Is ftsH the Key to Plastid Longevity in Sacoglossan Slugs?

Abstract

Plastids sequestered by sacoglossan sea slugs have long been a puzzle. Some sacoglossans feed on siphonaceous algae and can retain the plastids in the cytosol of their digestive gland cells. There, the stolen plastids (kleptoplasts) can remain photosynthetically active in some cases for months. Kleptoplast longevity itself challenges current paradigms concerning photosystem turnover, because kleptoplast photosystems remain active in the absence of nuclear algal genes. In higher plants, nuclear genes are essential for plastid maintenance, in particular, for the constant repair of the D1 protein of photosystem II. Lateral gene transfer was long suspected to underpin slug kleptoplast longevity, but recent transcriptomic and genomic analyses show that no algal nuclear genes are expressed from the slug nucleus. Kleptoplast genomes themselves, however, appear expressed in the sequestered state. Here we present sequence data for the chloroplast genome of Acetabularia acetabulum, the food source of the sacoglossan Elysia timida, which can maintain Acetabularia kleptoplasts in an active state for months. The data reveal what might be the key to sacoglossan kleptoplast longevity: plastids that remain photosynthetically active within slugs for periods of months share the property of encoding ftsH, a D1 quality control protease that is essential for photosystem II repair. In land plants, ftsH is always nuclear encoded, it was transferred to the nucleus from the plastid genome when Charophyta and Embryophyta split. A replenishable supply of ftsH could, in principle, rescue kleptoplasts from D1 photodamage, thereby influencing plastid longevity in sacoglossan slugs.

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).…”

“…A recent hypothesis suggests that the repair of damaged D1 might be key to kleptoplast longevity in sacoglossan sea slugs (de Vries et al, 2013), despite doubts based on photoinactivation under excessive light conditions that were previously raised (Vieira et al, 2009).…”

“…Once damaged, D1 needs to be pulled out from the reaction center and newly incorporated (Mulo et al, 2012). This so-called D1 turnover is crucial for photosynthetic organisms and largely nuclear controlled, although several tools, including psbA, tufA, and ftsH, are plastid encoded in the food sources of Sacoglossa (de Vries et al, 2013;Leliaert and Lopez-Bautista, 2015).…”

“…In particular FTSH, a quality control protease forming heteroor homo-oligomers (Janska et al, 2013) that removes damaged D1 from the PSII reaction center (Mulo et al, 2012), came into focus as a factor enabling kleptoplast longevity in Sacoglossa (de Vries et al, 2013). However, it is still unknown whether FTSH in kleptoplasts can function, because the M41 domain, needed for proteolysis of damaged D1 (Zhang et al, 2010), is missing in plastid encoded FTSH of the food source of one LtR Sacoglossa (de Vries et al, 2013).…”

“…However, it is still unknown whether FTSH in kleptoplasts can function, because the M41 domain, needed for proteolysis of damaged D1 (Zhang et al, 2010), is missing in plastid encoded FTSH of the food source of one LtR Sacoglossa (de Vries et al, 2013). But, for other food sources it was not yet analyzed if the M41 domain is also absent in plastid encoded FTSH.…”