelberg, London New York. 2011;439-475.

Kirby H. Trichomonad flagellates from termites. Univ Calif (Berkeley) Publ Zool. 1930;33:393–444.

Pester M, Brune A. Hydrogen is the central free intermediate during lignocellulose degradation by termite gut symbionts. ISME J. 2007;1:551–565.

Noda S, Mantini C, Meloni D, Inoue JI, Kitade O, Viscogliosi E, Ohkuma M. Molecular phylogeny and evolution of parabasalia with improved taxon sampling and new protein markers of actin and elongation factor-1α. PLOS ONE. 2012;7:e29938.

Hongoh Y, Sato T, Dolan MF, Noda S, Ui S, Kudo T, Ohkuma M. The motility symbiont of the termite gut flagellate Caduceia versatilis is a member of the “Synergistes” group. Appl Environ Microbiol. 2007;73:6270–6276.

Izawa K, Kuwahara H, Sugaya K, Lo N, Ohkuma M, Hongoh Y. Discovery of ectosymbiotic Endomicrobium lineages associated with protists in the gut of stolotermitid termites. Environ Microbiol Rep. 2017;9:411–418.

Nakajima H, Hongoh Y, Usami R, Kudo T, Ohkuma M. Spatial distribution of bacterial phylotypes in the gut of the termite Reticulitermes speratus and the bacterial community colonizing the gut epithelium. FEMS Microbiol Ecol. 2005;54(2):247-55.

Nakajima H, Hongoh Y, Noda S, Yoshida Y, Usami R, Kudo T, Ohkuma M. Phylogenetic and morphological diversity of Bacteroidales members associated with the gut wall of termites. Biosci Biotechnol Biochem. 2006;70:211–218.

Yang H, Schmitt-Wagner D, Stingl U, Brune A. Niche heterogeneity determines bacterial community structure in the termite gut (Reticulitermes santonensis). Environ Microbiol. 2005;7:916–932.

Cook SF. The respiratory gas exchange in Termopsis nevadensis. Biol. Bull. 1932;63:246257.

Conrad R. Methane production in soil environments—Anaerobic biogeochemistry and microbial life between flooding and desiccation. Microorganisms. 2020;8:881.

Rouland C, Brauman A, Labat M, Lepage M. Nutritional factors affecting methane emission from termites. Chemosphere. 1993;26(1-4):617–622.

Gomathi V, Ramasamy K, Mula RV, Ramalakshmi Aps, Ramanathan A. Methan emission by gut symbionts of termites. Acad J. Plant Sci. 2009;2:2.

Nauer PA, Hutley LB, Arndt SK. Termite mounds mitigate half of termite methane emissions. Proc Natl Acad Sci USA. 2018;115(52):13306-13311.

Purwadaria T, Ketaren PP, Sinurat AP, Sutikno I. Identification and evaluation of fiber hydrolytic enzymes in the extract of termites (Glyptotermes montanus) for poultry feed application. Indon. J. Agric. Sci. 2003;4:40-47.

Chai EW, H'ng PS, Peng SH, Wan-Azha WM, Chin KL, Chow MJ, Wong WZ. Compost feedstock characteristics and ratio modelling for organic waste materials co-composting in Malaysia. Environ Technol. 2013;34(17-20): 2859-2866.

Peng SH, Wan-Azha WM, Wong WZ, Go WZ, Chai EW, Hing PS. Effect of using agro-fertilizers and N-fixing azotobacter enhanced biofertilizers on the growth and yield of corn. J. Applied Sci. 2013;13:508-512.

Chutani P, Sharma KK. Concomitant production of xylanases and cellulases from Trichoderma longibrachiatum MDU-6 selected for the deinking of paper waste. Bioprocess Biosyst Eng. 2016;39:747–758.

Varghese LM, Agrawal S, Sharma D, Mandhan RP, Mahajan R. Cost-effective screening and isolation of xylano-cellulolytic positive microbes from termite gut and termitarium. 3 Biotech. 2017;7:108.

Talia P, Arneodo J. In termites and sustainable management Vol. 1 sustainability in plant and crop protection (Eds. Aslam. Khan & Wasim. Ahmad). 2018;Ch. 5:101–117. (Springer series, 2018).

Sharma R, Kaur R, Rana N, Poonia A, Rana DC, Attri S. Termite’s potential in solid waste management in Himachal Pradesh: A mini review. Waste Management & Research. 2020;1–9.

Singer E. Why termite guts could bring better biofuels. MIT Technology Review; 2007.

Victorica MR, Soria MA, Batista-Garcia RA, Ceja-Navarro JA, Vikram S. Neotropical termite microbiomes as sources of novel plant cell wall degrading enzymes. Sci. Rep. 2020;10:3864.

Hervé V, Liu P, Dietrich C, Sillam-Dussès D, Stiblik P, Šobotník J, Brune A. Phylogenomic analysis of 589 metagenome-assembled genomes encompassing all major prokaryotic lineages from the gut of higher termites. Peer J. 2020;8:e8614.