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.
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).
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
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.
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.
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.
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The copyrights to this original work belong to the author
(see right-most box in the title table). This document
appears in Plenury Lectures: ABSTRACT BOOK I –
XXI-International Congress of Entomology, Brazil, August