Engineering yeast endosymbionts as a step toward the evolution of mitochondria (original) (raw)
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Farming the mitochondrial ancestor as a model of endosymbiotic establishment by natural selection
Proceedings of the National Academy of Sciences of the United States of America, 2018
The origin of mitochondria was a major evolutionary transition leading to eukaryotes, and is a hotly debated issue. It is unknown whether mitochondria were acquired early or late, and whether it was captured via phagocytosis or syntrophic integration. We present dynamical models to directly simulate the emergence of mitochondria in an ecoevolutionary context. Our results show that regulated farming of prey bacteria and delayed digestion can facilitate the establishment of stable endosymbiosis if prey-rich and prey-poor periods alternate. Stable endosymbiosis emerges without assuming any initial metabolic benefit provided by the engulfed partner, in a wide range of parameters, despite that during good periods farming is costly. Our approach lends support to the appearance of mitochondria before any metabolic coupling has emerged, but after the evolution of primitive phagocytosis by the urkaryote.
Endosymbiosis before eukaryotes: mitochondrial establishment in protoeukaryotes
Cellular and Molecular Life Sciences
Endosymbiosis and organellogenesis are virtually unknown among prokaryotes. The single presumed example is the endosymbiogenetic origin of mitochondria, which is hidden behind the event horizon of the last eukaryotic common ancestor. While eukaryotes are monophyletic, it is unlikely that during billions of years, there were no other prokaryote–prokaryote endosymbioses as symbiosis is extremely common among prokaryotes, e.g., in biofilms. Therefore, it is even more precarious to draw conclusions about potentially existing (or once existing) prokaryotic endosymbioses based on a single example. It is yet unknown if the bacterial endosymbiont was captured by a prokaryote or by a (proto-)eukaryote, and if the process of internalization was parasitic infection, slow engulfment, or phagocytosis. In this review, we accordingly explore multiple mechanisms and processes that could drive the evolution of unicellular microbial symbioses with a special attention to prokaryote–prokaryote interact...
Evolution of Mitochondria Reconstructed from the Energy Metabolism of Living Bacteria
PLoS ONE, 2014
The ancestors of mitochondria, or proto-mitochondria, played a crucial role in the evolution of eukaryotic cells and derived from symbiotic a-proteobacteria which merged with other microorganisms-the basis of the widely accepted endosymbiotic theory. However, the identity and relatives of proto-mitochondria remain elusive. Here we show that methylotrophic a-proteobacteria could be the closest living models for mitochondrial ancestors. We reached this conclusion after reconstructing the possible evolutionary pathways of the bioenergy systems of proto-mitochondria with a genomic survey of extant a-proteobacteria. Results obtained with complementary molecular and genetic analyses of diverse bioenergetic proteins converge in indicating the pathway stemming from methylotrophic bacteria as the most probable route of mitochondrial evolution. Contrary to other a-proteobacteria, methylotrophs show transition forms for the bioenergetic systems analysed. Our approach of focusing on these bioenergetic systems overcomes the phylogenetic impasse that has previously complicated the search for mitochondrial ancestors. Moreover, our results provide a new perspective for experimentally re-evolving mitochondria from extant bacteria and in the future produce synthetic mitochondria.
Toward a Synthetic Yeast Endosymbiont with a Minimal Genome
Journal of the American Chemical Society, 2019
Based on the endosymbiotic theory, one of the key events that occurred during mitochondrial evolution was an extensive loss of non-essential genes from the protomitochondrial endosymbiont genome and transfer of some of the essential endosymbiont genes to the host nucleus. We have developed an approach to recapitulate various aspects of endosymbiont genome minimization using a synthetic system consisting of E. coli endosymbionts within host yeast cells. As a first step, we identified a number of E. coli auxotrophs of central metabolites that can form viable endosymbionts within yeast cells. These studies provide a platform to identify non-essential biosynthetic pathways that can be deleted in the E. coli endosymbionts to investigate the evolutionary adaptations in the host and endosymbiont during the evolution of mitochondria.
Late acquisition of mitochondria by a host with chimaeric prokaryotic ancestry
Nature, 2016
The origin of eukaryotes stands as a major conundrum in biology 1. Current evidence indicates that the Last Eukaryotic Common Ancestor (LECA) already possessed many eukaryotic hallmarks, including a complex subcellular organization 1-3. In addition, the lack of evolutionary intermediates challenges the elucidation of the relative order of emergence of eukaryotic traits. Mitochondria are ubiquitous organelles derived from an alpha-proteobacterial endosymbiont 4. Different hypotheses disagree on whether mitochondria were acquired early or late during eukaryogenesis 5. Similarly, the nature and complexity of the receiving host are debated, with models ranging from a simple prokaryotic host to an already complex proto-eukaryote 1,3,6,7. Most competing scenarios can be roughly grouped into either mito-early, which consider the driving force of eukaryogenesis to be mitochondrial endosymbiosis into a simple host, or mito-late, which postulate that a significant complexity predated mitochondrial endosymbiosis 3. Here we provide evidence for late mitochondrial endosymbiosis. We used phylogenomics to directly test whether proto-mitochondrial proteins were acquired earlier or later than other LECA proteins. We found that LECA protein families of alpha-proteobacterial ancestry and of mitochondrial localization show the shortest phylogenetic distances to their closest prokaryotic relatives, when compared to proteins of different prokaryotic origin or cellular localization. Altogether, our results shed new light on a long-standing question and provide compelling support for the late acquisition of mitochondria into a host that already had a proteome of chimeric phylogenetic origin. We argue that mitochondrial endosymbiosis was one of the ultimate steps in
Endosymbiont or host: who drove mitochondrial and plastid evolution?
