Entomology Today
https://entomologytoday.org/2017/11/15/nutritional-symbionts-why-some-insects-dont-have-to-eat-their-vegetables/

By Lora Kraft

Broccoli was the main vegetable at my family’s house growing up. Despite my sisters’ and my distaste for the veggie, it was cheap and packed full of nutrients, and so dinnertime would end in a dramatic pantomime where we laboriously chewed down the few pieces we were served, full of complaints. Why did we have to eat those nasty vegetables in the first place? The answer boils down to nutrition. The broccoli my parents served delivered essential amino acids and vitamins we weren’t getting elsewhere in our diet. We needed broccoli for better health, and it turns out that all animals have similar nutritional requirements that their diet must fulfill for them to survive and reproduce successfully.

Amino acids build the proteins and enzymes that make cellular work possible. There are 20 different amino acids, of which some are non-essential or can be synthesized by the organism itself, while nine are essential amino acids that the organism must acquire them through its diet. In addition to the amino-acid building blocks, all organisms require vitamins to complete certain reactions. For example, B vitamins, which cannot be created by insects, are required for a wide variety of chemical reactions to take place. Of course, no well-balanced diet is complete without energizing fuel. Insects require carbohydrates, which get broken down into smaller and smaller sugar chains to give insects the energy to grow and reproduce. This is by no means a complete list of required nutritional components. Insects also require minerals and lipids in their diet, but I will focus on amino acids, vitamins, and carbohydrates here.

While many animals, like humans, consume a varied diet to get these nutritional components, some insects have learned how to cheat the system and can extract nourishment from a nutritionally poor food source through symbioses with bacteria. A symbiosis is a long-term interaction between two different species. Symbioses can be parasitic or neutral, but many examples of symbiosis benefit both organisms. Such is the case with nutritional symbionts. A symbiont is a unicellular organism in a symbiotic relationship with an insect. These symbionts can be different types of bacteria, yeasts, or protozoans and are found in many different insect groups including cockroaches, white flies, lice, longhorn beetles, fruit flies, ants, termites, bed bugs, and aphids, to name a few. Each of these symbiont-insect interactions has a long evolutionary past and is specific to the organisms in question.

Good Things Come in Threes: Termites and Their Symbionts
Termites are major structural pests, and they do billions of dollars in damage in the U.S. yearly, but they are also important ecologically in the breakdown of woody plant material. Wood, though, is no easy meal. Woody plant material contains cellulose, which is a natural polymer that gives strength to plant cell walls. Most animals, including humans, can’t digest cellulose, and it simply passes right through them. Termites, on the other hand, can break down the chemical structure of cellulose with help from three different symbionts: a bacteria, an archae-bacteria, and flagellate protozoans.

Termite digestion works like this: A termite eats wood, which passes through a kind of gizzard that breaks it up with a lot of internal grinding “teeth.” Then, the broken-down wood moves into the midgut of the insect where some enzymes break down the sugars for absorption by the termite. For the most part, the cellulose fibers are still intact as they move into the next portion of the digestive system, the hindgut. The triage of symbionts hang out in the enlarged hindgut and begin to ferment the cellulose, breaking it down so that some of it can be absorbed by the termite and some by the symbionts (they have to eat, too). One small group of termites (Macrotermitinae) take this whole process a step further by tending fungus gardens within their colonies that the termites fertilize with their feces. Then, the termites feed on this fungus.

Eating fecal-fertilized fungus may sound gross, but termites are very familiar with supping on previously digested materials. Social termites will often feed on digested materials of their nestmates through anus-to-mouth feeding, or proctodeal trophallaxis. This has important implications for nutrition. The vital amino acids and vitamins found within wood material are often tied up in cellulose and other proteins. Only after this material passes through the hindgut where the symbionts are located can these nutrients be freed up for absorption, but the hindgut can only absorb very specific materials. The amino acids and vitamins must be absorbed in the midgut, which means it needs to pass through the termites another time.

