SYMBIOSIS

Symbiotic associations between organisms, even of different kingdoms, is not that unusual.  However, in almost all cases they represent an association between two intact, free-living organisms, both of which have retained their complete cellular genetic make-up.  Such associations are typically intercellular and, if intracellular, the symbiont is frequently isolated from the host’s cytosol by sequestration in a vacuole or host-provided membrane.  What makes the sea slug/algal chloroplast symbiosis so remarkable is that the symbiont is a “naked,” foreign organelle sustained intracellularly in direct contact with the host sea slug cytosol and the symbiont remains functional for several months despite the absence of any algal nucleo-cytosolic influence. There is some disagreement on whether an association between an organism and an isolated organelle such as a chloroplast constitutes symbiosis since the symbiont (chloroplast) is not a free-living organism.  The term symbiosis was first defined as, “unlike organisms” living together.  “Unlike organisms” came to mean different species and symbiosis changed to reflect, “prolonged physical associations without respect to outcome.”  In the early 1900's, the Russian scientist K.S. Mereschkovsky proposed that chloroplasts originated from blue-green algae (cyanobacteria), a process he named symbiogenesis or “the origin of evolutionary novelty via symbiosis.” In 1975, Robert Trench defined intracellular symbiosis as, “the coexistence of at least two genomes of divergent evolutionary origins occupying the same cytoplasmic environment.”   In her book on “Symbiotic Interactions,” Angela Douglas (1994) emphasizes that symbiosis is not dependent on mutual benefit to the partners, rather that at least one of the partners acquires a new metabolic property.  Considering both Trench’s and Douglas’ definitions, we conclude that the intracellular association of algal chloroplasts with molluscan cells can be considered a unique symbiotic association.  The chloroplast represents a symbiont genome and the host mollusc acquires a new metabolic capability, photosynthesis.  Still, others prefer to use the term kleptoplasty or “something borrowed” to describe the chloroplast symbiosis.  Regardless of definition or term used, today it is universally recognized that great biological novelty and diversity come from symbiotic associations and symbiosis is a widespread biological phenomenon.

PRIMARY, SECONDARY AND TERTIARY ENDOSYMBIOSIS
The endosymbiotic events leading to a solar-powered sea slug.
The endosymbiont theory traces the origin of the chloroplast to a free-living cyanobacterium that was engulfed by a eukaryote giving rise to the primary lineages of glaucophytes, red algae (rhodophytes), and the green plants and algae (the viridiplantae or streptophytes and chlorophytes, respectively). Subsequently, secondary endosymbiosis, the uptake of a eukaryotic alga (green or red lineage) by another heterotrophic eukaryotic host, gave rise to a diverse group of secondary or complex algae, including the heterokont Vaucheria litorea. Tertiary symbiosis is most commonly associated with dinoflagellates and the replacement of their endosymbiont with a new secondary endosymbiont. Here, we propose that the engulfment of secondary chloroplasts by a sea slug also represents a tertiary endosymbiotic association.