Research Article Ravi Kant Upadhyay et al. / Journal of Pharmacy Research 2011,4(4),1161-1166 ISSN: 0974-6943 Available online through http://jprsolutions.info Symbiotic and non-symbiotic micro flora of termite gut: a unique nonhuman agricultural system that can recycle photo-synthetically fixed carbon and nutrients Ravi Kant Upadhyay Department of Zoology, D D U Gorakhpur University, Gorakhpur, 273009. India Received on: 05-12-2010; Revised on: 14-01-2011; Accepted on:09-03-2011

ABSTRACT Termites are xylophagous insects which house a range of microorganisms including protozoan, bacteria and fungi inside their gut. These microbes associate to form mutualistic associations that help the termites to degrade the plant-derived biomass. These gut symbionts specially fungi predigest plant substrate and maintain food supply to termites. Besides this, fungi secrete few chemicals from decayed wood, which attract termites for feeding. Interestingly, presence of microflora in the gut makes termites able to degrade wood and wood constituents such as cellulose and hemi-cellulose. In turn, termites help the fungi by transporting and spreading them to new areas. Fungi play an important role in nutrition of termites by being a direct source of food, or by modifying it and do recycling of photo-synthetically fixed carbon with the aid of symbiotic gut micro-flora. These also play important role in termite survival and possess nitrogen fixation genes (nifH) that show potential for nitrogen fixation in natural environment. But, few termite species lack this gene. After being development of appropriate microbial technology, this unique nonhuman agricultural system can be used for the improvement of soil fertility, biological nitrogen fixation and in pest management. From scientific standpoint, if products and biological processes of novel microbial strains will be identified these might have wider applications in agriculture and industry. Certainly, in coming future it would become a part of sustainable agricultural development. The purpose of present article is to signify the importance of gut symbionts in termite life mainly in establishment of colony, decomposition of food material, recycling of nutrients and survival in adverse environmental conditions.

Key words: Termite-gut, microflora, symbionts, fungi, decayed-wood, cellulose, antagonistic, mutualistic-associations

INTRODUCTION Termites predominantly occur in tropical and subtropical forest environment mainly in arid Sands, 1960). These are designated as “ecological equivalents” (Chen and Henderson, 1997) ecosystem. These also occur in Sahara desert and Savannah grass lands of Africa (Havarty and and become potentially important source of heterogeneity in tropical forest soil system (Donovana Nutting, 1975) and mainly found highly colonized in humid areas of tropics. Termites live in et al., 2001). fringes by nesting, in drifting sands, in fertile soil and occur in woody plants. In deserts, termites do not build conspicuous above ground epigeal nests or mounds. Their diversity falls TERMITE NESTS off sharply in temperate regions and is absent altogether in boreal and arctic regions. These are Most of the termite species inhabit in moist decaying areas especially in trunks, logs of trees more diverse on continents in comparison to distantly placed islands from main land. Termites and make simple nests (Emerson, 1939), while few termite species inhabit inside galleries by as ecotone species also compete for food and foraging grounds in grassland and forest ecosys- excavating the wood and do not show any external manifestation of their presence. Normally tems. In arid ecosystem, their populations typically range from 2,000 to 4,000 individuals per forest living termites construct huge mounds or ‘termitaria’ which protect them from high square meter but may occasionally run as high as 10,000 individuals per square meter. Their temperature and strong sunlight. Termites also construct nests of soil mixed with termite feces biomass (up to 22 g/sq. m.) exceeds the combined biomass of all vertebrate species living in and make galleries and tunnels extend them far into the soil. This constructive architectural the same area. Termites are adapted to survive on optimum temperature i.e. 300C to 370C but approach helps nitrogenous compounds to adsorb into soil components with feces (Wood and show inability to tolerate the high relative humidity (Woodrow et al., 2000). Termites Sands, 1978). Brood is settled in inner galleries for a softer consistency, is made up of woody construct underground galleries or tunnels, which enable them to concealed from the light and or other comminuted material, which is passed through the alimentary canal. Some other enemies. More than 2700 species of termites are known in the world and most of them are seen genera such as Mastotermes, Kalotermes, Neotermes and Cryptotermes species, bore into dry highly destructive (Culliney and Grace, 2000). wood such as furniture, building doors, windows and other wood materials (Inta et al., 2007). Neotermes militaris and N. greeni found in forests of Ceylon make burrows inside tea stems HIGHLY DESTRUCTIVE SOCIAL INSECTS while Rhinotermes, Reticulitermes and Coptotermes live in the ground and infest wood Termites are highly destructive polyphagous insect pests, which largely damage household indirectly through the soil (Laine et al., 2003). Most remarkable features of termitaria are the materials, agricultural crops, forest products and other commercial products above threshold lofty steep structures constructed by termites (Hadlington, 1987). Macrotermes make very level (Su and Tamashiro, 1987; Lax and Osbrink, 2003). Termites cause heavy damage wood huge termitaria which measures over 8 m in height. It uses greater bulk of the earth and sand and wood products after capturing little humidity. Whether it is a rural area or an urban and soil collected from the surface to form the termitaria. Termites