The nudibranch Berghia stephanieae (Valdés, 2005) is not able to initiate a functional symbiosome-like environment to maintain Breviolum minutum (J.E.Parkinson & LaJeunesse 2018)

Abstract

Photosymbiosis is found in different animal lineages and is best understood in cnidarians. A successful initiation and maintenance of the symbiosis between the animal hosts and the photosymbiotic partners is based on a recognition by specific host receptors. This triggers signaling cascades that promote the photobiont tolerance by the host, including an interpartner nutrient exchange and the ability of the host to cope with increased levels of reactive oxygen species (ROS) generated by the photobiont. Key to the successful symbiosis is the inhibition of the phagosomal maturation resulting in the formation of the symbiosome. In animals other than cnidarians, little is known about the photosymbiosis initiation and maintenance, for instance in sea slugs belonging to the Nudibranchia. Here, we investigated the gene expression profile of Berghia stephanieae, which is able to incorporate Breviolum minutum from its cnidarian prey Exaiptasia diaphana (Rapp, 1829) but is not able to maintain the algae for more than a couple of days during starvation. We show that the recognition of the algae is based on similar mechanisms present in cnidarians, and we identified some additional candidate genes that might be molluscan specific for photobiont recognition. Downstream, B. stephanieae responds to increased levels of ROS but is not able to stop the phagosomal maturation or decrease the immune response against B. minutum, which seem to be the key factors missing in B. stephanieae that accounts for the unstable symbiosis in this slug. Hence, B. stephanieae can be considered a transitional state toward a stable photosymbiosis and can help to elucidate general aspects of the evolutionary processes involved in establishing photosymbioses in animals.

A chromosome-level genome for the nudibranch gastropodBerghia stephanieaehelps parse clade-specific gene expression in novel and conserved phenotypes

“…Berghia stephanieae (hereafter referred to as Berghia ) is a species of gastropod in the order Nudibranchia, a clade of marine slugs that lose their shell during metamorphosis [33]. This species has been used as a model for the study of both more conserved systems, such as neurodevelopment [34] and reproductive development [35], as well as clade-restricted phenotypes such as the sequestration of cnidarian nematocysts [36, 37] and endosymbiosis [38, 39]. We combined an inferred proteome from Berghia with available genome and transcriptome data from other metazoan species – including mollusks such as cephalopods, bivalves, and other gastropods – to identify clade-specific Berghia genes (i.e., restricted to Mollusca, Gastropoda, Heterobranchia, Nudibranchia, Aeolidina, or Berghia alone).…”

The highly developed symbiotic system between the solar-powered nudibranch Pteraeolidia semperi and Symbiodiniacean algae

“… 16 The striking resemblance between intracellular symbiosis in nudibranchs and corals underscores the potential value of employing nudibranchs as model organisms for investigating the mechanisms underlying coral–algal symbiosis. 17 , 18 Nonetheless, to date, only 2 molecular studies 19 , 20 have been conducted on this subject, leaving much to be uncovered about the symbiotic mechanism. Furthermore, the nudibranch Berghia stephanieae , which was employed in these investigations, is considered to possess a rudimentary symbiotic capacity.…”

The highly developed symbiotic system between the solar-powered nudibranchPteraeolidia semperiand Symbiodiniacean algae

“…16 The striking resemblance between intracellular symbiosis in nudibranchs and corals underscores the potential value of employing nudibranchs as model organisms for investigating the mechanisms underlying coralalgal symbiosis. 17,18 Nonetheless, to date, only 2 molecular studies 19,20 have been conducted on this subject, leaving much to be uncovered about the symbiotic mechanism. Furthermore, the nudibranch Berghia stephanieae, which was employed in these investigations, is considered to possess a rudimentary symbiotic capacity.…”