Photophysiology of kleptoplasts: photosynthetic use of light by chloroplasts living in animal cells

Abstract

Kleptoplasty is a remarkable type of photosynthetic association, resulting from the maintenance of functional chloroplasts—the ‘kleptoplasts’—in the tissues of a non-photosynthetic host. It represents a biologically unique condition for chloroplast and photosynthesis functioning, occurring in different phylogenetic lineages, namely dinoflagellates, ciliates, foraminiferans and, most interestingly, a single taxon of metazoans, the sacoglossan sea slugs. In the case of sea slugs, chloroplasts from macroalgae are often maintained as intracellular organelles in cells of these marine gastropods, structurally intact and photosynthetically competent for extended periods of time. Kleptoplasty has long attracted interest owing to the longevity of functional kleptoplasts in the absence of the original algal nucleus and the limited number of proteins encoded by the chloroplast genome. This review updates the state-of-the-art on kleptoplast photophysiology, focusing on the comparative analysis of the responses to light of the chloroplasts when in their original, macroalgal cells, and when sequestered in animal cells and functioning as kleptoplasts. It covers fundamental but ecologically relevant aspects of kleptoplast light responses, such as the occurrence of photoacclimation in hospite , operation of photoprotective processes and susceptibility to photoinhibition. Emphasis is given to host-mediated processes unique to kleptoplastic associations, reviewing current hypotheses on behavioural photoprotection and host-mediated enhancement of photosynthetic performance, and identifying current gaps in sacoglossan kleptoplast photophysiology research.

Photoprotective Non-photochemical Quenching Does Not Prevent Kleptoplasts From Net Photoinactivation

“…Understanding the basics of kleptoplast photophysiology is thus necessary to find factors that might be beneficial for an autonomous functioning of the photosynthetic apparatus (Handrich et al, 2017). Therefore, photoprotection mechanisms might be important to reduce PSII photoinactivation (Serôdio et al, 2014;Christa et al, 2017) and an active repair of damaged D1 would ensure continuing PSII activity (de Vries et al, 2013).…”

The Transition from Glycogen to Starch Metabolism in Cyanobacteria and Eukaryotes

“…During these tertiary endosymbiosis, heterotrophic dinoflagellate phagotrophs themselves resulting most probably from secondary endosymbiosis, followed by plastid loss, or loss of photosynthesis, or both, have acquired plastids from other primary or secondary eukaryotic algae, leading to an astonishing diversity of plastids (for a review of dinoflagellate evolution, see (Wisecaver and Hackett 2011)). To further complicate the issues, both dinoflagellates and ciliates are able to transiently steal and benefit from plastids or algae ingested by phagocytosis, a phenomenon known as kleptoplasty (Serodio et al 2014). In all alveolates, storage polysaccharides are found in the cytosol in the form of either glycogen found in majority of ciliates or of starch found in most dinoflagellates and apicomplexa.…”

The extraordinary longevity of kleptoplasts derived from the Ross Sea haptophyte Phaeocystis antarctica within dinoflagellate host cells relates to the diminished role of the oxygen-evolving Photosystem II and to supplementary light harvesting by mycosporine-like amino acid/s

“…In addition, functional algal chloroplasts exist symbiotically in the cytoplasm of some protozoans (ciliates, foraminifera, dinoflagellates) and of a single taxon of metazoans (sacoglossan sea slugs) that feed on unicellular algae [1]. The process of engulfing algae and using their chloroplasts for photosynthesis by non-photosynthetic host cells has been termed kleptoplasty [2]. It is a remarkable type of symbiotic association, involving the maintenance of the chloroplasts-the 'kleptoplasts'-in a functional state within a non-photosynthetic host cell.…”