also build large and elaborate domestic site, termite menace is everywhere. Termites eat upon dung, plant litter, wood, nests and make air holes and chambers to maintain humidity.The interior of such a termitarium clothes, paper, fibers and other household and woody building material. They also infest green presents maze of irregular chambers and passages, and its walls are so resistant that it is difficult standing foliages and cereals stored in godowns. Termites also attack wood houses, boats, to make any impression upon them even with a sharp pick. It also provides requisite humidity doors, bridges, bullock carts, underground electrical and telephone cables, finished goods such and manages to escape in underground chambers and reach the upper storey of buildings or as books, papers and fibrous plant materials (Lai et al., 1983; Tamashiro et al., 1987; Felix ascend lofty trees. Other termite species such as Indian, African and Australian construct huge and Henderson, 1995). Termites cause greater harm to wood and wood products and convert termitaria excavated over earth and make underground chambers. They also make passages and it into half digested earthy biomass within a short period of time (Mauldin, 1986). Termites royal cells composed of wet soil, plastered from outside to form a hard brick-like substance. depend on gut flora for wood digestion and their survival (Eutick et al., 1978). Termites make Subterranean termites make their mounds inside soil and increase the soil porosity. They heavy losses to crop yield, deteriorate crop quality and increase harvesting costs and cereal usually collect soil particles, cemented it from inside and make large structures resistant to crops mostly at seedling stage of crop. Normally, termite’s infestation starts in the early sapling erosion, and prevent the penetration of water to the underlying soil. Contrary to this Coptotermes stage of crop and it become higher at seedling stage (Umeh et al., 1999). In rainy season compress porous soil and excavate compact soil, to make tunnels with their feces and silt/ termites, start eating from root to top and construct foraging galleries inside plants. Overall saliva mixture (Lee and Wood, 1971). Termite species secrete agglutinating fluids consist of damage caused by termites around the globe is $120-200 billion approximately. Termites saliva and excrement. occur in different climatic regions and become economic pests. They possess appetite for wood and wood products; extend their search to find woody building material and other commercial TERMITE AND MICROBIAL RELATIONSHIP products. Few termite species such as Macrotermes, Microtermes, Odontotermes, Coptotermes In nature, interactions between insects, bacteria and fungi range from antagonistic to mutual- and Reticulitermes become highly destructive and make heavy losses and known as economi- istic and include many spectacular examples of complex symbiosis (Martin, 1992). Most of cally harmful species (Lewis and Haverty, 1996; them are still unknown. Termites as a social insect domesticate fungi in their nests, which help in decaying plant litter and other woody materials. Termites forage for plant material to provision their fungus gardens and convert carbon-rich plant material into nitrogen-rich fungal *Corresponding author. biomass. These fungus-growing termites eat unripe mushroom-like structures that contain Ravi Kant Upadhyay asexual spores. Termites mix spores with the consumed plant substrate and deposit it with the feces on top of the fungus garden. Fungus gardens are constructed from primary feces of termites Department of Zoology, that contain solid ‘fungus comb. More specifically, termites deposit wood decaying fungi D D U Gorakhpur University, inside shelter tubes in the bark of living trees, paste fecal pellets, loose detritus and frass in their Gorakhpur, India 273009 Journal of Pharmacy Research Vol.4.Issue 4. April 2011 1161-1166 Ravi Kant Upadhyay et al. / Journal of Pharmacy Research 2011,4(4),1161-1166 tunnels. Termites cultivate fungi and yield abundant growth to predigest the wood material 1995, Andrew et al., 2001 Chavarri et al., 2001), More commonly A. flavus is found attached (Hendee, 1934) and make it edible for termites (Esenther et al., 1961). For this, termites dig to external surface and gut of termites. These pathogenic fungi are introduced artificially tunnels in the wood and inoculate fungi to grow on the wood (Ebeling, 1975). Further, fungal through attractant-baited traps (Fuxa et al., 1998, Fuxa and Tanada, 1987). Further, pathogen- growth is supported by natural environmental conditions such as soil moisture and nutrients. esis is naturally spread by grooming behavior and proctodeal trophallaxis occurs in termites (Beard 1974). After enormous fungal growth products released help termites to locate the (Grace and Zoberi, 1992; Kramm et al., 1982; Rosengaus and Traniello, 1997). Thus, decaying wood (Esenther et al., 1961) and also play an important role in nutrition of termites transfer of pathogens imposes high mortality in termites mainly in Reticulitermes flavipes by being a direct source of food (Beard, 1974). ). Wood decaying fungi also furnish nitrogen, (Kollar) and R. virginicus (Banks) (Beal and Kais, 1962). A. flavus is also found toxic to vitamins, and other beneficial substances to termites (Becker 1976) and do break down of toxic Heterotermes indicola and Coptotermes amanii (Lenz, 1969) and R. flavipes (Beal and Kais, volatile materials present in wood (Ebeling, 1975). In return, termites help in transportation 1962), while Trichoderma spp. shows toxicity to Kalotermes flavicollis (Fabr.), Heterotermes of spores and hyphae to new areas (Hendee, 1934), carry fungi adhering to the integument, and indicola (Wassmann), Reticulitermes lucifugus (Rossi) var. santonensis Feytaud and in side their gut (Batra and Batra, 1966). Normally termites carry conidiophores and conidia Nasutitermes ephrate (Holmgren) (Becker