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

Abstract

The enigmatic association of photosynthetically active chloroplasts from algae and some sacoglossan sea slugs, called functional kleptoplasty, is a functional unique system of photosymbioses observed in metazoans. Besides the specific adaptations of the slugs necessary to incorporate and maintain the plastids, the organelles need to ensure optimal photosynthesis. Photoprotective mechanisms in the plastids, namely the xanthophyll cycle (XC) and the high-energy dependent quenching (q E ) part of the non-photochemical quenching (NPQ), and the repair of the D1 protein of Photosystem II (PSII) are considered crucial for kleptoplast longevity in the slugs. Here, we studied the sea slugs Elysia viridis fed with the naturally occurring XC and q E -deficient Bryopsis hypnoides, and E. timida fed on Acetabularia acetabulum, an alga that possesses both mechanisms. The aim of the study was to understand (i) whether q E remains active after ingestion of kleptoplasts by E. timida, (ii) how different light intensities affect the photosynthetic activity of kleptoplasts with and without photoprotection mechanisms, and (iii) if the kleptoplasts are able to repair photodamaged D1 protein. With regard to NPQ, freshly incorporated kleptoplasts responded to different light stress in the same manner as the chloroplasts in their native host algae. Even after 3 weeks of incorporation the q E part of NPQ was present in the kleptoplasts of E. timida. However, the presence of the q E component of NPQ did not prevent the kleptoplasts from significant PSII photoinactivation under high light intensities. This is probably due to the fact that the kleptoplasts have a reduced PSII repair capacity, despite plastid encoded repair mechanisms in every sacoglossan food source. Hence, photoprotective mechanisms are probably not a key factor explaining kleptoplast longevity in Sacoglossa sea slugs.

The photon menace: kleptoplast protection in the photosynthetic sea slugElysia timida

“…These results indicate that the efficiency of photoprotection via the Vx cycle decreased as kleptoplasts aged with animal starvation, indicating that the kleptoplasts lose the capacity for physiological photoprotection and suggesting that Vx-cycle enzymes are nuclear encoded in A. acetabulum, as already reported for other green algae (Zorin et al, 2017). Our results contradict recent findings by Christa et al (2018) reporting an equally active photoprotective component of NPQ (qE) in kleptoplasts of E. timida during starvation. These authors further argue that NPQ does not protect the kleptoplasts from net photoinactivation because E. timida and E. viridis showed comparable decreases in length and F v /F m when starved for 21 days under continuous high light.…”

“…More recently, de Vries et al (2013) hypothesized that the plastid-encoded FTSH, a D1 quality control protease that is essential for PSII repair, could rescue kleptoplasts from photodamage in photosynthetic sea slugs. More recently, Christa et al (2018) estimated the rate constant of PSII inactivation (k PI ) in kleptoplasts of E. viridis and E. timida and concluded that kleptoplasts have a reduced PSII repair capacity when compared with chloroplasts in their natural host algae.…”

Photosynthetic sea slugs induce protective changes to the light reactions of the chloroplasts they steal from algae

“…,H). Similar data has previously been presented from E. timida and also E. chlorotica(Cruz et al, 2015;Christa et al, 2018). Higher level of NPQ in the slugs is likely linked to the strong acidification of the lumen in the slugs (Figure 4A), since the major qE component of NPQ is pH dependent(Müller et al, 2001; Papageorgiou and Govindjee, 2014).The xanthophyll cycle of freshly fed E. timida is functional(Cartaxana et al, 2019), but it is unclear whether the NPQ induced already during the first 100 s of the RLC measurement (Figure 5G) is due to lumen acidification switching on the xanthophyll cycle, or whether lumen acidification directly enhances quenching capacity at the level of light harvesting antennae.…”

“…Unlike higher plants ( Järvi et al, 2015 ), the chloroplast genomes of all algal species involved in long-term kleptoplasty encode FtsH, a protease involved in PSII repair cycle ( de Vries et al, 2013 ). However, out of all prey algae species of photosynthetic sea slugs, only in Vaucheria litorea , the prey alga of Elysia chlorotica , the chloroplast-encoded FtsH contains the critical M41 metalloprotease domain required for degradation of the D1 protein during PSII repair ( Christa et al, 2018 ). Photoinhibition of Photosystem I (PSI) occurs especially during rapid changes in light intensity ( Tikkanen and Grebe, 2018 ) and should cause problems in isolated chloroplasts in the long run.…”

“…Recent efforts have advanced our understanding of photoprotection in kleptoplasts ( Christa et al, 2018 ; Cartaxana et al, 2019 ). It has been shown that kleptoplasts of E. timida do retain the capacity to induce physiological photoprotection mechanisms similar to the ones in the prey green alga Acetabularia acetabulum (hereafter Acetabularia ) ( Christa et al, 2018 ). The most studied mechanism is the ‘energy-dependent’ qE component of non-photochemical quenching of excitation energy (NPQ).…”