Demonstration of nucleomorph-encoded eukaryotic small subunit ribosomal RNA in cryptomonads

Abstract

In cryptomonads, unicellular phototrophic flagellates, the plastid(s) is (are) located in a special narrow compartment which is bordered by two membranes; it harbours neither mitochondria nor Golgi dictyosomes but comprises eukaryotic ribosomes and starch grains together with a small organelle called the nucleomorph. The nucleomorph contains DNA and is surrounded by a double membrane with pores. It is thought to be the vestigial nucleus of a phototrophic eukaryotic endosymbiont. Cryptomonads are therefore supposed to represent an intermediate state in the evolution of complex plastids from endosymbionts. We have succeeded in isolating pure nucleomorph fractions, and can thus provide, using pulsed field gel electrophoresis, polymerase chain reaction and sequence analysis, definitive proof for the eukaryotic nature of the symbiont and its phylogenetic origin.

Goniomonas: rRNA sequences indicate that this phagotrophic flagellate is a close relative of the host component of cryptomonads

“…When plastid-containing cryptomonads were used in similar PCRs, two nuclear-type srRNA gene products were recovered (Douglas et al, 1991b;McFadden et al, 1994). One product is from the host nuclear srRNA genes, while the other is from the endosymbiont nucleomorph genome (Douglas et al, 1991b;Maier et al, 1991;McFadden et al, 1994). Previous electron microscopy analyses found no trace of any endosymbiont in Goniomonas (Kugrens & Lee, 1991), and the PCR analysis undertaken here indicates that no endosymbiont srRNA genes are present in Goniomonas.…”

“…A biflagellate host harbours a photosynthetic endosymbiont (Maier et al, 1991;Douglas et al, 1991b). Although much reduced, the eukaryotic endosymbiont retains its nucleus and cytoplasm (McFadden et aL, 1994).…”

“…The endosymbiont nucleus, known as the nucleomorph (Greenwood, 1974), encodes rRNAs (Douglas et aL, 1991b;Maier et aI., 1991) which are apparently incorporated into ribosomes in the endosymbiont cytoplasm (McFadden et al, 1994). Genes for both the endosymbiont and host rRNAs have been cloned and sequenced (Maier et al, i991;Douglas et al, 1991b), and the sequences have been added to the eukaryotic phylogenetic tree to identify the evolutionary relationships of the two components making up cryptomonads (Maier et aL, 1991;Douglas et al, 1991b). These trees suggest that the endosymbiont is most closely related to extant red algae, which is also consistent with the presence of phycobilin pigments and the site of starch storage in the endosymbionts and red algae (see McFadden, 1993, for review).…”

“…Phylogenetic trees group the cryptomonad hosts with the rhizopods Acant hamoeba and Hartmanella (Maier et aL, 1991;Douglas et aI., 1991b). However, cryptomonads and rhizopods share few morphological features.…”

Organisation of the plastid genome from the rhodophyteChondrus crispus(Gigartinales); sequence and phylogeny of the 16S rRNA gene

“…It has been shown that the cryptophyte algae arose when a eukaryotic protist engulfed a eukaryotic alga related to red algae which became an endosymbiont Maier et al, 1991). An ancestral rhodophyte also seems to be the origin of heterokont plastids and it has * Author to contact regarding correspondence and offprints.…”