Biology Direct, 2011
The recognition that mitochondria and plastids are derived from alphaproteobacterial and cyanobacterial endosymbionts, respectively, was one of the greatest advances in modern evolutionary biology. Researchers have yet however to provide detailed cell biological descriptions of how these once free-living prokaryotes were transformed into intracellular organelles. A key area of study in this realm is elucidating the evolution of the molecular machines that control organelle protein topogenesis. Alcock et al. (Science 2010, 327 [5966]:649-650) suggest that evolutionary innovations that established the mitochondrial protein sorting system were driven by the alphaproteobacterial endosymbiont (an "insiders' perspective"). In contrast, here we argue that evolution of mitochondrial and plastid topogenesis may better be understood as an outcome of selective pressures acting on host cell chromosomes (the "outsiders' view").
Journal of Theoretical Biology, 2007
The endosymbiosis of proto-mitochondrial prokaryotes (PMP) into proto-eukaryotic host-cells was a major advance in eukaryotic evolution. The nature of the initial relationship remains the subject of controversy. Various conceptual models have been proposed, but none has definitive support. We construct a model of inter-species interactions based upon well-established respiratory pathways, describing the respective energy gain of host-cell and PMP resulting from varying levels of cooperation. The model demonstrates conflicting evolutionary strategies (''Prisoner's Dilemmas'') in the interspecies molecular transfers. Nevertheless, we show that coercion and iterated, multilevel selection on both species encourage endosymbiosis. Mutualism is favored if host-cells are significantly more effective than PMPs at gathering food. Otherwise, an unambiguous asymmetry between host-cell and PMP benefits implies that the initial relationship consisted of the host-cell deriving a reproductive advantage at the PMPs' expense-a cellular version of farming. Other initial relationships such as oxygen-detoxification mutualism and parasitism are not strongly supported by the model. We compare the model behavior with experiments on mutant human mitochondria and find the model predicts proliferation rates consistent with that data. We derive from the evolutionary dynamics counter-intuitive therapeutic targets for two human hereditary mitochondrial disorders that reflect the ongoing effect of short-term selection at the mitochondrial level. r
Diversity and reductive evolution of mitochondria among microbial eukaryotes
2010
All extant eukaryotes are now considered to possess mitochondria in one form or another. Many parasites or anaerobic protists have highly reduced versions of mitochondria, which have generally lost their genome and the capacity to generate ATP through oxidative phosphorylation. These organelles have been called hydrogenosomes, when they make hydrogen, or remnant mitochondria or mitosomes when their functions were cryptic. More recently, organelles with features blurring the distinction between mitochondria, hydrogenosomes and mitosomes have been identified. These organelles have retained a mitochondrial genome and include the mitochondrial-like organelle of Blastocystis and the hydrogenosome of the anaerobic ciliate Nyctotherus. Studying eukaryotic diversity from the perspective of their mitochondrial variants has yielded important insights into eukaryote molecular cell biology and evolution. These investigations are contributing to understanding the essential functions of mitochondria, defined in the broadest sense, and the limits to which reductive evolution can proceed while maintaining a viable organelle.
Biological organisms have taken part in a journey that has lasted the better part of the last few million years. The organisms we know today -including ourselves -are just a speck on the timeline of all evolutionary history. The origins of every mammal, bird, fish, and reptile is a subject of fascination for all in the scientific world. The two classes of cells which make up organisms are prokaryotic and eukaryotic cells. Endosymbiont Theory, first proposed by Konstantin Mereschkowski, states that the eukaryotic cells we find in ourselves today began from prokaryotes, originating from a moment of symbiosis which took place between "separate, single-celled organisms" around 1.2-1.5 billion years ago. (Waseemuddin, 2016) This paper will explore the evidence which substantiates Mereschkowski's theory and look at the counter theory of Symbiogenesis.
Proceedings of the National Academy of Sciences, 2012
The controlled biogenesis of mitochondria is a key cellular system coordinated with the cell division cycle, and major efforts in systems biology currently are directed toward understanding of the control points at which this coordination is achieved. Here we present insights into the function, evolution, and regulation of mitochondrial biogenesis through the study of the protein import machinery in the human fungal pathogen, Candida albicans. Features that distinguish C. albicans from baker's yeast (Saccharomyces cerevisiae) include the stringency of metabolic control at the level of oxygen consumption, the potential for ATP exchange through the porin in the outer membrane, and components and domains in the sorting and assembling machinery complex, a molecular machine that drives the assembly of proteins in the outer mitochondrial membrane. Analysis of targeting sequences and assays of mitochondrial protein import show that components of the electron transport chain are imported by distinct pathways in C. albicans and S. cerevisiae, representing an evolutionary rewiring of mitochondrial import pathways. We suggest that studies using this pathogen as a model system for mitochondrial biogenesis will greatly enhance our knowledge of how mitochondria are made and controlled through the course of the cell-division cycle.