Symbiotic organs shaped by distinct modes of genome evolution in cephalopods

Abstract

Microbes have been critical drivers of evolutionary innovation in animals. To understand the processes that influence the origin of specialized symbiotic organs, we report the sequencing and analysis of the genome ofEuprymna scolopes, a model cephalopod with richly characterized host–microbe interactions. We identified large-scale genomic reorganization shared betweenE. scolopesandOctopus bimaculoidesand posit that this reorganization has contributed to the evolution of cephalopod complexity. To reveal genomic signatures of host–symbiont interactions, we focused on two specialized organs ofE. scolopes: the light organ, which harbors a monoculture ofVibrio fischeri, and the accessory nidamental gland (ANG), a reproductive organ containing a bacterial consortium. Our findings suggest that the two symbiotic organs withinE. scolopesoriginated by different evolutionary mechanisms. Transcripts expressed in these microbe-associated tissues displayed their own unique signatures in both coding sequences and the surrounding regulatory regions. Compared with other tissues, the light organ showed an abundance of genes associated with immunity and mediating light, whereas the ANG was enriched in orphan genes known only fromE. scolopes. Together, these analyses provide evidence for different patterns of genomic evolution of symbiotic organs within a single host.