No Guts, No Worries: Worm Enlists Full-Service Microbes For Transportation, Energy, & Waste Management

From a species of marine oligochaete worm isolated off of the coast of Elba, the Mediterranean island of Napoleon's exile, scientists from the U.S. Department of Energy's Joint Genome Institute (DOE JGI) have described this complex worm/microbe quid pro quo revealed by DNA sequencing and other diagnostic techniques. Their results are published in the September 17 edition of the journal Nature.

The worm, Olavius algarvensis, has no mouth to take in food, but does not go hungry, thanks to the goodwill of its hardworking bacterial tenants. In the transaction, the worm shuttles the bacteria to optimal energy sources it encounters wending its way between the upper oxygen-rich and the lower oxygen-depleted coastal sediments. In exchange, fixed carbon, all required amino acids and vitamins are synthesized by the subcuticular communities of microbial symbionts, providing their host with ample nutrition.

On the other end of the digestive equation, such waste products as ammonium and urea, generated by the worm's metabolism, are taken up by these symbionts—not only aiding the host in the removal of these toxic waste products, but also conserving valuable nitrogen, further maintaining the microbial community.

"It's an excellent example of outsourcing energy and waste management, where this worm and the microbes living under its skin are enjoying a mutually beneficial relationship," said Eddy Rubin, DOE JGI Director. The work was conducted by postdoctoral fellow Tanja Woyke and colleagues from the Rubin lab at DOE JGI and Lawrence Berkeley National Laboratory, and collaborators led by Nicole Dubilier, Head of the Symbiosis Research Group in the Department of Molecular Ecology at the Max Planck Institute for Marine Microbiology in Bremen, Germany.

"The microbes, floating around in the sea, strike up a bargain with the worm—in exchange for housing, the microbes take care of energy production and handling the waste," Rubin said. The team had a hunch that this pact was taking place, because without a mouth or an anus, the worm's survival begged the question. O. algarvensis has no semblance of a renal or kidney system—revealing itself as one of nature's oddities.

The team uncovered the unique method of waste management employed by Olavius algarvensis by metagenomics, a strategy pioneered by DOE JGI and its collaborators. This technique entails isolating, sequencing, and characterizing DNA extracted directly from environmental samples—to obtain a profile of the microbial community residing in a particular environment. This is the first instance of such a symbiotic relationship being analyzed by using a metagenomic shotgun sequencing approach, heralding a renaissance in symbiosis research.

In this experiment, Woyke donned scuba equipment and dove into the Mediterranean to sift through tons of sediment to uncover enough of the worms and their microbial contents, which, like the vast preponderance of microbial life, cannot be grown in the laboratory.

What they found particularly unusual about this worm/bacteria relationship was that several different microbes came into play, unlike most symbiotic interactions between larger organisms and microbes where usually only one microbial species is present.

For the study in question, a total of 204 million bases, or units of genetic code, were generated. Through a process known as "binning," a protocol developed by collaborating author Frank Oliver Glöckner from the Max Plank Institute, these sequences were then organized by specific DNA signatures to reveal the identities of particular microbial species.

"By sequencing the genomes of the microbes we were able to discern how they cope with the needs of the worm and why such a diversity of microbes is warranted," Rubin said. It turns out that the worm isn't just housing for the microbes, but is also transportation. The worm burrows into the sediment and as it heads for different environments, each with different chemical constituents, provides energy adapted to the capabilities of a particular group of microbes. As the worm doesn't have a mouth, the microbes use chemical energy from the sediment, perfusing through the skin, to convert organic material into the stuff that nourishes the worm.

"It's not unlike a car with a hybrid motor that can run on both electricity and gas depending on the situation," Rubin said. "In certain places the worm is powered by specific bacteria that can exploit the chemical energy abundant at a specific location, while in other strata, where a different chemical energy source is abundant, the worm switches its energy production to resident bacteria that can exploit that available energy source."

Rubin suggested that society could learn a lot from the tale of the worm and its helpful microbial buddies and their successful adaptive lifestyle. "We have been dependent on fossil fuels. In the future we need to adapt like this worm has and use a variety of different energy sources to ensure our needs can be met in a changing world."

The work was conducted under the auspices of the DOE JGI's Community Sequencing Program (CSP). The goal of the CSP is to provide a world-class sequencing resource for expanding the diversity of disciplines—oceanography, geology and ecology, among others—that can benefit from the application of genomics, particularly at the intersection with DOE mission areas of bioenergy, carbon cycling, and bioremediation. Additional support for the project came from the Max Planck Society.

The DOE Joint Genome Institute, supported by the DOE Office of Science, unites the expertise of five national laboratories, Lawrence Berkeley, Lawrence Livermore, Los Alamos, Oak Ridge, and Pacific Northwest, along with the Stanford Human Genome Center to advance genomics in support of the DOE mission related to clean energy generation and environmental characterization and clean-up. DOE JGI's Walnut Creek, Calif. Production Genomics Facility provides integrated high-throughput sequencing and computational analysis that enable systems-based scientific approaches to these challenges.