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A species of roundworms in the genus Pristionchus possesses genes for digesting cellulose that were likely acquired millions of years ago from slime mold. Researchers of the Max Planck Institute for Biology in Tübingen found this rare example of horizontal gene transfer between higher organisms and were also able to explain its evolutionary advantages for the round-worms: it is as if one was able to eat a pizza with the box it comes in. The findings are now published in the Journal Molecular Biology and Evolution.
Just like individuals receive most genetic material ‘vertically’ from their parents, species inherit their genetic information mostly in a vertical line from their direct ancestors. This gives rise to the image of the tree of life, which connects all life on Earth by its common ancestry.
Horizontal connections in the web of life
But in reality, the tree of life is rather a web of life with myriads of additional horizontal links. ‘Horizontal’ genetic connections occur when different individuals or species exchange genetic ma-terial. Most frequently, this occurs in bacteria, who trade parts of their DNA with each other – one of the main causes of drug resistance.
One of these horizontal connections in the web of life – and a rather surprising one – are cellulase genes found about 15 years ago in Pristionchus pacificus. Pristionchus pacificus is a species of nematodes, little roundworms which are only few millimeters in length. The genes make it possi-ble to digest cellulose, the main component in cotton or paper. But why the nematodes possess these genes baffled researchers until recently.
Ziduan Han, who led the team at the Max Planck Institute for Biology who now uncovered the bio-logical function of the gene, comments on the puzzle: “Cellulose is mainly produced by plants; but our Pristionchus pacificus worms feed on microbes, not on plants. So, it is not obvious that they would possess a gene that facilitates digestion of cellulose.”
Interspecies gene comparison suggests slime mold origin
More precisely, the genes cause the worm to produce the enzyme cellulase. Cellulase is used by many microorganisms to break up cellulose into simple sugars; it is the enzyme that enables them to feed on plants. Like many microbes, Pristionchus pacificus secretes the cellulase into its food – a slimy biofilm produced by bacteria.
The researchers were able to trace where the genes likely came from by comparing them to cellu-lase genes for cellulose digestion in other species. In all likelihood, the worm acquired the gene from a slime mold, a kind of amoeba. “Horizontal gene transfers between eukaryotes – organisms with a proper cell nucleus like animals or plants, or in this case the worm and the amoeba – are a truly rare find”, states Han.
Eating the pizza with its box as an evolutionary advantage
But what really intrigued Han was the evolutionary role of the gene: “The real puzzle was, why has evolution apparently favored a gene for plant digestion in these non-plant eating worms?” When the worms originally acquired the cellulase gene at least a dozen million years ago, it was by mere chance. But since then, the gene was not only preserved, but was multiplied and is now present in eight copies in the nematode’s genome. To answer why this happened, Han and his col-laborators knocked out all eight copies of cellulase genes using CRISPR in some of the nematodes. The resulting mutants were thriving, but they did fall behind their cellulase producing peers signif-icantly in two aspects: they produced less offspring, and their developmental cycle was slower.
Cellulose is contained in rather small quantities in the bacterial biofilm the nematodes feed on. It stabilizes the biofilm and thereby makes it harder for predators like the nematodes to feed on the bacteria. By analyzing data from mutant and wild type worms in different food situations, the re-searchers concluded that the ability to secrete cellulase benefits the nematodes in two ways: the worms use the cellulase to break up the biofilm to reach the nutrients in it, and they also digest the cellulose itself.
“Secreting cellulase is as if you had the ability to eat the pizza with the box it comes in”, says Han. “You would have the double benefit of getting extra nutrients from the cardboard and at the same time being able to start eating right away without even opening the box.”
In a next step, Han wants to investigate the mechanisms of competition and altruistic behavior that may arise when other nematodes try to benefit of the cellulase secreted by another one of their kind.
Ziduan Han is supported by the Humboldt Research Fellowship.
Dr. Ziduan Han
Max Planck Institue for Biology Tübingen
email: ziduan.han@tuebingen.mpg.de
Ziduan Han, Bogdan Sieriebriennikov, Vladislav Susoy, Wen-Sui Lo, Catia Igreja, Chuanfu Dong, Aileen Berasategui, Hanh Witte, Ralf J Sommer: Horizontally Acquired Cellulases Assist the Ex-pansion of Dietary Range in Pristionchus Nematodes, Molecular Biology and Evolution, Volume 39, Issue 2, February 2022, msab370, https://doi.org/10.1093/molbev/msab370
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