A cryptic plastid and a novel mitochondrial plasmid inLeucomyxa plasmidiferagen. and sp. nov. (Ochrophyta) push the frontiers of organellar biology

Abstract

Numerous lineages of heterotrophs evolved from photosynthetic eukaryotic ancestors and usually have retained a plastid, although cases of secondary plastid loss are known, too. Based on a previous investigation by transmission electron microscopy (TEM), Leukarachnion sp. PRA-24, an amoeboid colourless protist related to the photosynthetic class Synchromophyceae within the algal phylum Ochrophyta, is a candidate for another case of a plastid loss. Here we provide a detailed characterisation of this organism and formally describe it as Leukarachnion salinum, sp. nov. While we could not find any unambiguous candidate for a plastid organelle by TEM, genome sequencing recovered a complete plastid genome with a reduced gene set similar to plastid genomes of other non-photosynthetic ochrophytes yet even more extreme in the sequence divergence. The presence in the L. salinum transcriptome assembly of homologs of hallmark plastid proteins, including components of the plastid protein import complexes, supported the notion that L. salinum has a cryptic plastid organelle. Based on an analysis of plastid-targeting signals in L. salinum proteins, the plastid presumably contains a unique combination of biosynthetic pathways producing haem, the folate precursor aminodeoxychorismate, and, surprisingly, tocotrienols. Our work thus uncovers the existence of a novel form of a relict plastid organelle.