Waste not, want not: highly efficient waste recycling in bacteria-worm symbiosis

EMBARGOED UNTIL: Monday 5/20, 3 PM MDT

(Symposium Session 139, Paper )

Manuel Kleiner
Max Planck Institute for Marine Microbiolgy
Bremen, -null-, Germany
Phone: 49-421-2028905
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A small marine worm has developed an extremely efficient way of recycling its waste products. Instead of excreting these, as most other animals do, this worm profits from its metabolic waste with the help of bacterial symbionts that live under the worm’s skin. The symbionts are so efficient in recycling their host's waste that these worms have lost the kidney-like excretory organs that nearly all other animals have. In our study, we discovered a novel pathway that enables the symbionts to function as highly efficient recycling centers by using the metabolic waste products of the worm to produce a special storage compound called polyhydroxyalkanoate (PHA). PHA is used by biotech companies to produce sustainable and biodegradable plastics, and the novel pathway we discovered could be useful for turning waste products from bioreactors, waste water treatment plants and landfills into bioplastics.

The work that we present here at the General Meeting of the American Society for Microbiology (ASM) in Denver on Monday May 20 was done at the Max Planck Institute for Marine Microbiology in Bremen, Germany (Manuel Kleiner, Cecilia Wentrup and Nicole Dubilier) in collaboration with Manuel Liebeke from the Imperial College in London, Jan Zarzycki from the Joint Genome Institute in Walnut Creek, CA and scientists from the ETH in Zurich, Switzerland (Patrick Kiefer, Julia Vorholt). The work was funded by the Max Planck Society.

Details:

The marine worm Olavius algarvensis lacks both a digestive and an excretory system, and relies instead on a symbiotic community of five symbionts for its nutrition and waste recycling. This worm's microbiota consists of a primary symbiont that uses reduced sulfur compounds as an energy source to generate organic compounds from carbon dioxide, and four secondary symbionts. In this study, we discovered proteins for a novel metabolic pathway in the primary symbiont of O. algarvensis, which would allow it to assimilate large amounts of the fermentative host waste products acetate and propionate into the storage compound polyhydroxyalkanoate (PHA). This novel pathway would enable the symbiosis to recycle energy and carbon rich compounds instead of loosing them to the environment. To examine if this pathway is really used for host waste assimilation by the primary symbiont, we incubated worms in the presence of 13C labeled acetate and propionate and found massive assimilation of these substrates into total worm biomass. We then followed substrate incorporation into O. algarvenis symbionts at the single cell level using a new method called nanoscale secondary ion mass spectrometry (NanoSIMS) combined with fluorescence in situ hybridization (FISH). NanoSIMS provides images of single bacterial cells that can show if these have taken up an isotopically labeled substrate such 13C-labeled acetate or propionate. When combined with FISH, a method that identifies the microbe of interest, one can resolve which microbial species has taken up the labeled compound.

The combined NanoSIMS/FISH approach showed that labeled acetate and propionate were assimilated in large amounts by the primary symbiont of O. algarvensis. We then used nuclear magnetic resonance spectroscopy to examine which PHA compounds the symbionts produced. We found that the primary symbiont assimilates acetate into polyhydroxyvalerate (PHV) and propionate into polyhydroxymethylvalerate (PHmV), both important precursors for bioplastics production. The pathway that we have begun to elucidate could be useful for bioplastics production because acetate is one of the major waste products in effluents from waste water treatment plants, H2 producing bioreactors and landfills, and therefore a cheap starting material for producing bioplastics.