concluded that the food relationships of the vast majority of wood-eating insects two types of wood-eating insects, those secreting a cellulase and those unable information (Hopf, ) suggests that wood-feeding beetle larvae may be in the digestive tracts of most Termites, the symbiotic yeasts in wood-boring beetle. symbiotic cellulolytic microorganisms. Thus, a dis- For example, oxidative processes that cleave . proposed to occur in cerambycid beetle larvae, in silverfish and .. and symbiotic relationships between the intestinal protozoa of termites. A good example of mutually beneficial symbiosis is the clownfish and the sea Their relationship is a parasitic one – the tapeworm gives nothing to its host, and the protozoans and bacteria in their gut and certain scarab beetle larvae house .
A proper grasp of the nature of interactions between humans and their microbiota can only come from an awareness of the parallels and contrasts with other animals. Insects represent a superb system for comparison because, as a group, they display far greater diversity than mammals in their interactions, including some associations of remarkable morphological intimacy and molecular integration. Research on insect-microbial interactions has been invigorated in recent years by the technical advances that make it possible to identify and study unculturable microorganisms.
The recent gains in mechanistic understanding of the relationships in molecular terms have immediate relevance to research on the impact of resident microbes on the physiology and health of humans. This review summarizes these recent advances by focusing on four topics: The impact of insect research on our understanding of associations in humans is also briefly considered.
Diversity of insect-microbial symbioses Insects and mammals share the common feature that they are inhabited by microorganisms. Even so, there are two important differences in the host-microbial relationship between the two animal groups: To address these differences, the gut microbiota and intracellular symbioses of insects are considered in turn.
The gut lumen is very densely colonized by microbes in most mammals and insects. The animal gut can be considered a portion of the external environment in which the conditions and resources are controlled largely by the animal. Microorganisms associated with food have unrestricted access to the gut; and those that can tolerate, modulate or evade the digestive processes and immune function of the animal gut gain access to a nutrient-rich environment and a vehicle for dispersal via the feces.
Nevertheless, the habitats in the insect and mammalian guts cannot be equivalent because the patterns in the composition and diversity of the gut microbiota are markedly different. Dillon and Dillon, ; Robinson et al. The reasons for this difference are unclear. As with many other low diversity habitats Connell,insect guts tend to be transient and have extreme disturbance regimes. It has also been suggested that the adaptive immune system of mammals may promote microbial diversity through its greater capacity than the innate immune system to discriminate among different microorganisms, enabling the mammalian host to maintain complex multispecies consortia McFall-Ngai, The greater microbial diversity in individual mammals than insects is overlain by a greater diversity across all insects relative to all mammals.
Thus, the dominant microbes in all mammals are Bacteroidetes and Firmicutes, but the gut microbiota of insects vary widely among different taxa, including Proteobacteria, Firmicutes and Protists Brugerolle and Radek, ; Dillon and Dillon, ; Morales-Jimenez et al.
This difference could be a consequence of the greater variation of diets and gut physiology in insects than mammals, which is linked to the greater phylogenetic diversity of insects.
The pH in many insects lies within the range of 6—8 units, and some, notably lepidopteran caterpillars, have a very basic midgut region, at 11—12 pH units Wieczorek et al. The second dominant habitat in insects utilized by microorganisms is cells. These associations are widespread or universal in several groups, notably cockroaches, hemipterans, ten families of beetles, and lice, and they also occur in some flies and ants [see Table 1 in Douglas ]. Although they have evolved independently multiple times, the microorganisms are invariably transmitted vertically from mother to offspring usually via the eggs in the female ovaries.
Fungi and Insect Symbiosis
Bacteriocytes are not the only insect cell type that contains microorganisms. Across all insect groups, microorganisms have been reported in cells of various organs, including the fat body, gut epithelium and gonads. Some species are known to have a broad range, but others are specific, occurring on only a single species of arthropod. It was even thought that some were restricted to a particular part of the anatomy of the organism on which it is growing.
However, some recent research on this relationship has shed light on this myth that had persisted for many years. With respect to insects, which are arthropods, it was once believed that every species of insects have fungi, in this group, associated with some part of their anatomy. However, more recent studies indicate that there appears to be certain groups of insects that are more prone to infections than others and that even in those groups not all species necessarily have this fungus.