and Kerner-Gang, 1964). Interestingly, soil envi- found attached to the body, appendages (Hendee, 1933) and accumulate large tufts of hyphae on ronment protect microorganisms from ultraviolet radiation and promote epizootics (Culliney their legs (Hendee, 1934). Hindgut of termite possesses diverse hindgut microbial commu- and Grace, 2000). nity, which helps in digestion of wood cellulose by secreting digestive enzymes. It is densely colonized by a multitude of symbiotic microorganisms, which degrade wood components to FUNCTIOINS OF GUT MICROBIAL COMMUNITY simple compounds. Wood digestion by micro-organisms favors and enables termites to live in bad habitats because of enormous food supply. (1)AS AN OXYGEN SINK Wood feeding termites contains deep penetration of oxygen into the hindgut lumen, which (A) MUTUALISTIC ASSOCIATIONS boost up high oxygen consumption rates of the symbiotic gut microbiota. Oxygen plays Mutualism shows symbiotic relationships between two or more living organisms that are not indispensable role in the mineralization of aromatic compounds. Wood feeding termites utilize closely related in terms of phylogeny, generally assuming mutual dependence as well as carbohydrate as foods after partial digestion of plant litter done by aero-tolerant lactic acid physical intimacy. It is much progressive mutual relationship serves to create new ecological bacteria within the gut (Wenzel et al., 2002). The anerobic bacteria utilize CO2 released by combinations of different organisms having desirable functions. Termites are a well-known termites with in the gut. Thus, symbionts inside termite gut pass a healthy and adaptive life. example of symbiosis, a relationship that enables termites to live on wood and its constitu- In return, gut microflora prepare supplement for termite diet and provide essential nutritional ents. More specifically, gut microorganisms, especially flagellated protists (eukaryotes) and means. Termites metabolize the monoaromatic compounds and lignin-derived phenylpropanoids cellulolytic flagellates degrade wood cellulose and produce acetate, which is in turn absorbed only in the presence of oxygen and this mechanism fulfill carbon and oxygen requirement of the by termites as their energy and carbon source. Prokaryotic symbionts also play many impor- host. In the anoxic condition, the substrates are metabolized endogenously within the termite tant role in termite nutrition (Fig. 1) Termites depend on nitrogen-fixing bacteria to supply gut a mini ecosystem that also functions as anoxic fermentor and maintain axially and radially nitrogen and on symbiotic protozoan that produce the cellulolytic enzymes and digest the structured environments in physico-chemically distinct microhabitats. It strengthens termite cellulose. T. shpaerica itself is unable to digest cellulose with out aid of bacteria that live survival in adverse conditions and helps in recycling of organic matter, by humification inside within its body. Protozoans, such as T. shpaerica also exhibit ectosymbiosis are covered by mound and degrade plant litter. Thus, gut microbes manage and balance carbon and nitrogen precise rows of thousands of bacteria adhered to the surface. Similarly, protozoans Mixotricha contents (C/N ratio) in plant litter before humification. During humification of organic material possess rows of spirochetes on its surface. In absence of gut fauna, the adult termites cannot both humic and fulvic acids are formed in the degraded plant litter, which smells very fast and effectively feed on wood, and show cannibalism. A classic example of mutation is the indicate the presence of termites and microbes. Thus, termites process the plant debris by two flagellated protozoa that live in the gut of termites and wood roaches. These flagellates survive different humification pathways in the two environments, one inside mound and another on a diet of carbohydrates, acquired as the cellulose wood chips ingested by their host. The outside mound for their own purpose. To maintain the system more dynamic, gut microbes protozoa engulf wood particles, digest the cellulose and metabolize it to acetate and other also provides impetus to the neonates for feeding on faecal pellets to get easy transfer of products. Termites absorb and oxidize the acetate released by these flagellates. Because the microflora in the gut to balance the energy requirement and population size. host is incapable of synthesizing cellulose, it is dependent on the mutualistic protozoa for its existence. (2)WOOD DIGESTION AND RECYCLING OF NUTRIENTS Termites play a major role in the recycling of photo-synthetically fixed carbon with the aid of Termites inhabit protozoans belong to Polymastigina and Hypermastigina groups (Kirby, their symbiotic intestinal micro-flora. Saprophytic fungi and bacteria that house in the termite 1937; Steinhaus, 1946), some soil-feeding bacteria, spirochaetes, Lipotrophidae and indig- gut helps in wood digestion (Wood and Cowie, 1988). Termites also degrade wood and wood enous actinomycetes (Costa-Leonardo et al., 2008; Hongoh et al., 2003; Lilburn et al., constituents such as cellulose and hemicellulose with the help of fungal products. These fungal 1999). Trichonympha a flagellated protozoa house in the termite gut. Termite provide living constituents formed after wood decaying provide feeding stimulus to termites, which varies habitat to Trichonympha, while Trichonympha possess the ability to break down cellulose that with the amount of the decay (Amburgey and Smythe, 1977). Generally termites do not prefer enables termites to use wood as a food source.Trichonympha is an anaerobic protozoon, which completely decayed wood because it becomes less suitable for feeding after breakdown of lives in the gut of termite have no mitochondria, no cytochromes and no functional tri- cellulose (Becker, 1976). Hence, termites consume fungus infected wood much higher than carboxylic acid cycle. Trichonympha