Abstract
It is well known that the use of insecticides is very effective in combating the immediate problem of insect attack on crops. But the recurrent use of the chemical insecticides is paving way to the 3R (residue, resurgence, and resistance) problems in food, in environment, and in insects. There is an alternative method for managing the insect pest problem in crop plants. The use of insect gut microbes serving as a biocontrol method to manage the insect pest problem is based on the concept of managing the BUG with BUG. To implement this concept, it should be clear about the type of microorganisms present in the host insect and their important contribution to the host insect success. Hence, the main objectives of this chapter are (1) to provide a brief overview of bacterial phylotypes present in the different orders of class Insecta and their functional role play in the host insect survival by protecting from the harmful effects of insecticides, biocontrol agents, toxic chemicals of host plant, etc., (2) to emphasize about the loss of gut microbes due to antibiotic treatment, which causes developmental deformities in the host insect, and (3) to address the potential of gut bacteria in the area of crop production with their multifaceted plant-growth-promoting (PGP) characteristics. To assess this, special emphasis is given to the bacterial phylotypes isolated from the cruciferous specialist diamondback moth – Plutella xylostella – and their significant characteristics such as antifungal activity through chitinase, β-1,3-gluconase activity, HCN, siderophore production, IAA and 1-aminocyclopropane-1-carboxylate deaminase activity, nitrogen fixation and solubilization of P and Zn, and oxidation of sulfur. Based on the literature reviewed in this chapter, it could be concluded that the use of gut microbe may serve as a novel avenue for crop, pest management, and production by improving their beneficial characteristics, for instance, chitinase and siderophore production.
Access provided by Autonomous University of Puebla. Download chapter PDF
Similar content being viewed by others
Keywords
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.
14.1 Introduction
The existence of an intimate relationship between many insect species and large numbers of microorganisms has been known for over a century. The success of insects has created myriad of opportunities for bacteria to occupy niches created by insects. The guts of insects offer such niches where the insects are able to take advantage of the products of bacterial metabolism and the adaptability of the prokaryotes. These insect–host and microbe associations form a dynamic spectrum in relation to the necessity as well as physiological impact toward those involved. The association of insects with a wide variety of bacteria includes beneficial endosymbionts, occasional disease causing entomopathogens, and harmless transient cuticle contaminants acquired from the environment (Wernegreen 2002). Endosymbiotic bacteria may be extracellular or intracellular and can be found in the digestive system, hemocoel, reproductive tract, or localized in specialized cells called mycetome. The interplay between insects and the microorganisms inhabiting the gut was recognized as early as 1929. In this year, Wigglesworth (1929) suggested that blood sucking triatomines, which feed solely on blood during its whole life cycle, would have symbionts to provide the insects with complex B vitamins. Bacterial symbionts have also been implicated in furnishing nutrients to sap feeders (aphids, psyllids, whiteflies, mealybugs, etc.). In aphids, the bacterium Buchnera was found to utilize nonessential amino acids present in the phloem sap to produce essential amino acids, completing the dietary needs of aphids (Shigenobu et al. 2000; Moran et al. 2003; Wilcox et al. 2003).
Insects living on nutrient-poor diets, where amino acids are very scarce like wood and humus, benefit from symbiotic bacteria that are able to fix atmospheric nitrogen and synthesize amino acids (Nardi et al. 2002). Nevertheless, gut microbes are not limited to insects with unbalanced diets, but could also be involved in insect temperature resistance (Montllor et al. 2002), host plant detoxification (Lauzon et al. 2003), and parasite protection (Olivier et al. 2003). Most of the arthropod symbioses involve highly specific interactions, often between one bacterial species and one insect (Kikuchi et al. 2005). There are a few examples of multispecies communities, such as the associates of the hindgut of termites. Degradation of complex carbohydrates and fixation of nitrogen form the metabolic foundation for the community’s function (Nakashima et al. 2002; Bakalidou et al. 2002). The intricacies of managing the carbon and nitrogen economy of the hindgut provide evidence for interdependence and coevolution among the members of the community. The termite system offers one of the most powerful existing models for studying nutritional interactions among community members.
Evidence for a more interactive relationship between microbiota and host was assessed by many researchers (Dillon and Dillon 2004; Genta et al. 2006). Barring situations in the relationships between insects and their microbiota remain under-researched and largely undefined. Studies have often been restricted to a catalogue of species present (Sittenfeld et al. 2002; Broderick et al. 2004; Xiang et al. 2006). This might be due to the culture-independent method of analysis of such interrelationships. In order to evaluate the functional significance of the gut bacteria to the host insect, the bacterial isolate should be cultivable under in vitro condition (Mohr and Tebbe 2007).
Thus, the interactions between insects and their microbial symbionts have provided the bases for many principles in symbiosis and have revealed unexpected mechanisms that illustrate how organisms cooperate to perform life functions and gain a competitive edge.
This chapter describes some of the bacteria associated with the class Insecta and their functional role in insect host nutrition and development. Furthermore, insight is given into the possible use of insect gut bacteria as potential plant-growth-promoting bacteria (PGPB) for crop production.
14.2 Functional Significance of Insect Gut Bacteria
Numerous studies in the past have described the microbial gut community using classical techniques, but little information was provided on its biological role. A number of reviewers commented on the lack of information on the biological role of the insect microbiota. Brooks (1963) stated that further isolation and characterization of insect intestinal biota were pointless unless they were correlative with either the ability of the host to control its biota or the effect of the biota on the host’s physiology. The microbial midgut inhabitants seem likely to benefit the insect host, based on the results of studies conducted with different insect orders by various researchers (Takatsuka and Kunimi 1998, 2000; Lauzon et al. 2003; Dillon and Dillon 2004; Behar et al. 2005; Xiang et al. 2006; Indiragandhi et al. 2007a, 2008a; Figs. 14.1 and 14.2). Gradually, literature related to the biological roles of gut bacteria to the host insect has been increasing. Some of the reported examples of benefits/biological roles of gut bacteria include its assistance in host insect morphogenesis (Zacharuk 1976a, b; Iverson et al. 1984) and food digestion (Borkott and Insam 1990), detoxification of plant allelochemicals and xenobiotics (both synthetic and biopesticides), disease resistance by providing antimicrobial metabolites, and modification of midgut pH by their own metabolism, thereby conferring protection against indigenous and invading pathogenic microorganisms.