Also, the relationship between the insect and fungus was unknown until recently. It is now believed that the fungi in this group are mild parasites on the insects, i. Some picture of Laboulbendiomycetes can be found for the following species: Peyritschiella protea on the back of a living Rove Beetle, low magnification imageand ascocarp under the microscope ; Laboulbenia cristata on the legs of a beetle, low magnification image showing ascocarps located only on the upper leg portions of the beetle, and an ascocarp as viewed under the microscope ; Rickia dendroiuli, the ascocarps are located only on the forelegs of the millipede low magnification imageand ascocarp as viewed under the microscope.
As can be seen from comparison of the low magnification and microscope images, the ascocarps are very small, even relative to the insect.
Because there have been few studies in this group and much is still not known with respect to the relationship between the fungus and insect. For example, it was once believed that the variations as to where the ascocarps occurred, for a particular species was so specific that it could be found only in a particular body part of the male and a different part of the female of the host species.
This phenomenon was first observed by Peyritsch It was later observed that the variations as to where the ascocarps are borne in the male and female seemed to be based on the mating habit of the insects, i. However, there are also species in which both sexes of host are equally heavily infested, and in the same position on the integument. A summary of the Laboulbeniomycetes may be found at the following link. Septobasidium The genus is mostly composed of fungi that form symbiotic relationships with various scale insects.
The genus is a member of the Basidiomycota and forms irregular, flattened, colonies that adhere closely to the bark of leaves of living trees, much like the growth of lichens. The colony may be flattened and only a few millimeters in diameter or may grow around the circumference of a branch. Based on this picture, Septobasidium appears to be nothing more than just another wood inhabiting fungus.
However, there is a great deal more to this fungus.
The scale insects can be found in the middle layer of the fungus, in chambers that are only slightly larger than the insects, which are connected with numerous tunnels. Some of these insects are parasitized by the fungus, which have inserted haustoria, specialized feeding hyphae, into the insect body.
These parasitized individuals are immobile and usually occupy a chamber where they are attached to the plant by their sucking apparatus the suctorial tube. A diagrammatic representation of what has just been described can be found here. The insect nourishes itself with the plant sap that it obtains through its sucking apparatus, and because the fungus is attached to the insect by haustoria, it is indirectly being nourished by the plant, with the insect serving as a "pumping" conduit.
However, why is this not a host parasitic-relationship, favoring the fungus? There are great benefits to the insects as well. A number of scale insects live within the so-call colony of the fungus and are sheltered from the environment and have their food supply beneath them. In addition, they are also protected from predators.
Thus, the fungus colony offers the insects shelter, resulting in them living longer than their free-living counter parts. The fungus colony with the insects may also over-winter without any harm coming to either the fungus or insects. The following spring, the fungus will continue growth and the female insects will be ready to lay its eggs. The larval stage that emerges will crawl about the colony, and if it should go to the surface, it will pick up the fungal spores, which will adhere to their bodies.
It may go back inside its colony of origin. It may crawl to a neighboring colony and join that colony. It may go to an area where there is not a preexisting colony and when the spores that are attached to its body germinates, a new colony of Septobasidium will form.
Although a number of species of Septobasidium are known, they are a poorly studied group and the relationship of the fungus and insect has not been that well studied.
Although haustoria are formed in the insect, by the fungus, its affect on the insect has not been well studied. Fungi Symbionts With Colonial Insects The most interesting of the fungus-insect symbiotic relationships are those involving colonial insects. One of the most important driving forces that result in symbiotic relationships between microorganisms is the inability of animals to digest cellulose. Instead, they have symbiotic bacteria, in their stomach, that have the cellulolytic enzymes that digest the plant material for them.
Other animals, such as detritivores, do not carry microorganisms in their gut, but rather consume mycelium in well decomposed plant material as their food source. Thus, symbiotic relationships between animals and various microorganisms are common. We will look at some examples of animal-fungi symbiosis, or more specifically, insect-fungi symbiosis, which I think are far more interesting than the above examples.
Ants, Termites and Mushrooms Social insects have always been of interest because of their seemingly, well ordered societies. In some of these social insects, the mound-building termites of Africa and Asia, and the leaf-cutting ants of Central and South America, there has evolved a rather unique strategy in the utilization of cellulose-rich plant material.
These insects cultivate cellulolytic fungi, in underground gardens, and I'm using the world cultivate in the true sense of the word, because these insects are deliberately growing these fungi. They establish pure cultures of their fungus.
That is they grow only one fungus in their garden, which is not easily done, since there are so many sources of contamination that can occur and prevent their gardens from being successful. However, these insects are able to keep their gardens pure by constantly weeding out foreign fungi.
