Facultative mutualism between Paramecium and the intracellular Rickettsiales bacterium Megaera mediated by a horizontally acquired biotin operon

Abstract The Rickettsiales are an alphaproteobacterial lineage engaging in ancient associations with a variety of eukaryotic hosts and with a wide spectrum of effects. They include vector-borne pathogens, as well as Wolbachia, which ranges from a reproductive manipulator to a mutualist in arthropods and nematodes. The majority of Rickettsiales are associated with aquatic protists, but these interactions are poorly understood. Here, we explored by dual RNA-Seq the effect of the host-generalist Rickettsiales bacterium Megaera polyxenophila on the protist Paramecium primaurelia. Megaera induces substantial changes in host gene expression, in particular, increased expression levels of certain cell replication–related functions, consistent with the higher growth observed in previous experiments. Conversely, the co-occurring reduction of catabolism and energy metabolism can be explained by the capability of the bacterium to efficiently exert the same pathways also for the host’s benefit. Therefore, Megaera likely behaves as a facultative mutualist, consistent with its predicted ability to provide the host with Adenosine triphosphate (ATP) and biotin, the latter synthesized, thanks to a recently horizontally acquired operon. At the same time, this bacterium expresses several genes involved in host cell invasion and possibly toxicity. Accordingly, it is envisioned that the overall effect of Megaera on its host is rather plastic, being the fine-tuned sum of supportive and parasitic actions, likely resulting in flexibility according to host and symbiont genotypes and environmental conditions, and subjected to evolutionary changes. Such flexibility may also explain the broad host range of Megaera and, from a more general perspective, hints for shared traits and analogies among other protist-associated Rickettsiales.