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Re-assessment of the role of the insect gut microbiota Copyright

R. J. Dillon Department of Biology and Biochemistry, University of Bath, Bath BA2 7AY, England

The success of the Class Insecta in our world is beyond dispute. What is less acknowledged is the extent to which microorganisms contribute to this success. The intestinal tract of many insects has been shown to harbour a large diverse microbial community. Although we are now aware of mutualistic associations between a number of insect species and their extracellular gut microbiota (Tanada and Kaya, 1993), many species are known to contain a substantial microbiota whose impact on insect survival is unknown. Lysenko (1985) stated that the role of the normal insect microbiota has not been determined. There are still relatively few studies on the role of the normal microbiota of insects compared to their obligate pathogens, this is partly due to the difficulty in recognizing beneficial relationships. One area of progress is the contribution of microbiota to the nutrition of the host (Tanada and Kaya, 1993). Nutritional contributions may take several forms; improved ability to live on suboptimal diets, improved digestion efficiency, acquisition of digestive enzymes and provision of vitamins. The purpose of this paper is to reassess other subtle, but nonetheless potentially important, ways in which the gut microbiota benefits the insect host.

TERMINOLOGY

The lack of consensus on the terminology used to describe the insect microbiota reflects our ignorance about the stability and role of microbial communities in the gut of most insect species. Terminology is based on that of the intestinal microbiota of humans and domesticated animals (Savage, 1977). The criteria for inclusion of a microbial species as indigenous, or autochthonous include the following; always found in normal adults, colonize particular areas of the intestinal tract, colonize their habitats during succession in the young animal, maintain stable populations in climax communities in adults and associate intimately with the epithelium of the area colonized. In insects where there is a highly complex biota usually required for nutrition (see above) and the bacteria are passed from generation to generation, many of the criteria described for autochthonous microbiota in other animals are appropriate. Each species will presumably have a niche in the gut habitat and thereby contribute to the economy of the whole insect. An indigenous biota is present in all individuals of the species and maintains stable climax communities. However, apart from a few exceptions, the microbial colonization of most insect species has not been studied and the terminology is unclear. The assumption is that many species initially derive their microbiota from the surrounding environment such as the phylloplane of food plants or the skin of the animal host but the persistence of strains of the ingested species is unknown. Do strains of these species engage particular niches in the gut and colonize gut epithelia? Presumably they are not present in all members of the same insect species. The critical distinction is whether a microbial species is able to colonize the gut habitat in contrast to allochthonous (transient) microbes that cannot colonize it except under abnormal circumstances. Locusts (Schistocerca gregaria) derive their relatively simple microbiota from the ingested food plant, starved insects develop a larger population of gut bacteria than fed insects (Dillon, Vennard, Charnley, unpublished). Here the term ‘locally indigenous microbiota’ will be used to describe the microorganisms acquired by individual insects, which multiply within the gut, but are not necessarily present in all members of a single community. This term implies that a range of microbial species acquired from the external environment may occupy the same niche but allows that the microbial species involved may interact positively with the insect host.
Where a positive interaction between insect and microbe is identified the terms commensalism and mutualism are useful. Commensalism occurs where the microbe while doing no harm, benefits from the host but provides no advantage in return. Mutualism is a less flexible association where the microbe and insect mutually benefit each other. In practice there is a continuum between the two extremes, from a commensal, locally indigenous microbiota through to the total integration found between the host and intracellular prokaryotes in specialized cells such as mycetocytes. One example of the integration of bacteria with its host are the intracellular symbionts (genus Buchnera) of aphids which share common ancestory with aphid gut microbes (species of Enterobacteriaceae) and the bacteria ingested from the food plant (Harada, et al, 1996).

DIVERSITY OF THE INSECT GUT MICROBIOTA

It is now realized that we cannot culture the vast majority of microorganisms using traditional techniques. Molecular studies have revealed unrecorded microbial sequences in many natural samples to the extent that new kingdoms of life have been discovered in the Domain Archaea. The number of investigations of the diversity of the insect gut microbiota using molecular phylogenetic approaches is limited but we already have a glimpse of the information that this will reveal about the microbial diversity of the gut environment. Two thirds of clonally isolated 16s rDNAs from the gut microbiota of termites (Reticulitermes speratus) had less than 90% sequence identity with known bacterial species (Ohkuma and Kudo, 1996). Ten of these clones failed to show close similarity with any recognized bacterial phyla. In situ hybridisation with species specific rRNA probes provides a complementary approach to cloning for the characterization of gut microbiota. Fluorescently labelled probes can be used to visualize phylotypes, establish morphology and determine number and spatial arrangement of cells. Fluorescently labelled probes were used to survey gut microbiota of five cricket species (Santo Domingo et al., 1998a). Species that are difficult or currently impossible to cultivate were detected eg. Bacteroides and Prevotella. spp. and species of Archaea, the probes were able to detect changes in the profile of the microbial community due to dietary changes. Fractionation of microbial DNA according to guanine plus cytosine content was used to give an overall measure of microbial community composition and structure in the cricket (Acheta domesticus) hindgut (Santo Domingo et al., 1998b). The cricket microbiota provides a supply of fermentation products to the insect. Changes in the insect diet resulted in the emergence of a new microbial community structure together with changes in the microbial fermentation activity. These results show that fundamental shifts in the microbial profile can occur even in insects with an indigenous mutualistic biota.