Lessons from Studying Insect Symbioses
They also care for their garden by providing suitable a food source, i. So the fungi obviously benefit from this arrangement, but the ants and termites also benefit from this relationship. These insects are exclusively mycophagous, i. The fungi that they cultivate decompose the wood and leaves brought in by the termites and ants, respectively, and provide them with digestible and nutritious mycelium.
They represent hundreds of species of ants, from approximately fifty genera. Although you probably have never heard of these ants, to the people of South America they are an all too familiar sight. In their search for food, these ants will devastate the natural vegetation and crops that are in their path, as they search for plant material to feed their fungus. When the Spanish Conquistadors arrived, they conquered the Native Americans, but were unable to do anything about the ants.
Their efforts in growing cassava and citrus fruits failed because of their inability to control these ants. At the base of their fruit trees could be seen the ant nests which were "white as snow," presumably from the mycelium that they were growing. Of all the known species, Atta sexdens is the most economically important and the one which is most intensely studied, and the species that we will look at in detail as representative of this group of ants.
The winged female by this time has already been fertilized and potentially can lay as many as million eggs during her lifetime. When the winged female finds a suitable site for her future colony, she takes out the fungus from her mouth and finds suitable plant material on which to inoculate the fungus.
Once the fungus is growing, the queen begins to lay her eggs on the fungus. At first she is laying approximately fifty eggs each day, but eats most of these in order to nourish herself until the worker population has become established, which normally takes approximately three months that's a lot of eggs that she has eaten by that time.
During this first year, there is only a single entrance to the ant colony, but by the end of the second year, another entrance is added. From there, entrances proliferate at a much greater rate and approximately 1, entrances may occur by the end of the third year. It is at this time that new winged females are produced each year that will establish colonies elsewhere. However, as is the case with many species, there are far more winged females produced than will ever establish successful colonies.
It is estimated that as many as In studies that have been carried out in excavated nest, it was found that one nest that was four years old contained subterranean chambers, of which contained fungus gardens. Another, approximately six years old, had chambers, or which contained fungus gardens. Gardens are usually cm in in diameter and weight approximately g It is estimated that these colonies had consumed kg 13, lbs of vegetation.
In a young colony, the queen and the first workers to hatch from eggs establish the first fungus garden by excavating a chamber and filling it with vegetation brought in by the workers and then inoculating it with the fungus. Different species will utilize different substrate material for their fungus gardens. The Attine ants are commonly called leaf-cutting ants because they forage for leaves and cut them into pieces with their mandibles before carrying them back to their colony.
Once they have returned with the leaf cutting, the workers cut the material into smaller pieces, lick it all over and often deposit anal excreta on it. The excreta, which serve as additional nutrients for the fungus garden, and plant material is then wedged into the garden and a tuft of mycelium placed on it.
The gardens are sponge-like in appearance and is composed of numerous cavities which the workers walk through. In walking through, the workers probe the mycelium with its antennae, lick it, deposit anal droppings on it and also eat the hyphae.
Regardless of the species of ants, the colony only contains one species of fungus. This is difficult condition to maintain since, as you should recall, from our lecture on decomposition, fungi and bacteria are everywhere ready to take advantage of whatever organic material that becomes available.
The worker ants in probing the mycelium with their antennae are able to distinguish their fungus from alien fungi. When foreign fungi are detected, the workers remove them. Some foreign fungi, undoubtedly, are present, but with the far more prevalent, cultured fungus, they are unable to compete and do not make up an appreciable part of the garden.
When colonies are abandoned because of disturbance or migration, the fungus garden left behind deteriorates and becomes contaminated with other fungi and bacteria. Before abandoning their colony, the Attine ants always take some of the fungus garden with them as an inoculum to start their new fungus garden.
Lessons from Studying Insect Symbioses
As the mycelium grows, swollen hyphal tips are formed, called the bromatiawhich is the part of the hyphae that the ants consume. Although a great deal of plant material is brought into the colony, apparently the ants consume none of it.
It is used entirely to feed the fungus and the ants only feed upon the fungus. Click here to go to an excellent web page where you can read more about the Atta ants. The discovery of the identity of the fungal species involved in these ants were determined by taking pure cultures into the lab and in some cases fruiting bodies have formed. In most instances, they have been determined to be species of the mushroom genera, Leucoagaricus and Lepiota.
Other fungi that have been fruited include Auricularia, and Xylaria, a member of the Ascomycota.