14.2.1 Role of Chitinase Produced by Gut Bacteria in Host Insect Processes
Chitin is one of the most important biopolymers in nature. In insects, it supports the cuticles of the epidermis and trachea as well as the peritrophic membrane (PM) lining the gut epithelium. An invertebrate–unique structure, the PM, is irreversibly permeable to secreted digestive enzymes and to the products of digestion (Chapman 1985). Insect growth and morphogenesis are strictly dependent on the capability to remodel chitin containing structures and food materials. For this purpose, insects repeatedly produce chitin synthases and chitinolytic enzymes in different tissues. In the context of morphogenesis, chitinolytic activity of the gut bacteria helps in the emergence of an adult from puparium (Iverson et al. 1984). Similar observations were reported in certain coleopterans in which gut bacteria were found to secrete enzymes capable of digesting portions of the pupal case, thereby weakening the wall and facilitating emergence. Winicur and Mitchell (1974) demonstrated that chitinase was present in the molting fluid of Drosophila melanogaster and described about the digestion of endocuticular chitin before larval emergence. It seems that a low level of chitinase activity imparted by the symbiotic bacteria is essential for the host insect throughout its life cycle (Iverson et al. 1984). It has been anticipated that gut microbial symbionts in the intestinal tract can be situated in the gut lumen or associated with the gut epithelium or PM (Buchner 1965). Likewise, studies on the house cricket (Acheta domestica) indicated that part of the bacterial gut microbiota is attached to the PM in the midgut, the gut wall, and cuticular bristles in the hindgut. The ability of insects to digest the chitin containing food resource is rather limited and is often dependent on symbiotic microorganisms. For instance, Brendelberger (1997) observed that the chitinase activity was parallel with the reduction in bacterial numbers in the host gut after antibiotic treatment. It indicates that chitobiase was not synthesized by the host but was taken up by bacteria from the food. This bacterial origin of chitinolytic enzymes was also shown by Genta et al. (2006) for the digestion of cell wall of wheat bran in yellow mealworm, Tenebrio moliter (Tenebrionidae), and in some other insects, in the digestion of their own exuvia (Mira 2000).
One more example for the evidence of chitinase produced by gut bacteria on host insect process is with the tsetse fly and its gut bacteria, Sodalis glossinidius. S. glossinidius has been shown to play a role in potentiating its host’s susceptibility to trypanosome infection by influencing the efficacy of the tsetse immune system (Welburn and Maudlin 1991, 1999). In the tsetse fly, it is known that trypanosomes can only be established in the fly midgut if these parasites can successfully evade the action of an N-acetyl-d-glucosamine (GlcNAc), a specific trypanocidal lectin which is secreted during feeding (Maudlin and Welburn 1987). Sodalis is thought to influence lectin activity through the production of lectin-inhibitory sugar (GlcNAc), which is known to accumulate during pupal development as a result of this bacterium’s chitinolytic activity (Welburn et al. 1993). More recently, it has been shown that the chitinase-producing gut bacteria (Fig. 14.1) isolated from P. xylostella increased the host insect consumption index (CI), relative growth rate (RGR), approximate digestibility (AD), efficiency of conversion of ingested food (ECI), and efficiency of conversion of digested food (ECD) (Table 14.1) (Indiragandhi et al. 2008a).
14.2.2 Gut Bacteria Mediated Detoxification of Allelochemical and Xenobiotics
Miyazaki et al. (1968) documented the significant role of gut bacteria Rhagoletis to detoxify harmful plant compounds, thereby protecting the host fly. Bacterial culture of Pseudomonas spp. could break down a variety of pesticides, apparently through the hydrolytic action of strong esterases, and might synthesize amino acids essential for growth of the maggot. Furthermore, gut microbes are reported for their detoxification of allelochemicals such as flavanoids, tannins, and alkaloids (Lauzon et al. 2003). There has been a report on bacterial modification of plant phenolics leading to the production of volatile phenolics in the locust Schistocerca gregaria to give guaiacol, a component of the locust aggregation pheromone (Dillon and Dillon 2004). Pseudomonas aerugenosa was reported for its detoxification of the plant secondary metabolite polyketide known as pederin in Paederus beetle (Piel 2002). Participation of gut bacteria Pantoea (=Enterobacter) agglomerans (a common inhabitant of fruit fly and its host plant apple) in biochemical transformation of plant allelochemical dihydrochalcone phloridzin has been explored for Rhagoletis pomonella. Since the extent to which insects catabolize harmful compounds in their digestive tracts or on their host plant is of considerable importance to their survival (Lauzon et al. 2003), it would be possible that when insects feed on plant materials that contain plant-produced defensive toxins or/are exposed to insecticides or other pesticides. Therefore, it is likely that the gut bacteria are also exposed to these toxins and may actually contribute to detoxification of these compounds (Davidson et al. 2000; Genta et al. 2006), since gut microbes can adapt rapidly to changes in the diet of the insect by changing the population profiles and induction of requisite enzymes (Santo-Domingo et al. 1998). Therefore, the ability of microbes to modify or detoxify plant allelochemicals is an additional property that may be important in certain insect–microbe relationships (Dillon and Dillon 2004).
