A new guest to the blood feast: a novel symbiotic lineage associated with a haematophagous leech from the genusHaementeria

Abstract

ABSTRACTSimilarly to other strict blood-feeders, leeches from theHaementeriagenus (Hirudinida: Glossiphoniidae) have established a symbiotic association with bacteria harboured intracellularly in oesophageal bacteriomes. Previous genome sequence analyses of these endosymbionts revealed co-divergence with their hosts, a strong genome reduction, and a simplified metabolism largely dedicated to the production of B vitamins, which are nutrients lacking from a blood diet.CandidatusProvidencia siddallii has been identified as the obligate nutritional endosymbiont of a monophyletic clade of Mexican and South AmericanHaementeriaspp. Nonetheless, given a lack of molecular investigations, the identity of the symbiont housed in the bacteriomes of its sister clade of Central and South American congeners remained unknown. In this work, we report on a novel bacterial endosymbiont found in a representative from thisHaementeriaclade. We found that this symbiont lineage has evolved from within thePluralibactergenus, known mainly from clinical, but also environmental strains. Similarly toCa. Providencia siddallii, theHaementeria-associatedPluralibactersymbiont displays clear signs of genome reduction, accompanied by an A+T-biased sequence composition. Genomic analysis of its metabolic potential revealed a retention of pathways related to B vitamin biosynthesis, supporting its role as a nutritional endosymbiont. Finally, comparative genomics of bothHaementeriasymbiont lineages suggests that the ancientProvidenciasymbiont was likely replaced by the novelPluralibacterone, thus constituting the first reported case of nutritional symbiont replacement in a leech without morphological changes in the bacteriome.