Proctodeal trophallaxis is also important to pass on the symbionts to the next generation. A newly hatched termite does not harbor the symbionts necessary to break down wood, so it picks up a nestmate’s symbionts through proctodeal trophallaxis to begin breaking down its own cellulose.

Bed Bugs, Blood Meals, and B-Vitamins
While eating wood may not be an appealing meal to most humans, many different cultures do consume protein-rich blood of other animals. (Blood sausage, anyone?) And, as we are all too aware, insects such as lice, mosquitoes, and bed bugs also value blood as a food source. While it is high in protein, blood lacks one major nutritional component: B-vitamins.

Bed bugs have made a recent comeback in the United States and other parts of the world.  While they do not harbor any known human diseases, they cause itchy, zig-zagging bites as they feed on human hosts. While plentiful, these blood meals are nutritionally deficient for the pests. Enter Wolbachia.

Wolbachia is a genus of symbiotic bacteria found in upwards of 60 percent of insect species. Unlike the termite symbionts discussed above, its role is not always entirely mutualistic. Wolbachia bacteria are most famous for being reproductive manipulators, changing their hosts’ methods of reproduction to further their own proliferation. Unlike the termite symbionts, they are maternally inherited from mother to offspring.

In some organisms, Wolbachia is mutualistic, such as in nematodes, where it may help confuse vertebrate immunity to allow the nematode to attack without the host’s immune system noticing. Recently, Wolbachia has also been found in all common bed bugs as a nutritional symbiont. While Wolbachia is found in multiple areas in the abdomen of the bed bug, it is most commonly found in specialized structures called bacteriomes, located near the reproductive structures of the bed bug. These bacteriomes likely provide a protected location for the bacteria. The bacteria in turn have DNA that contains pathways to synthesize many different variants of B-vitamins, more variants than they do when they infest other non-blood-feeding insects. Bed bugs that receive an antibiotic and are cured of Wolbachia develop more slowly, illustrating their usual dependence on this bacterial symbiont to bolster their bloodmeals.

Too Much Sugar? No Problem for Sugar-Sucking Aphids
Like the other two insect groups, aphids also feed on a nutritionally poor diet: plant sap. Aphids have specialized mouthparts that are shaped like a straw to suck the sugars that the plant uses for its own metabolism right from the channels that carry the sugars to the leaves and fruit.

Unsurprisingly, this sugar-water diet is low in protein and, therefore, the amino acids that protein provides. First, aphids must suck up massive quantities of this plant sap just to acquire enough proteins to work with. Because of this, the aphid has a special filter system in its digestive system that quickly filters out all extra sugary-sweet liquid from the remaining protein so that the aphid doesn’t pop open like an overfilled water balloon while feeding. This expelled sugary liquid is called honeydew and causes its own problems in agriculture when it provides a sugary substance for plant pathogens to grow on.

The few amino acids that remain after filtration do not complete the full set of essential amino acids required, so the aphid’s bacterial symbiont Buchnera steps in to convert these amino acids into the full suite of essential amino acids needed.

The aphid-bacteria system provides an excellent model to better understand just how these symbioses are maintained over time. In its long evolutionary history with the aphid, Buchnera, like many symbionts, lost genes that were redundant, like the genes encoding the ability to synthesize amino acids that the aphid could already create itself. But the host-symbiont interplay is even more interesting than that. Buchnera modifies a molecule it receives from the sugar-sap diet and then passes it to the aphid. The aphid then turns this modified molecule into the finished amino acid that it then shares with the Buchnera. Scientists believe this interplay increases the aphid’s dependence on Buchnera while at the same time allowing the aphid to control how much amino acid it shares with the symbiont to make sure the bacteria’s populations don’t grow out of control. Each player strengthens the symbiosis through its interdependence on the other.

These nutritional symbionts in termites, bed bugs, and aphids likely allowed them to specialize on nutrient-poor diets that may have had fewer competitors for the same food source. More importantly, they save their hosts from having to eat broccoli every night.