High specificity meets genomic flexibility in the Siphamia - Photobacterium symbiosis

ABSTRACT Host-microbe symbioses must balance partner specificity with enough flexibility to remain adaptable to environmental change. The Siphamia - Photobacterium symbiosis exemplifies this balance, as tropical siphonfish ( Siphamia spp. ) form a highly specific association with the bioluminescent bacterium Photobacterium mandapamensis , though it is unknown whether this specificity extends to temperate species of siphonfish. Here, we use long-read genome sequencing and functional assays to characterize the strain-level diversity of symbionts isolated from two temperate siphonfish hosts, Siphamia cephalotes and Siphamia roseigaster , and compare them to tropical isolates. We found that both hosts exclusively associate with P. mandapamensis in their light organs and that temperate strains form host-specific clades despite being collected in close proximity (< 5km). This is consistent with selective host filtering, microhabitat-driven adaptation, or conspecific host seeding. Pangenome analyses showed notable differences in accessory gene content, variation in the lux - rib operon, and a dramatic expansion of mobile genetic element (MGE) content in a subset of strains. We also identified the first host-derived P. mandapamensis isolate that is non-luminescent under laboratory conditions despite an intact lux - rib operon. Luminescence varied across strains, salinities, and temperature but was not correlated with the presence of luxF , with the majority of high-MGE strains exhibiting reduced light output. Together, these results extend the specificity of the Siphamia - Photobacterium symbiosis into temperate hosts and show that animals can maintain tight symbiont specificity despite the symbiont harboring substantial genomic and phenotypic flexibility at the strain level.