NON-NUTRITIONAL ROLE FOR MICROBIOTA

A) COLONIZATION RESISTANCE
The most important beneficial function of the indigenous intestinal microbiota in humans and domesticated animals is their ability to withstand the colonization of the gut by non-indigenous species including pathogens and therefore prevent enteric infections (Berg, 1996). The term colonization resistance (CR) is used to describe this function. The notion that this sort of function might be widespread in insects has received scant attention. Several approaches have been used to study colonization resistance. Insects whose resident microorganisms have been suppressed by antimicrobial agents are compared with insects containing an undisturbed microbiota. Alternatively, germ free insects are compared with their conventional counterparts or insects associated with one or two bacterial species. These studies can only be undertaken in insects with a non-obligatory microbiota unless specialized diets are used. Use of antimicrobials has a number of drawbacks. Apart from toxic effects towards the host even a broad antimicrobial regime may be overcome by resistant microorganisms. Some insect species such as locusts can be reared free from extracellular microorganisms using surface sterilized eggs and kept in sterile isolated environments. This system enables the production of gnotobiotic (defined biota) insects where bacterial species can be eliminated or reintroduced and population changes monitored. An isolator system, based on that developed for rearing gnotobiotic animals, was used to study the colonization resistance of the locust gut microbiota (Charnley et al., 1985). Another approach to the study of colonization is to use bacteria containing molecular markers (eg antibiotic resistance, Murphy et al., 1994). Locusts (Schistocerca gregaria) contain a relatively simple locally indigenous microbiota (Hunt and Charnley, 1981) located primarily on the hindgut cuticle. Axenic locusts were reared in an isolator system on ?-irradiated diet (Charnley et al., 1985) The insects were able to breed through several generations and there was no obvious nutritional requirement for a microbiota; indeed axenic locusts were physiologically comparable to conventional insects. Colonisation resistance of the locust gut microbiota was implicated in the inability of fungal entomopathogens to germinate and infect via the conventional locust gut (Dillon and Charnley, 1986ab, 1988, 1991). Axenic insects were susceptible to fungal infection. Antifungal phenolic compounds detected in the gut fluid or frass of conventional locusts were absent from the axenic locusts. The phenolic compounds inhibited germination of 10 species of insect pathogenic and plant pathogenic fungal species. Moreover the phenolics were present in concentrations sufficient to account for the antifungal activity of the gut. Hydroquinone, 3,4 dihydroxybenzoic acid and 3,5 dihydroxybenzoic acid were identified. Similar antifungal activity has been located in the gut of seven other Orthopteran species. Monoassocation experiments of axenic locusts with a commonly isolated bacterial component of the microbiota, Pantoea (Enterobacter) agglomerans resulted in the appearance of one of the antifungal phenolics and established germination inhibitory activity in the gut fluid (Dillon and Charnley, 1995). The presence of only one of the three phenolics detected in conventional locusts suggests that several bacterial species cooperate in their production. A wider role for these antimicrobial phenolics in colonization resistance is suggested by the finding that they are selectively bactericidal; the indigenous species were able to survive in comparison to other species. A few studies have examined the impact of the gut microbiota on the establishment of human pathogens and parasites in their insect vectors. Gnotobiotic insects (Greenberg et al, 1970) were used to provide evidence of the bacterial pathogen-suppressing ability of the microbiota of Musca domestica and Lucilia sericata. Erdmann et al, (1987) suggested that aromatic metabolites of the gut bacterium Proteus mirabilis are involved in the suppression of allochthonous bacteria in Calliphorid larvae. The possibility that CR is involved in suppressing medically important parasites such as Plasmodium and Leishmania in their Dipteran vectors has been discussed (Pumpuni et al, 1996; Dillon et al, 1996). The transmission of Chagas’ disease by its vector provides the first example of a gut bacterium that has been genetically modified to provide CR towards a parasite (Durvasula et al., 1997). The role of the tsetse fly midgut microbiota in promoting trypanosome development (Maudlin and Welburn, 1994) will not be considered here.

