Grand Prismatic Spring in Yellowstone National Park. A haven for archaea. Credit: Jim Peaco, National Park Service
Grand Prismatic Spring in Yellowstone National Park. A haven for archaea. Credit: Jim Peaco, National Park Service

A Flood of Borrowed Genes at the Origins of Tiny Extremists

We love origin stories. When we see successful groups of animals and plants, we wonder where they came from, and how they rose to power. How did the tetrapods—the group of four-legged animals that we belong to—start walking on land? What made the insects the most diverse group of animals on the planet? Why did flowering plants suddenly start diversifying during the Cretaceous period, filling the world with blossoms?

These enduring questions are so fundamental to biology that we sometimes forget how strongly they’re influenced by the limits of our senses. We can see the creatures they concern with our naked eyes. We can observe changes in their bodies, and we can tell that they must have gone through transformations from fins to legs, or needles into petals.

It’s much harder to make such observations when you deal with microbes. At that scale, it’s not so much physical features that set organisms apart, but genetic and biochemical ones. Groups differ more in what they do rather than what they look like. So to discover their origin stories, or even to know which origin questions to ask in the first place, you need to study their genes.

Shijulal Nelson-Sathi did this for the archaea, a group of single-celled microbes that excel at growing in extreme and inhospitable places. Volcanic springs and salty lakes—these are places where archaea thrive, although some also live in milder environments like your intestines.

Superficially, archaea look like bacteria and for the longest time, that’s what scientists thought they were. That changed in 1977, when the revolutionary scientist Carl Woese showed that archaea and bacteria were genetically distinct. Woese drew a tree of life with three great trunks or “domains”. The bacteria sat on one. The eukaryotes—the group that includes animals, plants, fungi and algae—occupied another. And the archaea were the third. Woese elevated these obscure extremists to one of life’s highest ranks. And he was right. As I’ve written before, archaea and bacteria turned out to be as different in their biochemistry as PCs and Macs are in their operating systems.

The archaea are still mysterious. No one knows, for example, how many species there are. But scientists have sequenced the complete genomes of at least 134 of them and, based on differences in their genes, classified them into 13 major groups. So, the classic origin questions raise their heads: how did these groups arise, and why?

To find answers, Nelson-Sathi developed software that took all the genes in every known archaeal genome and grouped them into some 26,000 families. At least two-thirds of these families were invented by archaea, and have no counterparts among other living things. And 85 percent of them are found in only one of the 13 major groups—an indication of just how distinct these lineages are from one another.

And then, the team found something weird.

In the Haloarchaea, a group of archaea that grow in extremely salty water, the team found 1,000 gene families that had originally come from bacteria. Some time ago, an ancestral Haloarchaean borrowed genes on a massive scale, and this loan happened at the origin of the group.

The team then looked at the other 12 lineages and found exactly the same pattern. The origin of every major archaeal group was marked by the acquisition of bacterial genes—sometimes dozens, sometimes thousands. They borrowed, then they branched out. “The implication here is that such transfers played an important role in the actual establishment of the groups themselves,” says John Archibald from Dalhousie University.

“It was a surprise for us,” says Bill Martin from Heinrich-Heine University in Dusseldorf, who led the study. “You might ask why no one else has seen this before.” It’s probably because most scientists focused on the essential “core genes” that are common to all archaea. But the core genes comprise just 1 percent of the genome. They can tell us the shape of the archaeal family tree, but they say nothing about the characteristics that define the branches. To do that, you need to look at the entire genome, which is exactly what Nelson-Sathi did.

The “horizontal gene transfers” that he found are alien to us humans, who can only pass genes from parent to child. But bacteria and archaea don’t suffer the yoke of vertical inheritance. They can pass genes to one another with great ease.

These transfers could flow in either direction but in reality, they were mostly one-way. Nelson-Sathi found that bacteria have donated gene families to archaea five times more frequently than vice versa, and none of the archaea-to-bacteria transfers correspond to the rise of major bacterial groups. Bacteria have repeatedly thrust their archaeal peers into new evolutionary directions, but the reverse isn’t true.

Why? Here’s a clue: most of the gene families that moved from bacteria to archaea are involved in metabolism. That is, they help their owners to exploit new sources of energy. Another clue: most of the recipients are methanogens—archaea that can grow on carbon dioxide and hydrogen alone. This trick allows methanogens to survive in deep-sea vents, cow guts, Greenland ice, and baking desert soils. But it’s also about as simple and specialised a lifestyle as you can get.

The methanogens are specialists that have colonised many difficult but narrow niches, and become stuck in their ways. They’re like the microbial version of pandas. “They’re rock-bottom. The only way is up,” says Martin. “And the only way they have of reaching new niches is to let bacteria do the inventing.” By borrowing bacterial genes, these specialists could carry out new chemical reactions and expand beyond their extreme niches.

“I think most of us envisaged horizontal gene transfer happening a gene at a time,” Martin adds. “You get one in here or there, and you tinker. But that doesn’t’ work very well when you’re changing your lifestyle. When you change a methanogen into something that isn’t, one gene at a time won’t help very much. Instead, it looks like the genes were coming in big chunks. We see lump acquisition, the wholesale introduction of new pathways.”

“This paper is one of the best demonstrations of the key role of horizontal gene exchange in the evolution of prokaryotes,” says Eugene Koonin from the National Center for Biotechnology Information. (Prokaryotes is a term that refers to both bacteria and archaea.) But Koonin adds that it’s now time to nail down the specifics.

Archibald agrees. The study “provides strong evidence for the existence of gene-sharing pathways in the evolutionary history of prokaryotes,” he says. But it’s a starting point. The team now need to follow up on each major archaeal group and working out how the bacterial genes changed the abilities and the lives of their recipients.

Of course, this is not the first indication that bacteria have dramatically changed the evolution of archaea. Martin and others have argued that the origin story of all complex life on Earth began when a bacterium and an archaeon fused together. This singular and incredibly improbable event provided the archaeal host with a source of extra energy, allowing it to become big and complex in a way that none of their kin could manage. That was the birth of the eukaryotes—the unique merger that made you and ewe and yew. You can read more about this extraordinary story in my Nautilus feature from earlier this year.

Reference: Nelson-Smith, Sousa, Roettger, Lozada-Chavez, Thiergart, Janssen, Bryant, Landan, Schonheit, Siebers, McInerney & Martin. 2014. Origins of major archaeal clades correspond to gene acquisitions from bacteria.