The Evolutionary Fate of Mitochondrial Aminoacyl-tRNA Synthetases in Amitochondrial Organisms

During the endosymbiotic evolution of mitochondria, the genes for aminoacyl-tRNA synthetases were transferred to the ancestral nucleus. A further reduction of mitochondrial function resulted in mitochondrion-related organisms (MRO) with a loss of the organelle genome. The fate of the now redundant ancestral mitochondrial aminoacyl-tRNA synthetase genes is uncertain. The derived protein sequence for arginyl-tRNA synthetase from thirty mitosomal organisms have been classified as originating from the ancestral nuclear or mitochondrial gene and compared to the identity element at position 20 of the cognate tRNA that distinguishes the two enzyme forms. The evolutionary choice between loss and retention of the ancestral mitochondrial gene for arginyl-tRNA synthetase reflects the coevolution of arginyl-tRNA synthetase and tRNA identity elements.

Biological lipid nanotubes and their potential role in evolution

The membrane of cells and organelles are highly deformable fluid interfaces, and can take on a multitude of shapes. One distinctive and particularly interesting property of biological membranes is their ability to from long and uniform nanotubes. These nanoconduits are surprisingly omnipresent in all domains of life, from archaea, bacteria, to plants and mammals. Some of these tubes have been known for a century, while others were only recently discovered. Their designations are different in different branches of biology, e.g. they are called stromule in plants and tunneling nanotubes in mammals. The mechanical transformation of flat membranes to tubes involves typically a combination of membrane anchoring and external forces, leading to a pulling action that results in very rapid membrane nanotube formation – micrometer long tubes can form in a matter of seconds. Their radius is set by a mechanical balance of tension and bending forces. There also exists a large class of membrane nanotubes that form due to curvature inducing molecules. It seems plausible that nanotube formation and functionality in plants and animals may have been inherited from their bacterial ancestors during endosymbiotic evolution. Here we attempt to connect observations of nanotubes in different branches of biology, and outline their similarities and differences with the aim of providing a perspective on their joint functions and evolutionary origin.

Changes in the transcriptome, ploidy, and optimal light intensity of a cryptomonad upon integration into a kleptoplastic dinoflagellate

Endosymbiosis of unicellular eukaryotic algae into previously nonphotosynthetic eukaryotes has established chloroplasts in several eukaryotic lineages. In addition, certain unicellular organisms in several different lineages ingest algae and utilize them as temporal chloroplasts (kleptoplasts) for weeks to months before digesting them. Among these organisms, the dinoflagellate Nusuttodinium aeruginosum ingests the cryptomonad Chroomonas sp. and enlarges the kleptoplast with the aid of the cryptomonad nucleus. To understand how the cryptomonad nucleus is remodeled in the dinoflagellate, here we examined changes in the transcriptome and ploidy of the ingested nucleus. We show that, after ingestion, genes involved in metabolism, translation, and DNA replication are upregulated while those involved in sensory systems and cell motility are downregulated. In the dinoflagellate cell, the cryptomonad nucleus undergoes polyploidization that correlates with an increase in the mRNA levels of upregulated genes. In addition, the ingested nucleus almost loses transcriptional responses to light. Because polyploidization and loss of transcriptional regulation are also known to have occurred during the establishment of endosymbiotic organelles, these changes are probably a common trend in endosymbiotic evolution. Furthermore, we show that the kleptoplast and dinoflagellate are more susceptible to high light than the free-living cryptomonad but that the ingested nucleus reduces this damage.

Large DNA virus promoted the endosymbiotic evolution to make a photosynthetic eukaryote

Chloroplasts in photosynthetic eukaryotes originated from a cyanobacterial endosymbiosis far more than 1 billion years ago1-3. Due to this ancientness, it remains unclear how this evolutionary process proceeded. To unveil this mystery, we analysed the whole genome sequence of a photosynthetic rhizarian amoeba4, Paulinella micropora5,6, which has a chloroplast-like organelle that originated from another cyanobacterial endosymbiosis7-10 about 0.1 billion years ago11. Here we show that the predacious amoeba that engulfed cyanobacteria evolved into a photosynthetic organism very quickly in the evolutionary time scale, probably aided by the drastic genome reorganization activated by large DNA virus. In the endosymbiotic evolution of eukaryotic cells, gene transfer from the endosymbiont genome to the host nucleus is essential for the evolving host cell to control the endosymbiont-derived organelle12. In P. micropora, we found that the gene transfer from the free-living and endosymbiotic bacteria to the amoeba nucleus was rapidly activated but both simultaneously ceased within the initiation period of the endosymbiotic evolution, suggesting that the genome reorganization drastically proceeded and completed. During this period, large DNA virus appeared to have infected the amoeba, followed by the rapid amplification and diversification of virus-related genes. These findings led us to re-examine the conventional endosymbiotic evolutionary scenario that exclusively deals with the host and the symbiont, and to extend it by incorporating a third critical player, large DNA virus, which activates the drastic gene transfer and genome reorganization between them. This Paulinella version of the evolutionary hypothesis deserves further testing of its generality in evolutionary systems and could shed light on the unknown roles of large DNA viruses13 in the evolution of terrestrial life.

Endosymbiotic Evolution of Algae, Secondary Heterotrophy and Parasitism

Photosynthesis is a biochemical process essential for life, serving as the ultimate source of chemical energy for phototrophic and heterotrophic life forms. Since the machinery of the photosynthetic electron transport chain is quite complex and is unlikely to have evolved multiple independent times, it is believed that this machinery has been transferred to diverse eukaryotic organisms by endosymbiotic events involving a eukaryotic host and a phototrophic endosymbiont. Thus, photoautotrophy, as a benefit, is transmitted through the evolution of plastids. However, many eukaryotes became secondarily heterotrophic, reverting to hetero-osmotrophy, phagotrophy, or parasitism. Here, I briefly review the constructive evolution of plastid endosymbioses and the consequential switch to reductive evolution involving losses of photosynthesis and plastids and the evolution of parasitism from a photosynthetic ancestor.

Multi-functional roles for the polypeptide transport associated domains of Toc75 in chloroplast protein import

Toc75 plays a central role in chloroplast biogenesis in plants as the membrane channel of the protein import translocon at the outer envelope of chloroplasts (TOC). Toc75 is a member of the Omp85 family of bacterial and organellar membrane insertases, characterized by N-terminal POTRA (polypeptide-transport associated) domains and C-terminal membrane-integrated β-barrels. We demonstrate that the Toc75 POTRA domains are essential for protein import and contribute to interactions with TOC receptors, thereby coupling preprotein recognition at the chloroplast surface with membrane translocation. The POTRA domains also interact with preproteins and mediate the recruitment of molecular chaperones in the intermembrane space to facilitate membrane transport. Our studies are consistent with the multi-functional roles of POTRA domains observed in other Omp85 family members and demonstrate that the domains of Toc75 have evolved unique properties specific to the acquisition of protein import during endosymbiotic evolution of the TOC system in plastids.