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

MPG-Autoren
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Jäckle,  Oliver
Department of Symbiosis, Max Planck Institute for Marine Microbiology, Max Planck Society;

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Seah,  Brandon K. B.
Department of Symbiosis, Max Planck Institute for Marine Microbiology, Max Planck Society;

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Tietjen,  Malin
Department of Symbiosis, Max Planck Institute for Marine Microbiology, Max Planck Society;

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Leisch,  Nikolaus
Department of Symbiosis, Max Planck Institute for Marine Microbiology, Max Planck Society;

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Liebeke,  Manuel
Department of Symbiosis, Max Planck Institute for Marine Microbiology, Max Planck Society;

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Berg,  Jasmine S.
Department of Biogeochemistry, Max Planck Institute for Marine Microbiology, Max Planck Society;

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Gruber-Vodicka,  Harald R.
Department of Symbiosis, Max Planck Institute for Marine Microbiology, Max Planck Society;

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Zitation

Jäckle, O., Seah, B. K. B., Tietjen, M., Leisch, N., Liebeke, M., Kleiner, M., et al. (2019). Chemosynthetic symbiont with a drastically reduced genome serves as primary energy storage in the marine flatworm Paracatenula. Proceedings of the National Academy of Sciences of the United States of America, 116(17), 8505-8514. doi:10.1073/pnas.1818995116.


Zitierlink: https://hdl.handle.net/21.11116/0000-0005-B7F3-A
Zusammenfassung
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 symbionts 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.