Left: Termite mound in Senegal, by H. Grobe. Right: Macrotermes soldier by Discott.
Left: Termite mound in Senegal, by H. Grobe. Right: Macrotermes soldier by Discott.

The Guts That Scrape The Skies

Take a walk through the African savannah and you might stumble across huge mounds, made from baked earth. They tower up to 9 metres tall, and are decorated with spires, chimneys and buttresses. These structures are homes, nurseries, and farms, all in one. They are also guts. They’re part of one of the most fascinating digestive systems on the planet—a distributed organ that begins inside the bodies of tiny insects and expands into towers that scrape the skies.

They are the work of a termite, Macrotermes natalensis. Like most of its kin, it eats wood and other plant matter. There are vast amounts of energy locked within the chemical bonds of wood, a fact that we attest to whenever we burn logs to heat our homes. But breaking those bonds is a demanding task. Humans lack the enzymes for the job. Termites fare better, but despite their reputation, their wood-breaking toolbox is surprisingly sparse. Instead, they rely on help.

M.natalensis is a farmer, which grows a fungus in its nest. It feeds the fungus with scraps of wood that the workers collect, chew, and regurgitate. The fungus spreads through this slurry and digests it, breaking apart the complex carbohydrates (known as lignocelluloses) into smaller sugary building blocks. The termites then eat the resulting compost. In their guts, legions of bacteria and other microbes take over, breaking down the sugars even further. Without the fungus or the microbes, the termites would be unable to eat.

So, the termite’s digestive system isn’t just a tube that runs through its body. It’s also a web of fungal threads growing in the many chambers of its nest, and a mass of microbes nestled within its gut. It’s a community of creatures from at least three kingdoms of life, which live inside the insect and outside it. It fills the termite’s body, and extends into the architecture of its homes.

This digestive alliance is an ancient one. Termites evolved from cockroaches around 150 million years ago and ever since, they’ve relied on gut microbes to launch assaults on tough plants. Around 30 million years ago, the macrotermites, the group to which M.natalensis belongs, added a new partner to the mix by domesticating an aptly named fungus called Termitomyces. The contract that sealed this partnership was a binding one. There are now 330 or so species of macrotermites and all of them cultivate Termitomyces, and nothing else.

This alliance has been spectacularly successful. Macrotermites are found throughout Africa and South Asia, and they shape the fates of entire ecosystems. They are lords of decay, breaking down the corpses of fallen plants and returning their stored energy back into the world. By pooling their powers with other minute partners, these uber-roaches can build cathedrals that are as tall as trees, while converting actual trees into termite flesh.

Michael Poulsen from the University of Copenhagen and Haofu Hu from BGI-Shenzen in China have now deciphered the different roles of the partners by sequencing the genomes of M.natalensis, the fungus it grows, and the microbes in its gut.

Between them, they wield a vast toolbox of plant-breaking enzymes called glycoside hydrolases (GHs), which cut the chemical bonds that link simple sugars into complex ones. There are 128 families of GHs and the three partners have 118 between them—an almost complete set. Most of these tools come from the gut microbes, while the fungus and (to a much lesser extent) the termite plug important gaps in the collection.

The fungus and the microbes seem to divide their digestive labours between them. The fungus excels at splitting large carbohydrates like lignin and cellulose into their constituents, but it’s no good at breaking down those constituents. That fits with its biology. Termitomyces isn’t so much a wood-eater as a wood-breaker. It sunders lignin to get at other nutrients deeper within a plant, rather than as an act of digestion itself.

The termite gut microbes, however, have plenty of enzymes that target the simpler sugars that the fungus produces. In fact, Poulsen and Hu found that the microbes in M.natalensis have far more of these enzymes than those in other termites that haven’t domesticated fungi.

So, the fungus launches the opening assault while the gut microbes land the finishing blows. The termites themselves contribute very little to these digestive labours. Their role is to grow and nurture the other partners.

This is a significant achievement. Termitomyces mushrooms are edible to humans and prized as delicacies in certain parts of Africa, but we have never been able to cultivate them. Termites can. These tiny-brained creatures construct mounds with in-built ventilation and air-conditioning, providing cool, humid oases in the parched savannah, where fungi can thrive. By building and nurturing these gardens, and by harbouring the right microbes in their bodies, the termites effectively cultivate their own digestive systems.

Poulsen and Hu found another twist to this tale: the M.natalensis queen is an oddity. She has none of the gut microbes that are most common in her workers, and her impoverished communities can only digest the very simplest of sugars. This fits with her biology. A macrotermite queen is an egg-laying machine, her abdomen grossly distended into a huge, white, pulsating sac. She can’t move. Instead, she relies on her worker daughters (and the microbes in their guts) to feed her.

It wasn’t always like this. The queen founded the entire colony and seeded her daughters with their gut microbes in the first place. Her own communities must have shrivelled later, even as her body expanded. You can think of the entire colony—workers, microbes, fungus, mounds and all—as her digestive system. It’s a huge symbiotic network that provides her with food and ensures the continuance of her genes.

Reference: Poulsen, Hu, Li, Chen, Xu, Otani, Nygaard, Nobre, Klaubauf, Schindler, Hauser, Pan, Yang, Sonnenberg, de Beer, Zhang, Wingfield, Grimmelikhuijzen, de Vries, Korb, Aanen, Wang, Boomsma & Zhang. 2014. Complementary symbiont contributions to plant decomposition in a fungus-farming termite. PNAS http://dx.doi.org/10.1073/pnas.1319718111