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

Abstract

Hosts of chemoautotrophic bacteria typically have much higher biomass than their symbionts and consume symbiont cells for nutrition. In contrast to this, chemoautotrophicCandidatusRiegeria symbionts in mouthlessParacatenulaflatworms comprise up to half of the biomass of the consortium. Each species ofParacatenulaharbors a specificCa. 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 ofParacatenulafrom 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 thatCa. 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.