Most insects detoxify chemicals by converting lipophilic compounds to more water-soluble compounds that are more easily excreted. A well-known enzyme responsible for this detoxification action is glutathione-S-transferase (GST), which is widely distributed in all living organisms. So far, reports indicate that the action of GST in the insect gut is the well-explored enzyme in the detoxification of insecticides sprayed against the insects (Mohan and Gujar 2003a). Some studies reported that the bacterially produced enzymes were responsible for the detoxification of toxic substances in host insects. For instance, field-collected strains of Spodoptera frugiperda (J.E. Smith) showed high activity of detoxification enzymes, namely, microsomal oxidases, glutathione S-transferases, and hydrolase (Yu 1992). Interestingly, the enzyme phosphotriesterase (PTE) from microorganisms in soil seems to be associated with the detoxification of organophosphorous pesticides and organophosphate resistance mechanism in insects. PTE was first detected in the soil microoganisms, Pseudomonas diminuta and Flavobacterium sp., which are capable of hydrolyzing paraoxon and parathion at a high catalytic rate (Munnecke and Hsieh 1974). Gut isolates of P. xylostella which are resistant to prothiofos were shown to have increased activity of GST than that of the same but susceptible field population (Indiragandhi and Sa, unpublished data). The high reliance to insecticides for the control of insect pests and the repeated use of the same insecticides may result in significant reduction of their biological efficacy. This loss of efficacy might be attributed to the rapid microbial degradation of insecticides by a gut symbiotic microflora as reported in soil applied nematicides (Karpouzas et al. 2005). Therefore, the enzymes of gut bacteria might contribute to the detoxification of insecticides in insects, consequently giving rise to resistance development.
14.2.3 Gut Bacteria Mediated Disease Resistance in Host Insect
The insect intestinal tract is generally inhospitable to fungi and infection rarely occurs via the gut. This is surprising as both foregut and hindgut are lined with unsclerotized cuticle, which is actively invaded, for example, in locust by an adapted fungal pathogen. It was generally thought that anaerobiosis, digestive enzymes, adverse pH, speed of food throughput, and protection from the peritrophic membrane are primarily responsible for the gut barrier to fungi (Dillon and Charnley 1991). However, none of these factors can account for the failure of the conidia of M. anisopliae to germinate in the guts of locusts (Dillon and Charnley 1991). Since the guts of germfree locusts do not have such inhibitory properties, it was concluded that an antifungal toxin was produced by the gut microbiota of the locust. Subsequently, antimicrobial phenolic compounds were purified from the gut and fecal pellets of conventionally reared locusts. Three phenolics were identified using GC-MS, namely, hydroxyquinone, 3,4-dihydroxybenzoic, and 3,5-dihydroxybenzoic acids. These compounds were not detected in fractions from germfree insects. A solution of authentic phenols inhibited germination of M. anisopliae at concentrations estimated to occur in the fecal pellets. When Pantoea agglomerans, a prominent member of the microbial population in the locust gut, was introduced into germfree insects the antifungal compounds reappeared in the feces in proportion to the size of the gut bacterial population (Dillon and Charnley 1995, 1996). In Hymenopteran social insect honeybees, in addition to the genetically determined hygienic behavior (uncapping of cells and removal of diseased and dead larvae) toward the Chalkbrood disease caused by Ascosphaera apis, gut bacteria of worker bees such as Paenibacillus alvei, B. circulans, B. licheniformis, B. megaterium, B. pumilus, and B. subtilis were reported for the host insect resistance to disease (Gilliam 1997). The phenolics produced by the gut microbiota are toxic to a wide range of insect and plant pathogenic fungi and insect pathogenic bacteria (Dillon and Charnley 2002). Antifungal activity of gut bacteria isolated from P. xylostella was reported for entomo- and phytopathogenic fungi under in vitro condition (Table 14.2 and Fig. 14.3) (Indiragandhi et al. 2007a, 2008a). The gut bacterial isolates showed significant activity of biocontrol determinants such as siderophore (Fig. 14.4), chitinase, and β-1,3 glucanase (Tables 14.3 and 14.4). Consequently, the antifungal activity of gut bacteria toward entomopathogenic fungi might be due to the action of individual or combination of all the biocontrol determinants. For the former case, it could be explained that the antibiotic activity might be due to the siderophore and its cross-utilization of siderophores produced by the fungal pathogens (Indiragandhi et al. 2008a, b) (Table 14.4).
14.2.4 Gut Bacteria Mediated Protection Against Biopesticides
The soil bacterium, Bacillus thuringiensis (Bt), is an important component of insect pest management program all over the world. Insecticidal proteins of Bt are effective for controlling many insect species, but insect resistance to Bt threatens the long-term effectiveness of these toxins (Oppert et al. 1997; Mohan and Gujar 2003b). The salient feature of this species is the accumulation of crystalline parasporal inclusions during sporulation. These inclusions are composed of one or more protoxins, known as δ-endotoxins, each of which is specific primarily at the level of insect orders, particularly Lepidoptera, Diptera, and Coleoptera. In Lepidoptera, specificity is in part due to the extremely alkaline midgut environment that is required to solubilize the protoxin into the active form (Broderick et al. 2004). In vivo, protoxins of 120 kDa undergo proteolytic conversion to active toxins of 60–65 kDa through the action of gut protease activity at high pH in the larval midgut. Several mechanisms of insect resistance to Bt toxin have been proposed, such as reduced binding of toxin to larval brush border membrane vesicle which results in increased resistance in the Indian meal moth – Plodia interpunctella, tobacco budworm, Heliothis virescens, and beet armyworm, Spodoptera litura (Oppert et al. 1997). However, in some insect species the development of resistance to Bt has been linked to altered gut protease activity that interacts with Bt toxins. Possibly, these protease enzymes in the gut juice would originate from the gut bacterial genera present in the host insect. Few studies have indicated the inhabitation of the lepidopteran insect gut by different phylotypes of bacteria and their role in determining the insecticidal activity of Bt (Takatsuka and Kunimi 2000; Broderick et al. 2004). Midgut pH is important from the perspective of both the microbes and the insect. A predominant member of the midgut microbial community, Enterobacter faecalis, is commonly found at higher pH (8–9) and acidifies its environment through its metabolism (Manero and Blanch 1999). This could confer some advantage to the insect host, as well-known microbial toxins of Lepidoptera such as Bt toxin are activated only in alkaline conditions (Wilson and Benoit 1993). Thus, E. faecalis might protect the insect from Bt toxin by decreasing the midgut pH as evidenced by the smaller population of E. faecalis in the larvae of more susceptible insects to Bt toxin (Broderick et al. 2003). The bacteria may also contribute to their own survival by managing midgut pH to enhance their own growth or exclude competing microorganisms. This was demonstrated in the reduction of Bt growth to about 20 times lesser than that of larvae without true gut bacteria Staphylococcus sp. and Streptococcus sp. of lepidopteran oriental tea tortrix, Homona magnanima (Takatsuka and Kunimi 2000). On the other hand, it was shown that the siderophore produced by the gut bacteria cross-utilizes the siderophore produced by other bacteria and fungi (i.e., entomopathogenic fungi and bacteria), such as Bt through their outer membrane receptor protein (OMRP) (Table 14.4 and Fig. 14.5) (Indiragandhi et al. 2008a).