species are found in the intestine of termites and produce non-infected wood (Becker, 1971) and prefer moderately decayed wood (Lenz et al., 1991). enzymes that the termite need to digest the wood particles on to which it feeds. Usually each Certain fungi like brown rot fungus belonging to basidiomycetes (Light and Weesner, 1947; species of termite contains only a single species of flagellate but some termite species harbor Becker, 1965; Ruyooka, 1979; Williams, 1965) predigest the wood and make it edible for more than two or three species of protozoa. Adult termites cultivate various symbiotic termites. For example, heartwood of Pinus caribaea (Moreler) was found to be more suitable microfauna inside their gut by eating carcasses of dead companions and other organic waste to eat after decayed by brown rot fungus, Lentinus pallidus (Williams, 1965). Thereafter, materials. Wood eating termites, O. obesus and Coptotermes mostly decompose branches, Coptotermes niger attacks only those areas of heartwood of pinus caribaea where timber is logs and tree stumps with the help of microbes which reside in their gut. This decomposition infected with brown rot fungus and predigested by it (Perry et al., 1985). Hence, fungal decay is also done by Gram-positive bacteria belong to the genera Bacillus, Paenibacillus, is very important for wood feeding termites because it changes the nutritional value of wood Brevibacillus Streptomyces or the actinobacteria group, and Gram-negative strains from genera and detoxifies it (Matsuura 2003). More exceptionally, termites more readily eat upon wood Pseudomonas, Acinetobacter, Agrobacterium/Rhizobium, Brucella/Ochrobactrum, Pseudomo- containing dead mycelium than the wood with living mycelium (Smythe et al., 1971). nas and Sphingomonas/Zymomonas, Ochrobactrum, and to genera belonging to the family Contrary to this, ceratin fungal products from decayed wood, also act as repellents (Amburgey, Enterobacteriaceae. Besides this, few cellulolytic bacteria also house gut of Coptotermes 1979) and cause enormous death in termites (Roessler, 1932). Mostly brown rot fungus curvignathus (Holmgren) and Zootermopsis angusticollis.. Gloeophyllum trabeum degrades and de-polymerizes lignocellulose of wood (Highley et al., 1994; Gilbertson and Lindsey, 1975). It results in the darkening of wood and affect the (B) ANTAGONISTIC ASSOCIATIONS mechanical properties of wood (Highley et al., 1994). Interestingly, few fungus-growing termites Besides symbiotic associations, few microbes exhibit antagonistic relationships with termite propagate single variants of Termitomyces symbionts and form an exclusive lifetime associa- and kill them. Spores of these fungi infect the host, permeate in the body and poison the host tion in colony. Most commonly, symbionts are propagated vegetatively from the older bottom very fast. Fungus Conidiobolus xoronayus behave as an entomopathogenic fungi which infest to the newer top of a fungus garden. These associations imply vertical symbiont transmis- termites and show strong pathogenic effect in termite workers (Yoshimura et al., 1992). sions in fungus-growing termites, which is very rare evolutionary phenomenon. Similarly a mould fungi Metarhizium anisopliae, Paecilomyeces fumosoroseus, Beauveria bassiana (Suzuki 1991; 1995) and Aspergillus niger and Aspergillus flavus (Link) (Andrew Besides this, eukaryotic flagellates also play a major role in the degradation of lignocellulose. et al., 2001) cause pathogenesis in subtereanean termite, Coptotermes formosanus (Suzuki, Flagellates also possess prokaryotic symbionts. Similarly, a gut flagellate Joenia annectens is 1995) and Reticulitermes speratus (Milner et al., 1996 and Ahmad et al., 1997) Similarly few isolated from the termite Kalotermes and cockroach, Periplaneta americana that contains other fungi such as Trichoderma harzianum (Rifai), Trichoderma viren (Miller), Trichoderma methane-producing microbes, which generate volatile fatty acids and maintain low hydrogen asperillum (Samuels-Lieckfeldt & Nirenberg) and Trichoderma ghanense also show antago- pressure in the hind gut. Similarly, aerobic and facultative anaerobic bacteria also occur in gut nistic behavior to C. formosanus (Doi et al., 1987). Spores of these fungi are toxic to C. of red palm weevil (Rhynchophorus ferrugineus), which also help in wood feeding. A small ant formosanus termites, after reaching on to surface of the gut, these grow, replicate and spread Atta cephalotes contains fungus gardens of mostly endophytic and epiphytic fungi. Similarly, pathogenesis in termite population. Besides this, other strains such as G. trabeum. Aspergil- beetles also harbor a community of microbes in the gut, which helps in break down of lignin. lus flavus, Hypocrea virens (T. asperillum, along with Penicillium janthinellum (Biourge) These gut-borne fungi could potentially be harnessed to produce bio-fuel. Thus, microbes can and Cladosporium cladosporioides (Fres.) are also entomopathogenic to termites. (Suzuki, provide much cheaper and more efficient enzymes and can perform direct conversion of wood

Journal of Pharmacy Research Vol.4.Issue 4. April 2011 1161-1166 Ravi Kant Upadhyay et al. / Journal of Pharmacy Research 2011,4(4),1161-1166 into ethanol. Among hindgut microbiota of termites spirochetes occur more abundantly. These Table 1. Symbiotic and non-symbiotic microflora identified from various termite species. are monophyletic group of motile bacteria thatpossess a characteristic spiral or wavy shape Name of termite Microbial strain interact References

