Evolution and physiology of the Paracatenula symbiosis

This thesis focuses on the symbiosis between the marine flatworm host Paracatenula, which lacks mouth and digestive system, and the alphaproteobacterial symbiont Candidatus Riegeria. Both host and symbiont are unique partners across all known symbioses - no other flatworm besides Paracatenula hosts chemosynthetic symbionts, and Ca. Riegeria is the only known chemosynthetic symbiont within the Alphaproteobacteria. Contained in specialized cells within the trophosome of Paracatenula, the Ca. Riegeria symbionts can comprise up to a half of the total host volume, representing the highest ratio of symbiont-to-host biomass among animal-bacteria symbioses. Ca. Riegeria have been transmitted vertically between host generations for at least 500 million years, leading to the presumption that their genomes contain signatures of reductive genome evolution. Yet only little is known about the genetic repertoire of Ca. Riegeria, their ecophysiology and how reductive genome evolution progressed over their evolutionary history. I have characterized key aspects of the Paracatenula symbiosis emphasizing the physiology of Ca. Riegeria and how it compares to "typical" gammaproteobacterial chemoautotrophs (I). I described the consequences of reductive genome evolution on retained functions and the underlying processes (II). I investigated the role of the symbionts in tissue regeneration as Paracatenula have an enormous regenerative capacity (III). Overall, I demonstrate that Paracatenula and Ca. Riegeria share an intimate biological connection that has been shaped over their long evolutionary history.