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.

Endozoicomonadaceae bacteria are widespread in many marine animals, and generally considered beneficial. Members of one clade, however,CandidatusEndonucleobacter, infect the nuclei of deep-sea mussels, where they replicate to ≥ 80,000 bacteria per nucleus and cause the nuclei to swell to 50 times their original size. How these parasites are able to persist in host nuclei without the cell undergoing apoptosis is not known. We show here that Ca. Endonucleobacter encodes and expresses 7-15 inhibitors of apoptosis (IAPs), proteins previously only known from animals and viruses. Dual RNA-seq transcriptomes of infected nuclei revealed parallel upregulation ofCa.Endonucleobacter IAPs and host caspases, suggesting an arms race between the parasite and host for control of apoptosis. Comparative phylogenetic analyses revealed thatCa.Endonucleobacter acquired IAPs repeatedly through horizontal gene transfer from their hosts in convergent acquisition, possibly mediated by herpes viruses that may infect both the parasite and the host.