(Paster et al., 1991). Soil termites constitute an enormous reservoir of novel free living Symbiotic microbes spirochetes, which perform metabolic functions such as H /CO -acetogenesis and N fixation 2 2 2 O. formosanus Shiraki Trabulsiella odontotermitis (Chou et al, 2007) (Liburn et al., 1999). Gut microbial community, contributes cellulose digestion, nitrogen C. formosanus Beauveria basiana, Metarhizium anisopliae fixation and acetogenesis. These also show CO2-reductive acetogenesisover methanogenesis Myxotricha Termitomyces in the hindgut of many termites. Nitrogen fixation is also done by free-living spirochete. C. formosanus Pilibacter, Gordiococcus sp., Coccobacillary-NO, Dysgonomonas S1 and S2, Citrobacter, Citrobacter amalonaticus (3)BIOLOGICAL NITROGEN FIXATION Enterobacter cloace, Kleibseilla pneumoniae, Nitrogen fixation by the symbiotic gut micro-organisms is an important biological process Acinetobacter, Aeromonas sp. which has many biotechnological applications. This most remarkable biological phenomenon Pseudotrichonympha sp. (Protists) (Noda et al, 2007) Group 1 bacteria (Okhiuma et al, 2007) occurs in diversity of nitrogen fixing organisms in the gut of termites (Breznak, et al., 1973). O. formosanus Actinobacteria phylotyes (Shinzato et al, 2007) Termites feed on nitrogen deficient diet, therefore, to fulfill the nitrogen requirement, most of Reticulitermes Speratus Fibularhizoctonia sp (Matsmura et al, 2000) termite species fix nitrogen with the help of nitrogen fixing bacteria inhabiting he gut (Tayasu Wood termite Pseudotrichonympha grasi Rhizobia (Frolich et al, 2007) et al., 1994). Free living and facultative anaerobic bacteria do mostly this job. So far studies Fungus Growing termite Macrotermes subhyalinus (Auklin –Mulhemann et al, 2006) have been done bacteria which perform nitrogen fixation are identified as Enterobacter, Beijenk, Fungus Growing termite Termitomyces (Duur et al , 2009) Desulfuvibrio, Knlebsiella, Ensifer and Treponema. Reticulitermes flavipes Heterotrophic bacteria (Schultz and Breznak, 1978) Wood eating termite Enterobacter agglomerans (Portikus and Breznak 1976) C. formosanus Methanogenic bacteria (Tsunoda et al, 1993) The termite species such as Coptoremes formosanus, Neotermes koshunensis, Reticulitermes Reticulitermes flavipes Methanobrevibacter cuticularis, speratus and O. obesus possess symbiotic intestinal flora which possess nitrogen fixation Methanobrevibacter curvatus. (Leadbetter and Breznak1996) genes and perform biological nitrogen fixation. Diversity of nitrogen fixing genes is available Pilibacter termites Lactic acid bacteria Higashiguchi et al, both in lower and higher termites. Nitrogen fixing gene encodes dinitrogenase reductase is Wood-eating termites Paenibacillus, Streptomyces (Breznak and Pankratz1977) evolutionary conserved. There is an array of nifH genes have been identified in termite gut Reticulitermes flavipes (Kollar) Pseudomonas, Acinetobacter, Ochrubactrum. (Ohkuma et al., 1996). In C. formosanus and N. koshunens is alternative nitrogenase genes Coptotermes formosanus Non symbiotic microbes: and identified while C formosanus lack the this property. Both feeding habit and nutritional Coptotermes formosanus Trichoderma harzianum, Aspergillus flavus, ecology of the host termite after nif gene activity (Noda et al., 2002). Simialarly, lower Trichoderma virens, Trichoderma asperillum, termites possess significant levels of nitrogen fixing activity due to presence of anaerobic nif Trichoderma ghanense, Hypoccrea virens, Penicillium janthinellum, group consisting of Clostridia while higher termites possess most divergent nif group. Cladosporium cladosporiodes. Coptotermes formosanus, Gloeophyllum trabeum Brown rot fungus. Besides this, few termite species lack nif gene and possess anf gene that also paly an Lentnus lepideus. Coptotermes formosanus Metarhizium anisopliae (Suzuki et al, 1991, 1995) important role in nitrogen fixation in the termites. Mostly free-living aerobic and facultative C. acinaciformis Metarhizium anisopliae (Milner et al, 1996, Ahmad anaerobic N fixing bacteria performs this job. On average nitrogen, fixing aerobes Said et al, 1997) viz., Azotobacter and Beijerinckia spp fix 49 and 37% of nitrogen by oxidation in the salivary C. fenchi Metarhizium anisopliae Reticulitermes speratus Metarhizium anisopliae (Suzuki et al,1991, 1995) gland while facultative N fixing anaerobe viz., Klebsiella and Clostridium contributed 51% Nasutitermes exitiosus Metarhizium anisopliae (Hanel and Watson 1983, and 93%. More interestingly termite gut house free-living aerobic bacteria i. e. Azotobacter spp Milner et al, 1996, Ahmad normally 19 x 104 CFU mL-1 and Beijerinckia 13.2 x 104 CFU mL-1 in the salivary gland. Said et al, 1997) Interestingly, foregut, mid gut and hindgut possess a low population of these bacteria. Coptotermes formosanus Beauveria bassiana (Suzuki et al, 1991, 1995) Reticulitermes speratus Beauveria bassiana (Suzuki et al, 1991, 1995) Facultative N fixing anaerobes with in the hindgut of termites are mostly Klebsiella (20 x C. curvignathus Conidiobolus coronatus (Ahmad Said and Yaacob 1997) 104 CFU mL-1) and Clostridium pasteurianum (39.1 x 104 CFU mL-1). C formosanus Paecilomyces fumosoroseus (Suzuki et al,1991, 1995) Reticulitermes speratus Paecilomyces fumosoroseus (Suzuki et al, 1991, 1995) C formosanus Aspergillus niger (Suzuki et al,1991, 1995 MICROBIAL ECOLOGY OF THE TERMITE GUT Reticulitermes speratus Aspergillus niger (Suzuki et al,1991, 1995 Termites are known as dark-dwelling insects, which pass a cryptic life on decayed woody material and stay inside tunnels, shelter tubes and nests. They construct galleries from soil, that propels its host through the termite gut. A second type of bacteria synthesizes ATP, some feces, saliva and plant substrate materials. In orchards, gardens and in forests they forage of which is used by the spirochetes. The locomotion provided by the Spirochetes help the through tunnels under the soil or remain hide under the cover of mud shelter tubes. Only few ATP-producing bacteria to new food sources. The lactic acid secretary bacteria maintain termite species like narrow-nosed nasute termites (Tenuirostritermas sp) from North America ecological balance in the termite gut (Bauer et al., 2000). These help in recycle of carbon and workers forage in dark in