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

Abstract

Absorption of excessive light by photosymbiotic organisms leads to the production of reactive oxygen species that can damage both symbiont and host. This is highly relevant in sacoglossan sea slugs that host functional chloroplasts 'stolen' from their algal foods (kleptoplasts), because of limited repair capacities resulting from the absence of algal nuclear genes. Here, we experimentally demonstrate (i) a hostmediated photoprotection mechanism in the photosynthetic sea slug Elysia timida, characterized by the closure of the parapodia under high irradiance and the reduction of kleptoplast light exposure; and (ii) the activation of a reversible xanthophyll cycle in kleptoplasts, which allows excessive energy to be dissipated. The described mechanisms reduce photoinactivation under high irradiance. We conclude that both hostmediated behavioural and plastid-based physiological photoprotective mechanisms can mitigate oxidative stress induced by high light in E. timida. These mechanisms may play an important role in the establishment of long-term photosynthetically active kleptoplasts.

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

“…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. Nevertheless, strong NPQ has obvious benefits for chloroplast longevity in E. timida.Flavodiiron proteins function as alternative electron sinks in E. timida and Acetabularia E. timida and Acetabularia utilize oxygen-dependent electron acceptors of PSI during dark-to-light transition, but their functionality is weaker in E. timida (Figure 4B-C).…”

“…Photoprotective mechanisms counteract photodamage. 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 xanthophyll cycle enhances qE ( Ruban and Horton, 1999 ; Papageorgiou GC, 2014 ) but there have been contrasting reports on the capability of E. timida to maintain a highly functional xanthophyll cycle if the slugs are not fed with fresh algae (i.e. starved) and about the effect of NPQ on kleptoplast longevity ( Christa et al, 2018 ; Cartaxana et al, 2019 ). Although advancing our understanding of the mechanisms of kleptoplast longevity, these recent publications underline the trend of contradictory results that has been going on for a long time.…”

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

“…41 3 Photoprotective mechanisms counteract photodamage. Recent efforts have advanced our 42 understanding of photoprotection in kleptoplasts (Christa et al, 2018;Cartaxana et al, 2019). It has 43 been shown that kleptoplasts of E. timida do retain the capacity to induce physiological photoprotection 44 mechanisms similar to the ones in the prey green alga Acetabularia acetabulum (hereafter Acetabularia) 45 (Christa et al, 2018).…”

On the art of stealing chloroplasts

“…The most obvious threat for these ‘solar-powered’ sea slugs are reactive oxygen species (ROS), which are formed by the addition of electrons to oxygen: these reactive molecules can severely damage tissues and eventually cause cell death ( Dorrell and Howe, 2012 ). Complex compounds that block oxidation (the loss of electrons) and mechanisms for dissipating excessive energy have both been proposed to play a protective role in kleptoplast-bearing sea slugs ( Cartaxana et al, 2019 ; Torres et al, 2020 ). However, despite over 50 years of research, it is still unclear how kleptoplasts are maintained in animal cells.…”