Solar-powered Sea Slugs - tertiary endosymbiosis?

Dear Sam,
When I suddenly get 5 or 6 messages all asking much the same question, I think it is fair to suspect that a teacher has asked a class to answer a question. So this answer is for all of your class mates as well.

The ability of some animals, such as solar-powered sea slugs to remove functioning plastids from plants and keep them alive in their own bodies [sacoglossans] or to keep whole plant cells alive in their bodies [nudibranchs], is fascinating for many reasons and is fertile ground for opisthobranch workers, physiologists, botanists, geneticists etc. I think it will be many years before we can say just how the symbiosis works. I think Kerry Clark coined the term kleptoplasty, or at least popularised it, for the phenomenon of 'stealing' plastids. It is from the same Ancient Greek word which gives us the word kleptomania - [compulsive stealing] an affliction which seems to infect American filmstars with monotonous regularity.

And now to your question about whether this is a tertiary symbiosis. I guess we have to define what a plastid is and what its origin is. This is, I am afraid, getting a little outside my field of expertise. What I can say is that you should have a look at some of Lynn Margulis's publications. I have a very thumbed copy of her 1981 book Symbiosis in Cell Evolution but I am sure you can find more up to date editions to have a look at. She clearly stated the hypothesis that eucaryotic cells evolved from bacteral ancestors by a series of symbioses. Many cell organelles are considered to be symbiotic organisms which 'invaded' protoorganisms in the early stages of the evolution of life on this planet. Plastids, like mitochondria, have their own genome, and at cell division act as though they are symbionts. I don't know if we gain much in our understanding of their biology by trying to number their 'grade' of symbiosis.

As I said above, their are two types of 'solar powered slugs. If we first consider the sacoglossans. In plants, the plastids could be considered primary symbionts. When they are removed by sacoglossans to their own cells, the plastids still occupy the same position in relation to the cell, as a primary symbiont. However if we look at the plastid in the sacoglossan we could say that this is its second primary symbiosis.

If we look at the solar-powered nudibranchs, the situation is a bit more complex. They remove whole single-celled plants [zooxanthellae] from the primary host (usually a cnidarian) and re-use them in their own tissue. In this case the plastid is a symbiont of the zooxanthella which is the symbiont of an animal. I guess you could call this a secondary symbiosis but it all becomes quite confusing if you want to record that it has been moved from its first host to a second host. In fact I once described the removal of zooxanthellae from cnidarians to nudibranchs as a 'secondary symbiosis' but I was describing the transfer of the zooxanthella from its primary host to a secondary host. You, on the other hand, are trying to number how many steps we can go back until we get to the first symbiont. I think its all a bit confusing and doesn't really enlighten us very much.

• Margulis, L. 1981. Symbiosis in Cell Evolution W.H.Freeman & Co.: San Francisco. 1-419.

I hope my answer is not too confusing,
Best wishes,
Bill Rudman