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Proc Natl Acad Sci U S A. 2019 Apr 23;116(17):8505-8514. doi: 10.1073/pnas.1818995116. Epub 2019 Apr 8.

Chemosynthetic symbiont with a drastically reduced genome serves as primary energy storage in the marine flatworm Paracatenula.

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Max Planck Institute for Marine Microbiology, 28359 Bremen, Germany.
Department of Geoscience, University of Calgary, AB T2N 1N4, Canada.
Department of Plant & Microbial Biology, North Carolina State University, Raleigh, NC 27695.
Institut de Minéralogie, Physique des Matériaux et Cosmochimie, Université Pierre et Marie Curie, 75252 Paris Cedex 05, France.
Max Planck Institute for Marine Microbiology, 28359 Bremen, Germany;


Hosts of chemoautotrophic bacteria typically have much higher biomass than their symbionts and consume symbiont cells for nutrition. In contrast to this, chemoautotrophic Candidatus Riegeria symbionts in mouthless Paracatenula flatworms comprise up to half of the biomass of the consortium. Each species of Paracatenula harbors a specific Ca Riegeria, and the endosymbionts have been vertically transmitted for at least 500 million years. Such prolonged strict vertical transmission leads to streamlining of symbiont genomes, and the retained physiological capacities reveal the functions the symbionts provide to their hosts. Here, we studied a species of Paracatenula from Sant'Andrea, Elba, Italy, using genomics, gene expression, imaging analyses, as well as targeted and untargeted MS. We show that its symbiont, Ca R. santandreae has a drastically smaller genome (1.34 Mb) than the symbiont´s free-living relatives (4.29-4.97 Mb) but retains a versatile and energy-efficient metabolism. It encodes and expresses a complete intermediary carbon metabolism and enhanced carbon fixation through anaplerosis and accumulates massive intracellular inclusions such as sulfur, polyhydroxyalkanoates, and carbohydrates. Compared with symbiotic and free-living chemoautotrophs, Ca R. santandreae's versatility in energy storage is unparalleled in chemoautotrophs with such compact genomes. Transmission EM as well as host and symbiont expression data suggest that Ca R. santandreae largely provisions its host via outer-membrane vesicle secretion. With its high share of biomass in the symbiosis and large standing stocks of carbon and energy reserves, it has a unique role for bacterial symbionts-serving as the primary energy storage for its animal host.


chemoautotrophic; ecophysiology; endosymbiont; energy storage; host nutrition

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