open fields. For foraging termites emerge out from the hidden confines nitrogen via metabolizinguric acid (Potrikus and Breznak, 1981). Besides this large number of their galleries, tunnels, and foraging tubes. Termites mutually feed each other with saliva, of symbiotic flagellates and prokaryotes also occurs in termite gut, which show intracellular utilize partially digested food and then ejected feces. They also eat upon body carcasses of dead location. Among which Trichonympha sp. and Trichomonas sp. help the termites to digest companions and other organic waste materials and digest it them with the help of gut wood. Eukaryotic gut symbionts of lower termites are adapted to a cellulolytic environment. symbionts. Few termite species such as wood-eating termites Odontotermes and Coptotermes These produce nutriments using their own cellulolytic enzymes for the benefit of their termite mostly decompose branches, logs and tree- stumps with the help of microfauna present in their host. Possibly, these are evolved from symbiotic Archaezoa living in the hindgut of the most gut. They also help in recycling of organic matter, soil nutrients and help in nitrogen fixation primitive termite, Mastotermes darwiniensis. (Breznak et al,. 1973). Termites are not only insect pests but also an important part of the community of decomposers. A complete microbial system resides inside their gut which helps FORAGING BEHAVIOUR to break down wood products and recycle nutrients. Termites also help in mobilization of Termites posses a high level of coordinated foraging behavior. Termites are detrivorous and organic nitrogen (Rong et al., 2000), stability and fertility of soil in natural ecosystem xylophagous insects which forage on a much wider array of foods, including fine woody (Gillison et al., 2003; Matsui et al., 2009). debris, plant litter, leaf litter, dead grass, organic layers of soil, humus, highly decomposed wood, live wood, live herbaceous plants and grass, dung, fungi, fungus gardens, and lichens. Microbial community resides in termites varies in different geographical regions. It differs Most termites are adapted for hot, warm, and humid climates and show xylophagous habit and according to eco-climate conditions. Based on microorganisms present termites are divided feed on dead wood or plant litter. Termites attack the root system of mature plants and make into two groups lower and higher termites. The lower termites (Pterotermes occidentis) it hollow within and filled empty space of tunnel with soil (Johnson et al.,1981). Termites harbour a dense and diverse population of bacteria and cellulose digesting flagellate protozoa heavily infest crops from root to top and construct foraging galleries inside plants. Although mainly Trichonympha ampla, Pterotermes, Mixotricha paradoxa in their alimentary tract plant leaves remain green, the whole plant gradually dries up and lead to sudden wilting and which help in cellulose digestion (Cleveland in 1924). Besides this, lower termite such as death (Mercer, 1978). In contrast few termite species damage the plant by cutting the base of Coptotermes curvignathus (Holmgren) and higher termite Macrotermes gilvus (Hagen) pos- stem (Umeh et al., 1999), make tunnels and damage wood, agricultural crops and forest sess facultative anaerobes and identified as Enterobacter aerogenes, Citrobacter, Kluyuvera products (Inta et al., 2007). They construct large termitarium adjoining with tunnels and sp, Enterobacter cloacae and Clavibacter agropyri (Corynebacterium). Other microbiota come out to forage food. Termite foraging activity is extremely seasonal, as maximum observed were aerobes and facultative anaerobes (Bacillus sp., Salmonella sp.,Enterococcus consumption rates occurred from January to April and get slow in the month of July to sp., and Xanthomonas sp.(Khiyami and Alyamani, 2008) According to Yamaoka and Nagatani September (Ripa et al., 2007). Similarly damage has correlation with winter and spring (1975), termites themselves produce a cellulase, which differs from the cellulase produced by rainfall (Nash et al.,1998). the intestinal protozoa. Contrary to this, higher termites harbour a dense and diverse array of gut bacteria but lack protozoa. More specifically, Odontotermes obesus culture diverse micro- Termites exhibit behavioral adaptations for facultative transfer of microbial cultures from adult flora such as bacteria, coccoid and rod-shaped bacteria, along with spirochaetes, pseudomonads to youngs. Termites make feeding stimulating signal by secreting substances from the labial and actinomycetes inside their gut. glands. The secretion carries a water- soluble, heat resistant, nonvolatile signal that stimulates gnawing, feeding and aggregation in workers (Reinhard and Kaib, 2001). Termites show two Besides this, few protists like Mixotricha paradoxa also occur in termite gut which possess at types of feeding first is stomodaeal feeding, in which a mixture of varying proportions of least two kinds of bacteria attached to its outer surface. First category of bacteria are spirochetes