14.2.5 Gut Bacteria Mediated Nitrogen Fixation in Insects
Nitrogen, although abundant in the atmosphere, is paradoxically a limited resource for multicellular organisms. In the class Insecta, biological nitrogen fixation has been greatly demonstrated in termites. Even though termite gut cells are now known to be capable of digesting lignocellulose without direct assistance from gut symbionts (Bignell 2000), no cells of arthropod guts are competent to fix nitrogen or to convert carbon dioxide to acetate. These two anaerobic activities are the sole province of the gut microbes. Microbial acetogenesis in termite guts has been demonstrated to provide at least one third of the energy requirements of termites (Breznak 2000). Anaerobic prokaryotes provide their arthropod hosts with important nutritional benefits that cannot be provided by eukaryotic cells alone. Behar et al. (2005) found that all individuals of field-collected mediterranean fruit flies, Ceratitis capitata, harbor large diazotrophic enterobacterial populations that express dinitrogen reductase in the gut. Moreover, nitrogen fixation was demonstrated in isolated guts and in live flies. This may significantly contribute to the fly’s nitrogen intake. The presence of similar bacterial consortia/activity in additional insect orders such as Lepidoptera (Table 14.3) (Hameeda et al. 2006b; Indiragandhi et al. 2008b) suggests that nitrogen fixation occurs in vast pools of terrestrial insects. On a large scale, this phenomenon may have a considerable impact on the nitrogen cycle (Behar et al. 2005). Insect gut bacteria associated with various orders of insects and their functional role in insects are summarized in Table 14.5.
14.3 Potential of Antibiotic Therapy for Insect Pest Management
The literatures reviewed under the various topics highlighted the importance of gut bacteria to the host insect species. The loss of gut bacteria often results in detrimental fitness costs for the host, such as growth impairment, shortened life span, and sterility, while their presence contributes to insect morphogenesis, digestion, nutrition, protection against toxic substances, pheromone production, and even reproduction (Brand et al. 1975; Buchner 1965; Nolte 1977; O’Neill et al. 1992). Evidently, the reduction or elimination of the gut bacteria in insects by antibiotic therapy would certainly cause deleterious effects on the host insect. For instance, Costa et al. (1997) evaluated the effect of different substances on the growth and development of whiteflies. They found significant negative effects on growth and development of whiteflies due to the bacterial protein synthesis affected by the test substances such as tetracycline and rifampicin. Likewise, the removal of Buchnera with antibiotics severely debilitates aphid performance and fecundity (Koga et al. 2007). Broderick et al. (2000) observed that lepidopterous larvae fed on antibiotics in various combinations display numerous signs of reduced health. For example, a cocktail of antibiotics including tetracycline reduced larval survival by 50% over the first 20 days after hatching, and the surviving larvae weigh one tenth of the untreated control larvae. Tetracycline alone has a similar effect on development, whereas gentamicin, rifampicin, and penicillin have no effect on survival or growth. Another antibiotic, zwittermincin A, dramatically increases larval sensitivity to the insecticidal toxin produced by Bt and also alters the population size of more than one member of the gut community. It is possible that a change in the gut microbiota may inhibit larval growth, instar development, and make the larvae more sensitive to pathogens and toxins. Thus, gut bacteria provide a potential target for insect control with systemic antibacterial materials, or transgenic plants that produce antibacterial proteins (Jaynes et al. 1987). With reference to P. xylostella, antibiotic-treated leaf-fed larvae showed malformed adult development and failed to successfully develop into pupae (Indiragandhi and Sa, unpublished data).
14.4 Insect Gut Bacteria as Biocontrol Agents and PGPB
Genetic modification of gut isolates which are mildly pathogenic to their host may be exploited as biocontrol agent. For example, Enterobacter cloacae WFA73, a mild pathogen to Bemisia argentifolii, has the ability to penetrate whitefly gut cells, which suggests that this microorganism could be genetically modified to enhance its effectiveness as a biological control agent. A similar report has been documented for soil microarthropods by Thimm et al. (1998).
Simultaneously, it is possible to exploit the insect gut bacterial isolates for the enhancement of growth and development of crop plants. The transformation of a phyllosphere bacterium, Bacillus megaterium, with Bt toxin genes for the control of Lepidoptera is an example of such manipulation (Bora et al. 1994). Similar modification of gut bacteria in other insects, to alter their ability to vector plant viruses or other characteristics of these insects, is also an interesting possibility (Richards 1993).
It could be noticeable that there is a tritrophic interaction between plant–insect–bacteria. As well documented, insect guts are known for their microbial population, which is able to fix atmospheric nitrogen, have the ability for mineral solubilization and oxidation and possess hydrolytic enzymes such as chitinase and indole derivatives.
