Evolution and theft: loss of state transitions in Bryopsidales macroalgae and photosynthetic sea slugs

Abstract

Green macroalgae within the order Bryopsidales lack the fundamental photoprotective mechanisms of green algae, the xanthophyll cycle and energy-dependent dissipation of excess light. Here, by measuring chlorophyll fluorescence at 77K after specific light treatments, we show that Bryopsidales algae also lack state transitions, another ubiquitous photoprotection mechanism present in other green algae. Certain Sacoglossa sea slugs can feed on Ulvophyceae algae, including some Bryopsidales, and steal chloroplasts -kleptoplasts- that remain functional inside the animal cells for months without the support of the algal nucleus. Our data reveal that the state transition capacity is not retained in the kleptoplasts of the sea slugs, and we provide evidence that the loss is caused by structural changes during their incorporation by the animals. This enforced chloroplast sphericity was observed in all studied kleptoplastic associations, and we propose that it is a fundamental property supporting long-term retention of kleptoplasts in photosynthetic sea slugs.