Journal of Pharmacy Research Vol.4.Issue 4. April 2011 1161-1166 Ravi Kant Upadhyay et al. / Journal of Pharmacy Research 2011,4(4),1161-1166 salivary secretions and regurgitated intestinal contents is received from another insect. The anaerobic cellulose digesting bacteria (Pochon et al.,1959) inside their gut which decompose second is proctodaeal feeding, in which a drop of the contents of the rectal pouch is obtained organic matter and change it into humus. Similarly Macrotermitinae (Termitidae) contains from the anus of another insect in response to tactile stimulation by the soliciting termite. ‘fungus gardens’ (Sands, 1960) composed of brown coral-like ‘comb’ constructed by workers Proctodaeal feeding ensures transfer of a fresh infection of flagellates from one termite to another by using small balls of comminuted vegetable matter, faecal pellets and fungal hyphae. The (Raina et al., 2008). Wood feeding insect termite produce two types of excrements, solid faeces chambers containing the fungus gardens are scattered throughout the nest, more concentrated and a liquid containing fragments of wood and intestinal flagellates. Such types of feeding near the royal cell. However, the symbiotic association of termites with ascomycetes and behavior has less nutritive value, but it helps in renewing the intestinal fauna of newly basidiomycetes fungus breaks lignin and cellulose, which are readily digested by the termites developed individuals. Thus worker termites transfer microbial cultures to young termites by (LaFage and Nutting, 1978; Rohrmann and Rossmann, 1980). These food items obtained in feeding or re-inoculation by proctodeal feeding (Grasse and Noirot, 1945). It helps to grow stomodaeal feeding serve as a source of vitamins and organic nitrogen. Wood eating termites, fungal comb in the hive and in galleries to feed young ones. Thus survival of newly founded which feed on a nitrogen deficient diet compiled by nitrogen fixing bacteria such as Klebsiella colonies depends on inoculation of the new comb with the fungus. The worker termites pneumoniae in their gut (Frohlich et al., 2007; Doolittle et al., 2008). More specifically, produce a comb of chewed wood on which the fungal hyphae grow and produce colonies. microorganisms not only help in deteriorating the plant material and make available for Termites use salivary secretions mixed with soil and wood particles to build tunnels and termites but sclerotium forming fungus protect termite’s eggs from putative pathogens (Matsuura galleries. et al., 2002). Symbiotic microorganisms inhabit in termites help in survival and existence of termite specific groups (Hayashi et al., 2007). NUTRIENT PHYSIOLOGY Termites are humivorous insects which mineralize humic and fulvic acids and release few Termite gut in a work place of so many microbes, which possess wood decomposition proteinceous compounds after wood deacy (Rong et al., 2000). The microbial community enzymes and have diverse array of capability for bio-fuel production. Presence of microbes is resides in the gut of termite worker plays a key role in nutrient physiology and ecology. highly essential for termite life, as without wood eating microbes, a termite would not be able Normally symbionts supply nutrients to termites and supplement nitrogen, sugars, vitamins to extract nutrients and energy from wood. Termites grind wood in to tiny pieces and provide and other mineral nutrients. Fungus growing termites receive few important enzymes like an oxygen free habitat within its gut. Some termite-gut microbes are bio-chemically capable cellulase, xylianase and nitrogen rich food in form of fungal hyphae. They also meet out energy of generating other potential fuels such as hydrogen or methane. Hydrogen produced by a demands of termites through methanogenesis and acetogenic reduction of CO2. The food group of microbes consumed by other gut microbes that helps to create energy producing by requirements and feeding habits of termites vary in castes and developmental stages (Cleve- products the termite could use. Termite gut microbes possess several novel enzymes capable land, 1924). Termites ascend to apex of the tree in search of food resources (Lee et al., 2007). of degrading cellulose in to fermentable sugars that can also help for processing plant biomass Their food includes vitamins like riboflavin (B-2), cyanocobalamine (B-12), L- ascorbic acid and bio-fuels. Thus, microbes are able to convert woody polymers to sugar that can be (C), and myo-insitol while some vitamins are also obtained from gut micro-organisms fermented in to fuels such as ethanol. Termites help the chomp the wood in to bits while (Rockstein, 1978). enzymatic juices excluded by microbes attack and deconstruct the cellulose and hemi-cellu- lose, which along with lignin and major building blocks of wood. Termites primarily consume the prepared foods and feeding preference is influenced by nutri- tional value of the food source. Cellulose and lignin are major feeding materials. Cellulose is CONCLUSION a polymer of glucose while lignin is a polymer of phenyl-propane units derived from cinnamyl The termite gut is a source of wide variety of bacteria and fungi including novel genera and alcohols. In plants ratio of lignin/cellulose varies from species to species (LaFage and Nutting, species. From scientific stand point of view, it has wider implications in biological research. 1978; Lee and Wood, 1971; Wood, 1978). Termites also digest living and decaying wood and It is most optimized and alternative specialized field to work, yet still evolving. However, other lignin depolemerizing agents (Gidh et al., 2006). Thus, microbes inhabiting in the positive interactions between termite and microbes can be used for agricultural and industrial termite gut of wood eating termites have a direct role in termite nutrition (Yoshimura, 1995, purposes after proper identification of strains, substrate utilized and synthesis of metabolic end Shelton and Grace, 2003) and feeding is partially influenced by the nutritional ecology (Sun, products. It will help in development of gigantic agricultural enterprises and benefits by 2007; Rojas et al., 2001). They also process and predigest lignocellulose and can decompose incorporation of beneficial genes like nif gene (nitrogen fixing), methanogenes and acetogenes. any type of plant detritus, wood, humus, and dung with help of gut symbionts. Termites feed Besides this, plant liter and wood decomposing microbial enzymes can be used for degrada- on dead plant material that consists of hollow, water transporting, vascular plant parts. They tion of harmfull polymers like polythene. This nonhuman agriculture system can be used for also utilize cytoplasmic nutrient reserves of living plant tissues. Thus, termites mostly rely on improvement of soil fertility in barren land areas by