Most reported PGPB are rhizosphere, phyllosphere, and soil isolates, except for a few from milk and cow dung (Nagarajkumar et al. 2004; Swain and Ray 2007). The microbial population in insect guts (4 × 105 to 2 × 1011 ml−1 of gut suspension) is greater than that in the phyllosphere (3 × 105 cm−2) (Jacques et al. 1995), representing a well-explored niche for beneficial bacterial isolation. It is assumed that many insect species derive their microbiota from the surrounding environment, for instance, the phylloplane of plants (Dillon and Dillon 2004; Kremer and Souissi 2001). Presumably, the nutrient cycling rates in the gut environment are much higher and the potential disturbances are more dramatic than in soil and plants. Crop plants generally immobilize the nutrients in their leaves. Insects also have well-developed mouth parts that are used to grind and shred organic substances, making insects more accessible for microbial colonization. Insect gut bacterial strains are also more metabolically versatile than isolates from elsewhere (Dillon and Dillon 2004). Spiteller et al. (2000) reported that the metabolic products produced by gut bacteria of Spodoptera exigua, Mamestra brassicae, and Agrotis segetum play a role in triggering a range of systemic responses with the result of larval feeding. Synthesis of N-acyl amino acid by the gut bacteria of Spodoptera exigua attracts the predators of the herbivores, when the host insect regurgitates its oral secretions. Findings of this study indicated that the involvement of bacteria in the biosynthesis of compounds which play a pivotal role in the interaction of plants, herbivores, and their predators adds a new trophic level to this complex network of interactions.
The gut passage may also enhance rates of decomposition by inoculating the organic material with bacteria, which might continue to grow outside the gut in the feces. After getting into the soil, the bacteria in the feces can establish in the rhizosphere. Living plant roots exude organic compounds, e.g., water-soluble sugars, amino acids, and organic acids into the rhizosphere, which in turn utilize the products of bacterial metabolism for plant growth. Bacterial features such as the ability to produce ACC (1-aminocyclopropane-1-carboxylate) deaminase, indole derivatives (IAA), and salicylic acid (SA) could benefit plants by restraining the inhibition of root elongation by reducing the level of stress ethylene (Fig. 14.6). SA also acts as (1) a signaling compound in inducing systemic resistance against insect and disease attack and (2) antimicrobial agent (Indiragandhi et al. 2007b). By using the sugar compound as growth substrate, bacterial strains could produce some organic acids, which lead to solubilization of insoluble nutrients such as P and Zn and make them available to crop plants. This may be the reason behind the hypothesis that the insect herbivores can accelerate nutrient mobilization in soil. A number of bacterial isolates colonizing insect gut area have been reported for its potential for plant-growth promotion. Bacterial isolates from the macrofauna and P. xylostella were reported for their antagonistic activity against various phytopathogenic fungi, solubilization of rock phosphate by the gluconic acid production, siderophores, ACC deaminase, and hydrolytic enzyme production (Hameeda et al. 2006a, b; Indiragandhi et al. 2008b). Siderophores and indole derivatives synthesized by the insect gut bacterial strains were documented for their antagonistic activity against soil-borne pathogen (Ciche et al. 2003). Bacterial strains of P. xylostella significantly inhibit the phytopathogenic fungal growth and enhanced the seedling growth and vigor in economically important crops such as canola, tomato (Indiragandhi et al. 2008b) (Table 14.6), rice, chili, and maize (Indiragandhi and Sa, unpublished data).
14.5 Future Thrust
This review of earlier studies is indicative of the possibility of utilizing the insect gut bacterial strains as biocontrol agent and PGPB. Therefore, isolation, characterization, and exploitation of microbes from such specialized dynamic environments represent a step forward in the development of bioinoculants for increased crop production through effective crop protection.
References
Adams L, Boopathy R (2005) Isolation and characterization of enteric bacteria from the hindgut of formosan termite. Bioresour Technol 96:1592–1598
Bakalidou A, Kampfer P, Berchtold M, Kuhnigk T, Wenzel M, Konig H (2002) Cellulosimicrobium variabile sp. nov., a cellulolytic bacterium from the hindgut of the termite Mastotermes darwiniensis. Int J Syst Evol Microbiol 52:1182–1192
Behar A, Yuval B, Jurkevitch E (2005) Enterobacteria-mediated nitrogen fixation in natural populations of the fruit fly Ceratitis capitata. Mol Ecol 14:2637–2643
Bignell DE (2000) Introduction to symbiosis. In: Abe T, Bignell DE, Higashi M (eds) Termites: evolution, sociality, symbioses, ecology. Kluwer Academic Publishers, Dordrecht, pp 189–208
Bora RS, Murty MG, Shenbagarathai R, Sekar V (1994) Introduction of lepidopteran-specific insecticidal crystal protein gene of Bacillus thuringiensis subsp. kurstaki by conjugal transfer into a Bacillus megaterium strain that persists in the cotton phyllosphere. Appl Environ Microbiol 60:214–222
Borkott H, Insam H (1990) Symbiosis with bacteria enhances the use of chitin by the springtail, Folsomia candida (Collembola). Biol Fertil Soils 9:126–129
