Maize weevil (Sitophilus zeamais). Credit: USDA
Maize weevil (Sitophilus zeamais). Credit: USDA

Lessons from Nature: Recycle Allies that Stop Being Useful

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Two cereal weevils. Credit: Vigneron et al, 2014. Current Biology.

These two insects are cereal weevils of the same age and species. They have different colours because the one on the bottom has a thinner, weaker shell. It is the lesser of two weevils.

Cereal weevils are long-snouted beetles, no bigger than corn kernels. They are serious pests that devour crops like rice and wheat, and like many insect pests, they owe their success to bacteria. Their microbes in question all belong to a species called Sodalis pierantonius and they live inside some of the weevil’s cells. These cells are packed into special organs called bacteriomes, which branch grape-like from their guts and ovaries. The bacteriomes provide the microbes with shelter from the environment, and from the weevil’s immune system.

If the weevils are deprived of their microbes, they grow more slowly, fly more poorly, and produce fewer young. They’re clearly important. But they’re also temporary. Back in the 1930s, an Egyptian scientist noted that the gut bacteriomes mysteriously disappear a few days after the weevils reach adulthood. Now, eight decades later, Abdelaziz Heddi from the National Institute for Applied Sciences in Lyon has discovered why.

As adults, the weevils use their microbes for one very specific purpose: to mass-produce the building blocks they need to create their hard outer shells. This takes a week. After that, the shells are secure and the bacteria have outlived their usefulness.

So the weevil kills them.

It packages them up, breaks them down, and recycles their molecules for its own use. Their existence is a loan, and the weevil eventually demands repayment.

Heddi’s team, led by Aurelien Vigneron (now at Yale School of Public Health) found that the rise and fall of the weevil’s microbes plays out over just two weeks. The boom begins when the insect sloughs off its final larval shell and emerges as an adult. Its resident bacteria start multiplying, eventually quadrupling in number over a week. Then: the bust. The bacteria start to die. By two weeks, they’re completely gone. The bacteriomes that housed them change from plump grapes to shrivelled raisins.

Why are the bacteria useful during those first weeks of adulthood, but not afterwards? The team found a clue in the weevils’ colour. Normally, their shells are a dark, almost black-ish brown. But if the researchers killed off the Sodalis symbionts at an early age, the insects’ shells were lighter and rust-coloured. They were also thinner and weaker.

The difference boils down to two amino acids—phenylalanine and tyrosine—that are crucial for hardening and tanning the weevil’s shell. Unfortunately, these same substances are rare in the grains that the weevils eat—an unfortunate shortfall that threatens to leave them with feeble armour. But Sodalis comes to the rescue. It makes the two amino acids, and so supplements the weevil’s deficient diet.

This is why Sodalis is so important in those two weeks of adulthood. That’s when the beetle creates its final protective shell, a trait that will determine its odds of survival, its ability to fly, and more. In these crucial weeks, its supply of Sodalis expands to meet its skyrocketing demand for phenylalanine and tyrosine.

When the shell-making process is finished, the weevils turn on their symbionts. The cells that house Sodalis initiate a program that recycles their innards by packaging them up and breaking them into raw materials. This process, known as autophagy, allows cells to free up nutrients in times of need or to kill invading germs; here, the weevil uses it to destroy its symbionts. It also mobilises executioner enzymes in the cells that make up the bacteriomes, causing them to self-destruct. It’s like a foreman that melts every machine in the factory for scrap, before blowing up the building.

This destruction is clean and coordinated. By digesting the bacteria, the insect prevents any components from leaking into its bloodstream and triggering an immune reaction. It also partly recovers the materials and energy that it invested in nurturing the bacteria during the previous week.

This whole process might be self-controlled. The two amino acids that the bacteria provide are processed into a third one called DOPA. If Heddi’s team fed the weevils with DOPA, the insects eliminated their symbionts two days earlier than usual. It seems that as this substance builds up, it triggers the weevil’s shift from cultivation to culling.

How should we view this relationship? On one hand, it’s hard to see it as a two-way partnership. The bacteria are more like living tools that the insect uses to build its own body, and casually recycles when the job is done.

But there’s an important twist: not all the bacteria die. A smaller population of Sodalis blooms in the ovaries, and they are never reclaimed. They survive, so that they can pass to the next generation of weevils. These ovarian bacteria are either clones or very close relatives of those in the gut; they’re all descended from the same inherited stock. So even though the gut bacteria die, their genes will still pass to the next generation of weevils via their ovarian kin.

Perhaps, the right way to think of them is as workers in an ant or bee colony. They are born, they do their jobs, and they die without ever reproducing, all so that the queen (who shares much of their genes) can found future colonies. In the same way, the gut Sodalis live brief but necessary lives, allowing their host to survive and their ovarian sisters to infect future weevils.

Reference: Vigneron, Masson, Vallier, Balmand, Rey, Vincent-Monegat, Aksoy, Aubailly-Giraud, Zaidman-Remy & Heddi. 2014. Insects Recycle Endosymbionts when the Benefit Is Over.