The worm affair: fidelity and environmental adaptation in symbiont species that co-occur in vestimentiferan tubeworms

The symbioses between the vestimentiferan tubeworms and their chemosynthetic partners (Gammaproteobacteria, Chromatiales and Sedimenticolaceae) hallmark the success of these organisms in hydrothermal vent and hydrocarbon seep deep-sea habitats. The fidelity of these associations varies, as both the hosts and the symbionts can be loose in partner choice. Some tubeworms may host distinct symbiont phylotypes, which often co-occur in a single host individual. To better understand the genetic basis for the promiscuity of tubeworm symbioses, we assembled and investigated metagenome-assembled genomes of two symbiont phylotypes (species, based on the average nucleotide identity < 95%) in Lamellibrachia anaximandri, a vestimentiferan endemic to the Mediterranean Sea, in individuals collected from Palinuro hydrothermal vents (Italy) and hydrocarbon seeps (Eratosthenes seamount and Palmahim disturbance). Using comparative genomics, we show that mainly mobilome and genes involved in defence mechanisms distinguish the symbiont genotypes. While many central metabolic functions are conserved in the tubeworm symbionts, nitrate respiration (Nar, Nap and Nas proteins) is modular, yet this modularity is not linked to phylotype, but rather to geographic location, potentially implying adaptation to the local environment. Our results hint that variation in a single moonlighting protein may be responsible for the fidelity of these symbioses.