Brand JM, Bracke JW, Markovetz AJ, Wood DL, Browne LE (1975) Production of verbenol pheromone by a bacterium isolated from bark beetles. Nature 254:136–137
Brendelberger H (1997) Bacteria and digestive enzymes in the alimentary tract of Radix peregera (Gastropoda: Lymnaeidae). Oecologia 42:1635–1638
Breznak JA (2000) Ecology of prokaryotic microbes in the guts of wood and litter feeding termites. In: Abe T, Bignell DE, Higashi M (eds) Termites: evolution, sociality, symbiosis, ecology. Kluwer Academic Publishers, Dordrecht, pp 209–231
Broderick NA, Goodman RM, Raffa KF, Handelsman J (2000) Synergy between zwittermicin A and Bacillus thuringiensis subsp. Kurstaki against gypsy moth (Lepidoptera: Lymantriidae). Environ Entomol 29:101–107
Broderick NA, Goodman RM, Handelsman J, Raffa KF (2003) Effect of host diet and insect source on synergy of gypsy moth (Lepidoptera: Lymantriidae) mortality to Bacillus thuringiensis subsp. kurstaki by zwittermicin A. Environ Entomol 32:387–391
Broderick NA, Raffa KF, Goodman RM, Handelsman J (2004) Census of the bacterial community of the gypsy moth larval midgut by using culturing and culture independent methods. Appl Environ Microbiol 70:293–300
Brooks MA (1963) Symbiosis and aposymbiosis in arthropods. Symp Soc Gen Microbiol 13:200–224
Broza M, Pereira RM, Stimace JL (2001) The nonsusceptibility of soil collembola to insect pathogens and their potential as scavengers of microbial pesticides. Pedobiologia 45:523–534
Buchner P (1965) Endosymbionts of animals with plant microorganisms. John Wiley & Sons, Inc., New York
Chapman RF (1985) Structure of the digestive system. In: Kerkut GA, Gilbert LI (eds) Comprehensive insect physiology biochemistry and pharmacology. Pergamon Press, New York, pp 165–211
Ciche TA, Blackburn M, Carney JR, Ensign C (2003) Photobactin: a catechol siderophore produced by Photorhabdus luminescens, an entomopathogenic mutually associated with Heterorhabditis bacteriophora NC1 nematodes. Appl Environ Microbiol 69:4706–4713
Costa HS, Henneberr JT, Toscano CN (1997) Effects of antibacterial materials on Bemisia argentifolii (Homoptera: Aleyrodidae) oviposition, growth, survival and sex ratio. J Econ Entomol 90:333–339
Davidson EW, Rosell RC, Hendrix DL (2000) Culturable bacteria associated with the whitefly, Bemisia argentifolii (Homoptera: Aleyrodidae). Fla Entomol 83:159–171
de Vries EJ, Breeuwer JAJ, Jacobs G, Mollema C (2001) The association of Western flower thrips, Frankliniella occidentalis, with a near Erwinia species gut bacteria: transient or permanent? J Invertebr Pathol 77:120–128
Dillon RJ, Charnley AK (1991) The fate of fungal spores in the insect gut. In: Cole GT, Hoch HC (eds) The fungal spore and disease initiation in plants and animals. Plenum Press, New York, pp 129–156
Dillon RJ, Charnley AK (1995) Chemical barriers to gut infection in the desert locust: in vivo production of antimicrobial phenols associated with the bacterium Pantoea agglomerans. J Invertebr Pathol 66:72–75
Dillon RJ, Charnley AK (1996) Colonization of the guts of germ-free desert locusts, Schistocerca gregaria, by the bacterium Pantoea agglomerans. J Invertebr Pathol 67:11–14
Dillon RJ, Charnley AK (2002) Mutualism between the desert locust Schistocerca gregaria and its gut microbiota. Res Microbiol 153:503–509
Dillon RJ, Dillon VM (2004) The gut bacteria of insects: nonpathogenic interactions. Annu Rev Entomol 49:71–92
Dillon RJ, Vennard CT, Buckling A, Charnley AK (2005) Diversity of locust gut bacteria protects against pathogen invasion. Ecol Lett 8:1291–1298
Franke IH, Fegan M, Hayward C, Leonard G, Stackebrandt E, Sly LI (1999) Description of Gluconacetobacter sacchari sp. nov., a new species of acetic acid bacterium isolated from the leaf sheath of sugarcane and the pink sugarcane mealybug. Int J Syst Bacteriol 49:1681–1693
Genta FA, Dillon RJ, Terra WR, Ferreira C (2006) Potential role for gut microbiota in cell wall digestion and glucoside detoxification in Tenebrio molitor larvae. J Insect Physiol 52:593–601
Gilliam M (1997) Identification and roles of non-pathogenic microflora associated with honey bees. FEMS Microbiol Lett 155:1–10
Hameeda B, Reddy HK, Rupela OP, Kumar GN, Satyavani K (2006a) Effect of carbon substrates on rock phosphate solubilization by bacteria from composts and macrofauna. Curr Microbiol 53:298–302
Hameeda B, Rupela OP, Reddy G, Satyavani K (2006b) Application of plant growth-promoting bacteria associated with composts and macrofauna for growth promotion of pearl millet (Pennisetum glaucum L.). Biol Fertil Soils 43:221–227
Indiragandhi P, Anandham R, Madhaiyan M, Poonguzhali S, Kim GH, Saravanan VS, Sa TM (2007a) Cultivable bacteria associated with larval gut of prothiofos-resistant, -susceptible, and field-caught populations of diamondback moth-Plutella xylostella and their potential for antagonism towards entomopathogenic fungi and host insect nutrition. J Appl Microbiol 103:2664–2675
Indiragandhi P, Anandham R, Kim KA, Yim WJ, Madhaiyan M, Sa TM (2007b) Induction of defense responses in tomato against Pseudomonas syringae pv. tomato by regulating the stress ethylene level with Methylobacterium oryzae CBMB20 containing 1-aminocyclopropane-1-carboxylate deaminase. World J Microbiol Biotechnol 24:1037–1045
Indiragandhi P, Anandham R, Madhaiyan M, Kim GH, Sa TM (2008a) Cross utilization and expression of outer membrane receptor proteins for siderophores uptake by Diamondback moth Plutella xylostella (Lepidoptera: Plutellidae) gut bacteria. FEMS Microbiol Lett 287:27–33