employing novel approaches of insect dead wood and withered leaves and grass, which are composed of polymers, cellulose and symbiont. Further, this goal can be achieved by applying outcomes of antagonistic approach lignin. Termites mostly prefer woody small twigs, leaves, and plant debris that contain of gut microbes. These methods can be used for management of termites by incorporation of lignocellulosic matter. This dead plant biomass having high caloric value, but low nutritive detrimental cellulose inhibitor genes by genetic engineering methods. For this purpose, value. controlled release of microbes is essential from lab to field. Besides this, conservation of gut microflora can play vital role in operation integrity of ecosystems including trophic relation- Termites help in nitrogen mobilization in tropical soil and release nitrogenous compounds ship, soil microstructures, processes, energy flow and recycling of materials through bio- after decomposition of organic matter. Nitrogenous products of termite origin may enter and be geochemical cycles. Thus, soil rehabilitation programs can be undertaken to increase the soil distributed within the ecosystem in several ways. Mainly nitrogen enters the ecosystem porosity, water holding capacity, improving water infiltration in to soil and humification. through direct deposition onto soil. Adult termites are able to pass nitrogen-containing Besides employment of microbes can reduce soil compaction and breaking up the surface compounds to their young ones through trophallaxis. This mutual exchange of food through crests. Incorporation of soil fauna especially termite can be used to improve soil structure. saliva work as the basis of soil system in insects (Wheeler, 1922; Richard, 1953). This transfer Termites can affect the soil by their burrowing and excavation activities in search of food, or the can occur from stomodeal food, proctodeal food, and salivary secretions (Waller and La Fage, construction of living species or storage chambers in the soil or above ground. However, 1987). Stomodeal food is food that is partially digested in the crop of the donating termite, structural solubility, porosity and decomposition process and chemical fertility of soil can be which is regurgitated and fed to a recipient termite. The dependent castes receive nutrients and managed up to large extent by termites. Termite can trigger above activities can mediate and digestive enzymes of this process. Although this behavior is not common among termites (La promote the rehabilitation of the degraded soil. Termites reduced run off and increased soil Fage and Nutting, 1978), it represents a possible mode of distribution of nitrogen containing water content through the plant growing period. Thus in semi acid condition termite activity compounds to colony members. Proctodeal food is transferred from the anus of donor termites. plays a key role in nutrient cycling and allow nutrient release from plant biomass after This food is also partially digested and differs from feces (Waller and La Fage, 1987). Flagellate decomposition. protozoans and other gut symbionts are transferred along with proctodeal food. Salivary secretions of termites are rich in lipids and proteins (La Fage and Nutting, 1978) provide as Besides this, bacterial enzymes can be used in wood digestion to turn agricultural plant wastes feed to dependent castes (Waller and La Fage 1987). to ethanol for the production of eco-friendly bio-fuel. Suitable enzyme extracted from gut microbes can be used for industrial processes. Besides this, termite gut micro-flora can be used DECOMPOSERS as organic recourses to improve soil productivity. It can also counteract land degradation Termites also decompose organic materials such as ploughed weeds, green manure and crop through their soil borrowing and feeding activities. Therefore, microbial density and ecologi- residues for foraging purpose (Mattew, 1989). Lignocellulosic matter is the most abundant cal studies on termite gut will open new approaches for insect control, industrial microbiology material produced annually in the biosphere by photosynthesis. Fungi are the main organisms and agricultural farming. Thus, termites can efficiently convert lingo-cellulose in to ferment- that consume it, and they are able to do so because their threads like hyphae, which secrets able sugar in their tiny bioreactors. This important process can convert biomass in to bio-fuel. appropriate enzymes for wood digestion. Wood-rotting fungi are extremely economical in Significant findings can be used for industrial scale system. In near future it will become a high their nutrient requirements. Vertebrate animals in general cannot derive sufficient nutriment priority research area. Certainly, outcomes of environmental management can be used for from lignocellulosic matter but ruminant ungulates or hoofed animals, utilize this abundant bioremediation, site reclamation, improvement of soil fertility and become a potential source matter as food. However, a few groups of insects have evolved a successful detritivorous habit, of genes of agricultural importance . which coevolved symbiotic relationships with microbial organisms such as bacteria, protozoa and fungi. The protozoa ingest wood particles, are capable of digesting cellulose in the gut, and ACKNOLEDGEMENT decomposed into glucose (Hungate, 1943). Nevertheless, in some species such as Zootermopsis Author is highly thankful to University Grants Commission, New Delhi, for cellulose degrades into carbon dioxide, hydrogen and acetic acid, which is absorbed and providing financial assistance metabolized by the termites. At each nymphal moult the flagellates are lost (Grasse and Noirot, 1945) but these are rapidly retained through proctodaeal feeding (Andrew, 1930). Contrary to REFERENCES this, members of family Termitidae do not inhabit protozoans to digest cellulose but have 1. 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