Evolutionary origin of termite gut microbiome revealed

Termites are among the rare organisms that can feed on wood. This remarkable ability has allowed them to become one of the most abundant animals in the terrestrial tropics, and they've got their gut bacteria to thank.

Many animals rely on microbial communities in their guts to aid the process of digestion. For instance, there are approximately 39 trillion bacteria in the human gastrointestinal tract. However, the termite gut microbiome is among the most complex of any animal group. It comprises a diverse mixture of bacteria, protists and fungi which can break down and extract essential nutrients from materials that are indigestible to most animals, such as lignocellulose in wood.

Biologists have studied the termite gut microbiota for more than a century, but they have disagreed over one important question: How did termite gut bacteria evolve?

Some studies say that termites inherited their gut microbial make-up from their parents -- a process called vertical transmission. Others argue that diet-specific lineages have been independently acquired from the environment over the course of evolution -- so-called horizontal transmission.

In the largest study to date examining the DNA of termite gut microbes, researchers at the Evolutionary Genomics Unit at OIST, in collaboration with colleagues at the University of Sydney, have an answer that unites both sides of the debate -- vboth.

"We found that termites predominantly acquire their gut bacteria both from their parents and from other termite colonies," says Professor Thomas Bourguignon, unit leader, "meaning that both vertical and horizontal transmission have been important during the 150 million years of termite evolution."

Past studies have relied on small sample sizes of 20 species or fewer, taken from a narrow range of locations and diet types. Here, however, Prof. Bourguignon and his colleagues analyzed 211 bacterial lineages from the guts of 94 different termite species, collected across four different continents -- Asia, Oceania, South America and Africa. Their results were published in the journal Current Biology.

They extracted bacterial DNA from termite guts and sequenced a specific stretch of genetic material called 16S rRNA, which is often used to identify bacterial species. With this genetic information, they could reconstruct family trees showing the evolutionary history and relationships between bacterial species.

Their results showed that termite gut microbiomes have been shaped by "mixed-mode" transmission, which combines colony-to-offspring vertical transmission with colony-to-colony horizontal transfer.

When bacteria are transferred vertically between termite generations, they can co-evolve with their termite hosts, becoming highly specialized to their diets, habitats, and diseases. "Many of the bacteria we found only exist inside termites, and some of these only inside specific regions of the termite gut," says Prof. Bourguignon.

Vertical transmission is important to the human gut microbiome too -- in 2016, biologists showed that we humans inherited some gut microbes from the ancestors we share with our great ape cousins.

However, certain features of the termite lifestyle mean that they are also prone to horizontal transmission of gut bacteria. Bacteria can be transferred between termites during fights because the stronger termite often eats the weaker contender. Termites may also acquire gut bacteria from other species of termites, or even other animals entirely, through soil or other food sources by ingesting fecal matter.

The finding that some bacteria have switched hosts during the course of evolution could mean that some species of termite gut bacteria are much more widespread among the guts of other organisms than we once thought.

The Evolutionary Genomics Unit is now conducting further research into the genetics of termite gut bacteria, hoping to discover more about the specific enzymes that the bacteria use to break down wood -- a process biologists still know little about.

"There is still much to learn about this fascinating group of animals," says Bourguignon.