B) SEMIOCHEMICAL PRODUCTION
Some insects sequester plant compounds for use directly as pheromone components or make minimal modifications to a dietary precursor (see review Tillman et al., 1999). The production of pheromone components by bacteria in the insect gut has also been inferred in a number of studies but conclusions were based solely on their ability to produce the relevant compound in vitro. Alternatively they have used antibiotic treatment to link the microbiota to pheromone production. Given the shortcomings of this approach in studies on gut microbiota (see earlier) it is not surprising that subsequent studies demonstrated an insect origin for the compounds. Nolte et al. (1973) suggested that bacteria in the digestive tract of the locust Locusta migratoria migratorioides convert lignin to locustol (5-ethylguaiacol), a pheromone involved in aggregation. Subsequent studies failed to isolate locustol (eg. Fuzeau-Braesch et al., 1988). Considerable advances have been made in the last 10 years in understanding the process that causes solitary locust populations to turn gregarious. There is interplay of visual, tactile and chemical stimuli (Byers, 1991; Pener and Yerushalmi, 1998). Pheromone involvement in attraction, group cohesion and transformation of locusts has been studied (Pener and Yerushalmi, 1998). Some of the pheromone compounds that modulate locust behaviour are phenolic compounds released from the insect faeces (Fuzeau-Braesch et al., 1988; Obeng-Ofri et al., 1994). These compounds do not elicit the gregarization process but seem to function as cohesion pheromones. The phenolic compounds guaiacol and phenol are the predominant electrophysiologically active components released from juvenile and adult faecal pellets of the locust Schistocerca gregaria (Obeng- Ofri et al., 1994), adult male pellets also contained phenylacetonitrile. Phenylacetonitrile is probably derived from cuticular glands, but the origin of the other phenolics is unknown. In view of the finding that gut microbiota are involved in the production of related phenolic compounds in locusts the possibility that the gut bacterial biota were involved in the production of components of the locust cohesion pheromone has been recently investigated (Dillon et al., 2000). Volatile compounds collected from faecal pellets from conventional adult and juvenile locusts contained guaiacol and phenol. In contrast, there was a marked absence of guaiacol-like odour emitted from axenic locust faecal pellets compared to conventional locust pellets. GC-MS analysis revealed that the difference in odour was indeed due to the absence of guaiacol and the low level of phenol detected in volatiles collected from axenic faecal pellets (Dillon et al., 2000). The monoassociation of the bacterium P. agglomerans with newly hatched axenic locusts, subsequently reared on ?-irradiated diet, resulted in the detection of the 2 phenolics in 5 th instar larvae although phenol was already present at a low level. These results indicate a bacterial origin for guaiacol and a proportion of the phenol. This is supported by experiments that demonstrated the ability of three species of locust gut bacteria (including P. agglomerans) to produce guaiacol and phenol directly from axenic faecal pellets in vitro. Microbial production of guaiacol was not a universal attribute. Guaiacol was not produced by Serratia marcescens (Enterobacteriaceae), a locust pathogen, or by locust gut enteroccocal species (Dillon, Vennard and Charnley, unpublished). A role for bacteria derived aromatics in other locust species is likely since guaiacol, and phenol were the main compounds detected from three species of locusts and their faecal pellets with guaiacol being the major product in each case (Fuzeau-Braesch et al, 1988). Veratrole, which was detected in previous studies, was not detected. Differences in the profiles of phenolic volatiles might be attributable to variations in the species composition of the gut microbiota. The fact that some of these aromatic compounds are microbially derived might account for variations in the results obtained from previous studies – the gut microbiota of lab-reared locusts will vary widely in both population size and diversity depending on the diet and rearing conditions. Bacterial fermentation continues in the faecal pellet after being voided from the insect. Continuation of aromatic volatile production by bacteria within the faecal pellets will depend on the availability of precursors and the moisture content of the pellet. Thus the duration of pheromone component release from faecal pellets surrounding locust roosting sites will depend partly on external environmental factors. Knowledge of the bacterial origin of the aromatic compounds enables us to explain the variation in amounts of compound released from different ages of locusts. Lower quantities of aromatic compounds were produced in young adults in this study confirming the observations of the two previous studies (Fuzeau-Braesch et al., 1988; Torto et al., 1994). The hindgut cuticle is the site of the main bacterial population and during moulting it is renewed and the bacterial population declines (Hunt and Charnley, 1981), young adults will therefore contain a reduced population of bacteria which correlates with the fall in guaiacol and phenol production observed at this stage. Periods of starvation may change the composition and total population of bacteria and this would influence the amount of pheromone produced. The intriguing possibility that changes in the metabolism of the gut microbiota are linked to changes in the pheromonal profile is being investigated. The precursor for guaiacol synthesis in faecal pellets must either be a component of the plant material or an excretory product of the insect. The former is indicated, as guaiacol production was dependent on the diet; considerably more guaiacol was present when conventional locusts were fed fresh wheat seedlings than the freeze-dried, ?-irradiated grass. Incubation of the locust diet with bacteria resulted in only minor amounts of guaiacol or phenol, indicating that digestion of the plant material in the locust gut is required for production of guaiacol by the bacteria. The most obvious precursor for guaiacol synthesis lignin-derived vanillic acid (4-hydroxy-3-methoxybenzoic acid) which is detected in the faeces of both axenic and conventional locusts (Dillon and Charnley, 1988, 1995). Microbial transformation of vanillic acid to guaiacol is via loss of a carboxyl group by the action of an inducible decarboxylase (Dillon, Vennard and Charnley, unpublished). Consistent with this, we found guaiacol was released by three species of locust gut bacteria from glucose/peptone broth cultures containing vanillic acid. Furthermore faecal pellets from conventionally reared insects fed filter paper impregnated with vanillic acid solution yielded large amounts of guaiacol (Dillon et al, 2000). Locusts possess a locally indigenous microbiota composed of species commonly encountered in their environment, in particular the phylloplane biota on food plants (Hunt and Charnley, 1981). Guaiacol production by vanillic acid decarboxylation is an attribute of some plant and soil saprophytes (Crawford and Olson, 1978) which will be ingested with the food plant, so locust faecal pellets will always contain guaiacol though the bacterial species producing it may differ. The flexibility in the association between the locust and its microbial partners was predicted by Jones (1984) who suggested that insects should evolve mechanisms to minimize the adverse consequences of mutualist loss by reduced reliance on single microbial species. Bacteria colonizing the insect plant food may be adapted to deal with aromatic compounds and these plant-inhabiting strains may be selectively enriched in the gut environment. Microbial communities adapt through extensive transfer of degradative genes. Although we know that transconjugation between bacterial strains occurs in insect guts (eg.Watanabe et al., 1998), the extent to which this may occur within the insect gut community or on the food source prior to ingestion by the insect is unknown. Behavioural responses to microbial metabolites associated with insect frass have been reported for other insect species. Klebsiella oxytoca and Bacillus spp. produce the volatile alkyl disulphides present in the faecal pellets of the leek moth (Acrolepiopsis assectella; Thibout et al, 1995) which serve as kairomones to attract the parasitoid Diadromus pulchellus to the moth host. These also appear to result from the action of the bacterial enzymes on plant precursor molecules. It is intriguing to note that guaiacol was implicated as a kairomone for another parasitoid Microplitis demolitor; though the origin of the compound in the faeces of the soybean looper host (Pseudoplusia includens; Ramachandran et al, 1991) was not determined.

