Great idea, but

The early attempts to see what genetics could say about the tree of life seemed to work beautifully. But “science doesn’t go in a linear path,” says Andrew Roger of Dalhousie University in Halifax, Canada, who entered the field during the tumultuous 1990s.

Those first genetics-based trees of life for eukaryotes were built by comparing variations in the gene for small subunit ribosomal RNA across species. The result looked believable, with plants, animals and fungi on big branches at the top. Lower down, in the zone for more ancient branches, sprouted some oddball parasites such as Giardia (the bane of hikers who drink untreated water), sexually transmitted Trichomonas and tiny micro­sporidia, which attack many animals.

Engulfing another organism and turning it into an organelle has been important in the history of complex life. Even engulfers get engulfed themselves sometimes.

J. Hirshfeld; Source: A. Worden et al/ Science 2015

Researchers had begun to wonder if these bizarre parasites and their relatives could be living relicts of an early, pivotal time in eukaryote history. The organisms had no obvious mitochondria, the organelles that serve as the cell’s power stations. Perhaps the parasites had never had any mitochondria, Thomas Cavalier-Smith of the University of Oxford had suggested in 1983. This notion played off the idea championed by maverick biologist Lynn Margulis at Boston University in 1970 in The Origin of Eukaryotic Cells. She suggested that mitochondria came from a free-living microbe that some ancestor of eukaryotes had swallowed and put to work. Perhaps the parasites were relicts from before the Big Swallow.

To use these select parasites as glimpses of life before mitochondria “would be really, really interesting,” says Dalhousie biologist Alastair Simpson. “It was a lovely hypothesis. But then it all went to hell.”

One problem came when researchers expanded their analyses to look at more than one gene. Unexpectedly, says Roger, “we had different genes saying different things.”

The potential unraveling of the parasites-as-relicts hypothesis had a special zing for Roger. He was in the middle of a Ph.D. project based on the assumption that the parasites came from premito­chondrial times. “It was one of those cases when you’re trying to work on the carpet that’s being pulled out from under you,” he says. “I thought it was pretty exciting.”

Yes, he said “exciting.” That view of eukaryote evolution based on analysis of a single gene “was in textbooks, and it was what many people had made their careers on,” he says. “It seemed like if it was going to fail, it was going to be something big.” He and his lab mates were going to be in on it.

Roger and his colleagues struck a blow to the old hypothesis by looking for genetic traces of bygone mitochondria lingering in the cell nucleus of select parasites. Even though mitochondria need some 700 to 1,000 genes to operate, only about 10 to 100 of them are inside the organelle itself. The rest reside in the cell nucleus and ship proteins to the mitochondria. The researchers detected some left-behind nuclear genes in supposed ancients, such as Giardia, Trichomonas and some microsporidia.

Various research groups eventually found the tiny, overlooked remnants of mitochondria themselves inside the fake relicts. The parasites looked very ancient only because their mitochondria had shriveled into hard-to-recognize bits.

Microsporidia, it turned out, were nowhere near being relicts. Examining a handful of genes, Keeling and other researchers demonstrated that the single-­gene tree had put microsporidia in the wrong kingdom.

Microsporidia are “really nasty parasites, but fascinating,” Keeling says. Their tough spores enclose a coiled tube. To infect a victim, they pump inward such a rush of water that the pressure blows the top off the parasite and the tube shoots out like a harpoon. As much as 100 times longer than the spore, the tube-harpoon punches into its prey. The parasite cell nucleus and other internal parts are injected through the tube into the victim. Although they have this elaborate equipment for infection, microsporidia are simple cells with genomes that are “tiny, tiny, tiny,” Keeling says. Another misleading hint that they were ancient, simple creatures.

STRUCTURAL BEAUTY Ernst Haeckel’s remarkable drawings of microscopic organisms (radiolarians shown) introduced generations to the beauty of complex, single-celled life. Even in the 19th century, he protested biologists’ neglect of microbial marvels.

Ernst haeckel/ Kunstformen der Natur 1904

Keeling and his colleagues in the 1990s found evidence that the microharpooners didn’t belong at the bottom of the tree. They were fungi, a more recent and much more metabolically versatile branch of organisms. Before this revelation of misclassification, researchers accepted the simplicity of microsporidial cells by assuming that complicated traits hadn’t evolved in supposedly ancient, simple cells. After recognizing microsporidia as members of the fungal kingdom with all its elaborate metabolic tricks and lifestyles, biologists could see that microsporidia had been more complex at one time, but eventually lost fancy traits. “You have the exact opposite view of how they got to be the way they are, based on where they go on the tree,” Keeling says. “The tree matters.”

As evidence built that the supposed ancient parasites and their relatives weren’t so ancient, “smart people worked out that the molecular trees were just wrong,” Simpson says. The problem, now widely recognized, was the peril of “long-branch attraction.”

Lineages that change a lot end up as long-branch lines in an evolutionary tree. Younger branches that change fast can by chance develop similarities to genuinely old branches. In simple analyses, they end up closer than they should be at the base of the tree, as if they’ve “attracted” each other.

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