Indiragandhi P, Anandham R, Madhaiyan M, Sa T (2008b) Characterization of plant growth promoting traits of bacteria isolated from larval gut of diamondback moth-Plutella xylostella (Lepidoptera: Plutellidae). Curr Microbiol 56:327–333
Iverson KL, Bromel MC, Anderson AW, Freeman TP (1984) Bacterial symbionts in the sugar beet root maggot, Tetanops myopaeformis (van Röder). Appl Environ Microbiol 47:22–27
Jacques MA, Kinkel LL, Morris CE (1995) Population sizes, immigration, and growth of epiphytic bacteria on leaves of different ages and positions of field grown endive (Cochorium endivia var. latifolia). Appl Environ Microbiol 61:899–906
Jaynes JM, Xanthopoulos KG, Destefano-Beltran L, Dodds JH (1987) Increasing bacterial disease resistance in plants utilizing antibacterial genes from insects. BioEssays 6:263–271
Karpouzas DG, Fotopoulou A, Menkissoglu-Spiroudi U, Singh BK (2005) Nonspecific biodegradation of the organophosphorus pesticides, cadusafos and ethoprophos, by two bacterial isolates. FEMS Microbiol Ecol 53:369–378
Kikuchi Y, Meng XY, Fukatsu T (2005) Gut symbiotic bacteria of the genus Burkholderia in the broad-headed bugs Riptortus clavatus and Leptocorisa chinensis (Heteroptera: Alydidae). Appl Environ Microbiol 71:4035–4043
Koga R, Tsuchida T, Sakurai M, Fukatsu T (2007) Selective elimination of aphid endosymbionts: effects of antibiotic dose and host genotype, and fitness consequences. FEMS Microbiol Ecol 60:229–239
Kremer RJ, Souissi T (2001) Cyanide production by rhizobacteria and potential for suppression of weed seedling growth. Curr Microbiol 43:182–186
Kuzina LV, Peloquin JJ, Vacek DC, Miller TA (2001) Isolation and identification of bacteria associated with adult laboratory mexican fruit flies, Anastrepha ludens (Diptera: Tephritidae). Curr Microbiol 42:290–294
Kuzina LV, Miller ED, Ge B, Miller TA (2002) Transformation of Enterobacter gergoviae isolated from pink bollworm gut with Bacillus thuringiensis toxin. Curr Microbiol 44:1–4
Lauzon CR, Robert BJ, Bussert TG, Prokopy RJ (1994) Could bacteria in nature be detoxifying compounds for the apple maggot fly? Mass. Fruit Notes 55:1–3
Lauzon CR, Potter SE, Prokopy RJ (2003) Degradation and detoxification of the dihydrochalcone phloridzin by Enterobacter agglomerans, a bacterium associated with the apple pest, Rhagoletis pomonella (Walsh) (Diptera: Tephritidae). Environ Entomol 32:953–962
Lefévre C, Charles H, Vallier A, Delobel B, Farrell B, Heddi A (2004) Endosymbiont phylogenesis in the dryopthoridae weevils evidence for bacterial replacement. Mol Biol Evol 21:965–973
Lukwinski AT, Hill JE, Khachatourians GG, Hemmingsen SM, Hegedus DD (2006) Biochemical and taxonomic characterization of bacteria associated with the crucifer maggot (Delia radicum). Can J Microbiol 52:197–208
Manero A, Blanch AR (1999) Identification of Enterococcus spp. with a biochemical key. Appl Environ Microbiol 65:4425–4430
Maudlin I, Welburn SC (1987) Lectin mediated establishment of midgut infections of Trypanosoma congolense and Trypanosoma in Glossina morsitans. Trop Med Parasitol 38:167–170
Mira A (2000) Exuviae eating: a nitrogen meal? J Insect Physiol 46:605–610
Miyazaki S, Bousch GM, Baerwald RJ (1968) Amino acid synthesis by Pseudomonas meltophthora bacteria symbiote of Rhagoletis pomnonella (Diptera). J Insect Physiol 14:513–518
Mohan M, Gujar GT (2003a) Local variation in susceptibility of diamondback moth, Plutella xylostella (Linnaeus) to insecticides and role of detoxification enzymes. Crop Prot 22:495–504
Mohan M, Gujar GT (2003b) Characterization and comparison of midgut proteases of Bacillus thuringiensis susceptible and resistant diamondback moth (Lepidoptera: Plutellidae). J Invertebr Pathol 83:1–11
Mohr KI, Tebbe CC (2007) Field study results on the probability and risk of a horizontal gene transfer from transgenic herbicide-resistant oilseed rape pollen to gut bacteria of bees. Appl Microbiol Biotechnol 75:573–582
Montllor CB, Maxmen A, Purcell AH (2002) Facultative bacterial endosymbionts benefit pea aphids Acyrthosiphon pisum under heat stress. Ecol Entomol 27:189–195
Moran NA, Plague GR, Sandstrom JP, Wilcox JL (2003) A genomic perspective on nutrient provisioning by bacterial symbionts of insects. Proc Natl Acad Sci USA 100:14543–14548
Munnecke DM, Hsieh DPH (1974) Microbial decontamination of parathion and p-nitrophenol in aqueous media. Appl Environ Microbiol 28:212–217
Murphy KM, Teakle DS, Macrae IC (1994) Kinetics of colonization of adult queensland fruit flies (Bactrocera tryoni) by dinitrogen fixing alimentary tract bacteria. Appl Environ Microbiol 60:2508–2517
Nagarajkumar M, Bhaskaran R, Velazhahan R (2004) Involvement of secondary metabolites and extracellular lytic enzymes produced by Pseudomonas fluorescens in inhibition of Rhizoctonia solani, the rice sheath blight pathogen. Microbiol Res 159:73–81
Nakashima KI, Watanabe H, Azuma JI (2002) Cellulase genes form the parabasalian symbiont Pseudotrichonympha grassii in the hindgut of the wood feeding termite Coptotermes formosanus. Cell Mol Life Sci 59:1554–1560
Nardi JB, Mackie RI, Dawson JO (2002) Could microbial symbionts of arthropod guts contribute significantly to nitrogen fixation in terrestrial ecosystem? J Insect Physiol 48:751–763
Nolte DJ (1977) The action of locustor. J Insect Physiol 23:899–903
O’Neill SL, Giordano R, Colbert AME, Karr TL, Robertson HM (1992) 16 S rRNA phylogenetic analysis of the bacterial endosymbionts associated with cytoplasmic instability in insects. Proc Natl Acad Sci USA 89:2699–2702