CONCLUSIONS.

The gut microbiota is regarded as a valuable metabolic resource for insects on sub -optimal diets but apart from this, most relationships between insects and their microbiota remain undefined. Studies with gnotobiotic locusts suggest that the microbiota confers previously unexpected benefits for the insect host. Microbial transformation of plant secondary compounds in an insect gut and adaptation by the host to use the resulting common metabolites are unlikely to be processes unique to locusts since seven other Orthopterans also have antimicrobial phenolics in their gut fluid. These findings have potentially wide implications for our appreciation of insect-microbe-plant tritrophic interactions. The importance of colonization resistance of the gut microbiota in other animals is well documented though progress in establishing the mechanisms involved are hampered by the overwhelming complexity of the gut microbiota. Unequivocal demonstration of cooperative effects of the gut microbiota requires the use of rigorous quantitative microbiological methods using in vivo models and this has also restricted the work on insects. Insects are often used to establish principles which are common to all animals; perhaps the most famous being Pasteurs’ demonstration of disease transmission using silkworm larvae as a model system. In view of the relatively simple microbiota of insects such as locusts, they can be used to establish the principles of colonization resistance which will be of relevance to work on colonization resistance in other animals. Furthermore, there is much interest in the role of the human gut microbiota in carcinogen metabolism and the production of naturally occurring compounds which may prevent tumour formation. One putative suppressor of tumour formation is also a bacteria- derived compound found in the locust gut. The studies with locusts provide evidence for a moderately mutualistic association between the locust and its microbiota. The bacterial community of the locust gut is adapted to metabolize plant allelochemicals into antimicrobial compounds with increased activity against allochthonous microbes and provision of pheromonal compounds. This dual benefit for the insect suggests a closer degree of integration between the locust and its microbial community than was previously suspected. Surprisingly, this has not resulted in the development of an obligately mutualistic association; instead the locust has minimized the consequences of mutualist loss by not relying on a single microbial species.

ACKNOWLEDGEMENTS.

Keith Charnley and Viv Dillon for discussions and critical comments. Chris Vennard for lab support and BBSRC (UK) for financial support.

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Index terms: Schistocerca, intestine, bacteria, symbionts, pheromone.

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