Ciliates are common carriers of cytoplasmic bacteria, however little is known about the molecular basis of the symbiotic relationships with their host. Working on interbreeding bipolar (Arctic and Antarctic) populations of the ciliate Euplotes nobilii, members of these populations were found to stably host Parafrancisella γ-proteobacteria. These bacteria (originally isolated from an Antarctic population of another Euplotes species, E. petzi) are phylogenetically related to pathogenic Francisella species which are well known for their capacity to colonize eukaryotic cells, causing animal diseases known as francisellosis. The finding that Parafrancisella/Euplotes associations are common in polar marine environments suggested that both microbial partners benefit from their stable partnership. To inquire into mutual advantages, we carried out a genomic analysis of E. nobilii and its Parafrancisella symbionts. In the E. nobilii genome, no gene was detected encoding methionine sulfoxide reductase of type A (MsrA), an enzyme which is essential to face damages from oxidative stress imposed by the high (saturated) oxygen concentrations of the polar sea waters. At the same time, the Parafrancisella genome revealed genes encoding MsrA sequences endowed with a N-terminal signal peptide for the secretion into the host’s cytoplasm, and the effectiveness of this secretion was further supported by the identification of a complete gene set coding for the so-called ‘Type VI Secretion System’ that many Gram-negative bacteria use to transfer their proteins into target cells. On the other side, in the Parafrancisella genome no gene encoding enzymes involved in the biosynthetic pathways of cysteine, lysine, methionine, and threonine was detected, implying that Parafrancisella cells rely on their E. nobilii host to obtain these four essential amino acids