Diversity of Organellar Genomes in Non-photosynthetic Diatoms.

We determined the complete sequences of the plastid and mitochondrial genomes of three non-photosynthetic Nitzschia spp., as well as those of a photosynthetic close relative, Nitzschia palea. All the plastid genomes and the three mitochondrial genomes determined were found to be circularly mapping, and the other mitochondrial genomes were predicted to be of a linear form with telomere-like structures at both ends. We found that all the non-photosynthetic plastid genomes are streamlined and lack a common gene set: two RNA genes, and 60 protein-coding genes, most of which are related to photosynthetic functions. Nevertheless, the non-photosynthetic plastid genomes commonly retain ATP synthase complex genes, although atpE is missing in Nitzschia sp. NIES-3581 and three other non-photosynthetic species lack atpF instead of atpE. This observation suggests an evolutionary constraint against the loss of ATP synthase complex genes. All the non-photosynthetic diatom plastid genomes lacked two genes, thiS and thiG, involved in thiamin biosynthesis. Consistent with this gene loss, non-photosynthetic Nitzschia spp. were incapable of thriving in vitamin B1-lacking media. This study clearly demonstrated not only the evolutionary trends of plastid genome reduction but also the linkage between plastid genome reduction and a biological change of nutrient requirements in Nitzschia.

Proposal of a Twin Arginine Translocator System-Mediated Constraint against Loss of ATP Synthase Genes from Nonphotosynthetic Plastid Genomes. [Corrected].

Organisms with nonphotosynthetic plastids often retain genomes; their gene contents provide clues as to the functions of these organelles. Yet the functional roles of some retained genes-such as those coding for ATP synthase-remain mysterious. In this study, we report the complete plastid genome and transcriptome data of a nonphotosynthetic diatom and propose that its ATP synthase genes may function in ATP hydrolysis to maintain a proton gradient between thylakoids and stroma, required by the twin arginine translocator (Tat) system for translocation of particular proteins into thylakoids. Given the correlated retention of ATP synthase genes and genes for the Tat system in distantly related nonphotosynthetic plastids, we suggest that this Tat-related role for ATP synthase was a key constraint during parallel loss of photosynthesis in multiple independent lineages of algae/plants.