Olivier KM, Russell NA, Moran NA, Hunter MS (2003) Facultative bacterial symbionts in aphids confer resistance to parasitic wasp. Proc Natl Acad Sci USA 100:1803–1807
Oppert B, Kramer KJ, Beeman RW, Johnson D, McGaughey WH (1997) Proteinase-mediated insect resistance to Bacillus thuringiensis toxins. J Biol Chem 272:23473–23476
Piel J (2002) A polyketide synthase-peptide synthetase gene cluster from an uncultured bacterial symbiont of Paederus beetles. Proc Natl Acad Sci USA 99:14002–14007
Richards FF (1993) An approach to reducing arthropod vector competence. ASM News 59:509–514
Santo-Domingo JW, Kaufman MG, Klug MJ, Holben WE, Haris D, Tiedje JM (1998) Influence of diet on the structure and function of the bacterial hindgut community of crickets. Mol Ecol 7:761–767
Santos AV, Dillon RJ, Dillon VM, Reynolds SE, Samuels RI (2004) Occurrence of the antibiotic producing bacterium Burkholderia sp. in colonies of the leaf-cutting ant Atta sexdens rubropilosa. FEMS Microbiol Lett 239:319–323
Shigenobu S, Watanabe H, Hattori M, Sasaki Y, Ishikawa H (2000) Genome sequence of the endocellular bacterial symbiont of aphids Buchnera sp. APS. Nature 407:81–86
Sittenfeld A, Uribe-Lorío L, Mora M, Nielson V, Arrieta G, Janzen DH (2002) Does a polyphagous caterpillar have the same gut microbiota when feeding on different species of food plants? Rev Biol Trop 50:547–560
Spiteller D, Dettner K, Boland W (2000) Gut bacteria may be involved in interactions between plants, herbivores and their predators: microbial biosynthesis of N-acylglutamine surfactants as elicitors of plant volatiles. Biol Chem 381:755–762
Swain MR, Ray RC (2007) Biocontrol and other beneficial activities of Bacillus subtilis isolated from cowdung microflora. Microbiol Res 164:121–130
Takatsuka J, Kunimi Y (1998) Replication of Bacillus thuringiensis in larvae of the mediterranean flour moth, Ephestia kuehniella (Lepidoptera: Pyralidae): growth, sporulation and insecticidal activity of parasporal crystals. Appl Entomol Zool 33:479–486
Takatsuka J, Kunimi Y (2000) Intestinal bacteria affect growth of Bacillus thuringiensis in larvae of the oriental tea tortrix, Homona magnanima Diakonoff (Lepidoptera: Tortricidae). J Invertebr Pathol 76:222–226
Thibout E, Guillot JF, Ferary S, Limouzin P, Auger J (1995) Origin and identification of bacteria which produce kairomones in the frass of Acrolepiopsis assectella (Lepidoptera: Hyponomeutoidea). Experientia 51:1073–1073
Thimm T, Hoffmann A, Borkott H, Munch JN, Tebbe CC (1998) The gut of the soil microarthropod Folsomia candida (Collembola) is a frequently changeable but selective habitat and a vector for microorganisms. Appl Environ Microbiol 64:2660–2669
Welburn SC, Maudlin I (1991) Rickettsia-like organism, puparial temperature and susceptibility to trypanosome infection in Glossina morsitans. Parasitology 102:201–206
Welburn SC, Maudlin I (1999) Tsetse-trypanosome interactions: rites of passage. Parasitol Today 15:399–403
Welburn SC, Arnold K, Maudlin I, Gooday GW (1993) Rickettsia like organisms and chitinase production in relation to transmission of trypanosomes by tsetse flies. Parasitology 107:141–145
Wernegreen JJ (2002) Genome evolution in bacterial endosymbionts of insects. Nat Genet 3:850–861
Wigglesworth VB (1929) Digestion in the tsetse-fly: a study of structure and function. Parasitology 21:288–291
Wilcox JL, Dunbar HE, Wolfinger RD, Moran NA (2003) Consequences of reductive evolution for gene expression in an obligate endosymbiont. Mol Microbiol 48:1491–1500
Wilson GR, Benoit TG (1993) Alkaline pH activated Bacillus thuringiensis spores. J Invert Pathol 62:87–89
Winicur S, Mitchell HK (1974) Chitinase activity during Drosophila development. J Insect Physiol 20:1795–1805
Xiang H, Wei GH, Jia S, Huang J, Miao XX, Zhou Z, Zhao LP, Huang YP (2006) Microbial communities in the larval midgut of laboratory and field populations of cotton bollworm (Helicoverpa armigera). Can J Microbiol 52:1085–1092
Yu SJ (1992) Detection and biochemical characterization of insecticide resistance in fall armyworm (Lepidoptera: Noctuidae). J Econ Entomol 85:675–682
Zacharuk RY (1976a) Penetration of the cuticular layers of elaterid larvae (Coleoptera) by fungus Metarizium anisopliae and notes on a bacterial invasion. J Invertebr Pathol 21:101–106
Zacharuk RY (1976b) Structural changes of the cuticle associated with moulting. In: Hepburn HR (ed) The insect integument. Elsevier Scientific Publishing Co., New York, pp 299–321
Acknowledgments
The authors wish to thank the financial support given by a BK21 Research Fellowship through a doctoral fellowship to PI to carry out the works pertaining to Diamond Back moth in Department of Agricultural Chemistry at Chungbuk National University, South Korea. The facility provided by TamilNadu Agricultural University, Tamil Nadu, India, to complete this review work is greatly acknowledged.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2011 Springer-Verlag Berlin Heidelberg
About this chapter
Cite this chapter
Indiragandhi, P., Anandham, R., Sa, T.M. (2011). Functional Significance of Insect Gut Bacteria and Their Role in Host Insect Processes, Development, and Crop Production. In: Maheshwari, D. (eds) Bacteria in Agrobiology: Plant Growth Responses. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-20332-9_14
Download citation
DOI: https://doi.org/10.1007/978-3-642-20332-9_14
Published:
Publisher Name: Springer, Berlin, Heidelberg
Print ISBN: 978-3-642-20331-2
Online ISBN: 978-3-642-20332-9
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)