O. algarvensis can thrive on these poisons thanks to millions of symbiotic bacteria that live under its skin. The bacteria use the energy from carbon monoxide and hydrogen sulphide to produce food for the worm, just like plants do by fixing carbon dioxide into carbohydrates - but instead of using light energy from the sun, the symbionts use the energy from chemical compounds like carbon monoxide.
It's so effective the worm has lost its entire digestive system, including its mouth and gut, during the course of evolution, and feeds only through its symbionts, explains Nicole Dubilier, Head of the Symbiosis Group at the Bremen-based Max Planck Institute.
Carbon monoxide and hydrogen sulfide are not the only energy sources this worm can live on. Some of the symbiotic bacteria in the worm can take up hydrogen and organic nutrients from the environment, even if these are present in only tiny amounts. Olavius algarvensis, unlike most animals, can recycle their own waste products thanks to its symbiotic microbes. The symbionts are true recycling masters.
Olavius algarvensis. © C. Lott/HYDRA/ Max Planck Institute for Marine Mikrobiology, Bremen
"This is the reason why the worm has been able to not only reduce its digestive system, but also its kidney-like excretory organs," notes Dubilier, "something that has not been discovered in any other marine animal."
For their investigations, the researchers used metaproteomics and metabolomics, which make it possible to analyze a large proportion of the proteins and metabolic products in an organism. Metaproteomic analysis presented a particular challenge, as it required the researchers to separate the cells of the symbionts and the host. Thomas Schweder from the Institute of Pharmacy at Greifswald University explained, "Using metaproteomics, we were able to identify thousands of proteins and assign them to the individual partners in the symbiosis. This gave us direct insights into the metabolism of the bacterial symbionts and their interactions with the host."
The researchers were surprised when their analyses revealed that the worm has large amounts of proteins that allow it to use carbon monoxide as an energy source, because this gas is so poisonous. "Also, we couldn't imagine that carbon monoxide is present in the worm's environments", said Manuel Kleiner, a doctoral student in Nicole Dubilier's research group, "so we were amazed to find such unusually high concentrations of carbon monoxide in the Elba sandy sediments."
Nicole Dubilier said, "We have known for quite some time that the symbiotic bacteria in Olavius algarvensis can interact with one another to use the energy-rich sulfur compounds to gain energy." But it is only now that the researchers have been able to work out other metabolic pathways – and to discover new energy sources. The study highlights the importance of complementing metagenomic analyses with metaproteomics and metabolomics. "The worm provides us with an example of the power of evolution. Over the course of millions of years, adaptation and selection have led to the development of an optimally adapted host-symbiont system. And these seemingly modest worms are an excellent model for a better understanding of other complex symbioses, such as those of the human gut."
Published in Proceedings of the National Academy of Sciences
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