Western corn rootworm. Credit: Joe Spencer.
Western corn rootworm. Credit: Joe Spencer.

Gut Bacteria Allows Insect Pest to Foil Farmers

Here is a lesson that we’re going to be taught again and again in the coming years: Most animals are not just animals. They’re also collections of microbes. If you really want to understand the animal, you’re also have to understand the world of microbes inside them. In other words, zoology is ecology.

Consider the western corn rootworm—a beetle that’s a serious pest of corn in the US. The adults have strong preferences for laying eggs in corn fields, so that their underground larvae hatch into a feast of corn roots. This life cycle depends on a continuous year-on-year supply of corn. Farmers can use this dependency against the rootworm, by planting soybean and corn in alternate years. These rotations mean that rootworms lay eggs into corn fields but their larvae hatch among soybean, and die.

But the rootworms have adapted to this strategy by reducing their strong instincts for laying eggs in corn. These ‘rotation-resistant’ females might lay among soybean fields, so their larvae hatch into a crop of corn.

There are almost certainly genetic differences that separate the rotation-resistant rootworms from their normal peers, but what are they? Researchers at the University of Illinois have been studying the problem since 2000 and, despite generating a vast mountain of data, have failed to find the genes in question. “The western corn rootworm has been an enigma for long time,” says Manfredo Seufferheld. “This insect has the ability to adapt to practically all control methods deployed against it, including crop rotation. After many years of research about the mechanisms of rotation resistance, results were mostly inconclusive.”

So, Seufferheld looked elsewhere. Rather than focusing on the rootworm’s own genes, he studied the genes of the bacteria in its gut… and found some answers. The rotation-resistant varieties have very different gut bacteria to the normal ones. And when the team killed these microbes with antibiotics, they severely reduced the beetle’s ability to cope with rotation.

“The bad guy in the story—the western corn rootworm—was actually part of a multi-species conspiracy,” says Joe Spencer, who was part of the study. “No wonder it was hard to figure out what was happening. We were only looking at the most obvious aspects of the story.”

The team, including graduate student Chia-Ching Chu, found that a third of the rootworms’ gut bacteria comprise species that are unique to either the resistant or normal varieties (the green and gray groups in the diagram below). These two factions also differ in the relative numbers of the bacteria that they share (compare the orange and blue groups).

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Gut bacteria in a normal and rotation-resistant western corn rootworm.

These changing microbes give the resistant beetles an edge when eating soybean. The rootworms digest the protein in their meals using enzymes called cysteine proteases, and soybeans defend themselves with substances that can block these enzymes. But Chu found that the more the beetles’ bacteria differed most from the ‘normal’ set, the higher the levels of cysteine proteases in their guts. By avoiding indigestion, these beetles were better at surviving among soybeans, and more likely to lay their eggs there. Across the US Corn Belt, there’s a gradient of gut microbes that affect how well the beetles cope with our farming practices.

The team proved that the bacteria were responsible by killed them with antibiotics. Sure enough, this drastically  lowered the cysteine protease activity in the guts of the rotation-resistant beetles (but not the normal ones) and wrecked their ability to thrive among soybeans.

So, if you really want to understand the animal, you’re also have to understand the microbes. The rootworm’s gut bacteria are effectively another one of its organs, but an astonishingly flexible one that can change dramatically when exposed to a new food source. This allows the insects to adapt very quickly to environmental challenges, far more quickly than if they could only rely on mutations in their own genes.

The bacteria are certainly part of the rotation-resistance puzzle, but it’s not clear how big their role is. Seufferheld still wants to know how the insect’s own genes affect their ability to live among soybean, how they control the bacterial communities in their guts, and how those different communities emerge in the first place.

Such studies might give us clues about how to control the rootworm. Spraying fields with antibiotics is out of the question—these drugs have already been heavily misused in agriculture to the detriment of our own health.  “I don’t think we’ll be crop-dusting western corn rootworms to manage their adaptable gut microbes,” says Spencer. “I do think we need consider how those microbes might interact with our pest management tactics.”

He adds, “Modern agriculture has always underestimated the ability of pests to circumvent pest control, and I think the realization that pest insects are not alone in their efforts should give us some pause. There is a brand new tiny world out there inside every creature, and we need to start thinking seriously about it.”

Reference: Chua, Spencer, Curzi, Zavala & Seufferheld. 2013. Gut bacteria facilitate adaptation to crop rotation in the western corn rootworm. PNAS http://dx.doi.org/10.1073/pnas.1301886110