Why It Is Time to Look Beyond Algal Genes in Photosynthetic Slugs

Abstract

Eukaryotic organelles depend on nuclear genes to perpetuate their biochemical integrity. This is true for mitochondria in all eukaryotes and plastids in plants and algae. Then how do kleptoplasts, plastids that are sequestered by some sacoglossan sea slugs, survive in the animals’ digestive gland cells in the absence of the algal nucleus encoding the vast majority of organellar proteins? For almost two decades, lateral gene transfer (LGT) from algae to slugs appeared to offer a solution, but RNA-seq analysis, later supported by genome sequencing of slug DNA, failed to find any evidence for such LGT events. Yet, isolated reports continue to be published and are readily discussed by the popular press and social media, making the data on LGT and its support for kleptoplast longevity appear controversial. However, when we take a sober look at the methods used, we realize that caution is warranted in how the results are interpreted. There is no evidence that the evolution of kleptoplasty in sea slugs involves LGT events. Based on what we know about photosystem maintenance in embryophyte plastids, we assume kleptoplasts depend on nuclear genes. However, studies have shown that some isolated algal plastids are, by nature, more robust than those of land plants. The evolution of kleptoplasty in green sea slugs involves many promising and unexplored phenomena, but there is no evidence that any of these require the expression of slug genes of algal origin.

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

“…Clearly, there is no algal genomic support (Pelletreau et al, 2011;Wägele et al, 2011;Bhattacharya et al, 2013), neither through remnants of an algae nucleus nor through a eukaryotic horizontal gene transfer (Rauch et al, 2015). It is still unknown whether the slugs are able to actively support the kleptoplasts to stay functional.…”

“…The M41 domain is crucial for the functionality of FTSH, in which monomers are assembled into heterooligomers (Janska et al, 2013) and at least one monomer needs to have the M41 domain (Zhang et al, 2010). It is thus likely that, although cp encoded, FTSH is not functioning in kleptoplasts, because there is no evidence that algal, nuclear encoded counterparts containing a M41 domain are present in the slugs genome (Rauch et al, 2015). Hence, kleptoplasts would not be able to repair damaged D1.…”

Life Cycle Analysis of Endosymbiotic Algae in an Endosymbiotic Situation with Paramecium bursaria Using Capillary Flow Cytometry

“…Several ongoing plastid-acquisition types of endosymbiosis are observed in sacoglossan sea slugs such as Elysia chlorotica and E. timida [11,[35][36][37], and in the marine ciliate Mesodinium rubrum [38][39][40][41]. However, they are defective in their ability to maintain permanent endosymbiosis.…”

Ist die Schnecke, was sie isst?

“…Eine Gruppe deutscher und niederländischer Wissenschaftler, zu denen auch Wägele gehört, räumt nun in einer Gemeinschaftspublikation mit der Gentransfertheorie auf [8]. Die geringe Zahl nachgewiesener Algentranskripte bei Pierce et al sowie deren zu den entsprechenden Genen der Herkunftsalge identische Sequenz sprächen für eine Probenverunreinigung durch Nahrungsreste, da nach horizontalem Gentransfer üblicherweise eine Anpassung an den Codongebrauch des Empfängers erfolgt.…”

“…Laut Berechnungen der Forscher ist ein Anteil von 0,0001% an Algentranskripten 200.000fach zu niedrig, um Photosynthese zu ermöglichen, und liegt sogar noch unter dem Wert, der üblicherweise auf Verunreinigungen zurückzuführen ist. Auch Ergebnisse von DNA‐Hybridisierungsexperimenten zum Nachweis von Algen‐DNA im Schneckengenom [9] sind aufgrund fehlender Spezifitätskontrollen der Sonden nicht überzeugend, was die Forscher schließen lässt, dass die bisher publizierten Daten keine Hinweise auf eine Expression von Algengenen im Schneckengenom liefern [8].…”