Bacterial symbioses. Predation and mutually beneficial associations.

The endosymbiotic theory, which has proved to explain the origin of mitochondria and chloroplasts, also posits the origin of nucleus and other cellular organelles that could have derived from ancient relationships among bacteria. It seems that predation might have been a prerequisite to the establishment of symbiosis as a source of evolutionary novelty. This review describes current different examples of bacteria able not only to attack and degrade other bacteria, but also to establish stable symbiotic relationships with different eukaryotic organisms.     

The origin of the eukaryotic cell. II. A critical analysis of the symbiotic (exogenous) concept

The exogenous (symbiotic) conception of the eukaryotic cell origin is unable to explain satisfactory the structure of mitochondria and chloroplasts. Either of these organelles possess its genome that can be compared with the viral one rather than with the bacterial one, judging by the dimensions and quantity of coding genes. The mitochondria resemble a little prokaryotes in the number of their proteins, chemical composition of their inner membrane and peculiarities of the protein-synthesizing apparatus. The primitive structure of mt DNA, the lesser quantity and greater unspecifity of the mitochondrial tRNA prove, additionally, the non-bacterial origin of this organelles. The deflexion of the genetic code from the universal one in the mitochondrial nucleoids also testify in favour of this point of view. The results of micropaleontological and paleobiochemical investigations evidence towards initial ability of the primary eukaryotes (primary protists) to photosynthesis. In this case, they did not need to acquire plastids from outside by symbiotic way. The autogenous origin of the flagellum of the primary protists was reported earlier (Seravin, 1985). The accumulated data permit us to consider that the cell organelles formed endogenously in the process of evolution of the cell.     

Evolutionary origin of cell organelles]

A review on the evolutionary origin of the energy-yielding eukaryotic organelles is presented. Current autogenetic (endogenous compartmentalization) schemes, as well as different variants of symbiogenesis, are critically envisaged. A new symbiogenetic scheme is put forth, according to which mitochondria and chloroplasts originated divergently from a primordial photosynthetic organelle; the latter was acquired by endosymbiosis of ancient cyanobacteria in the cells of protoeukaryotes.     

The evolutionary origin of glycosomes

The glycolytic pathway of the Kinetoplastida is organized in a unique manner: the majority of its enzymes are contained in organelles called glycosomes. In this article Paul Michels and Fred Opperdoes argue that the glycosomes are equivalent to the microbodies and peroxisomes identified in other eukaryotic cells. They explore the possible evolutionary origin of the glycosome by comparing many of its structural and functional properties with those of other members of the microbody family and with some features of other organelles, the mitochondria and chloroplasts, which have been studied in much more detail.     

The origin of eukaryotic cells and origination of apoptosis

The unified conception of the origin of eukaryotic cells has been proposed. In the author's opinion, evolutionary transformation of prokaryotic cell into eukaryotic cell took place 3.3-1.4 billion years ago and involved the next four stages: 1) the appearance of intracellular membranes due to prokaryotic cell plasmalemma invaginating into its cytoplasm; 2) the cell nucleus formation by the double sheet of intracellular membrane surrounding and sequestrating genetic material of the cell; 3) the appearance of cytoskeleton in parallel with mitotic spindle formation and gradual transition from prokaryotic way of cell division to mitosis; 4) the establishment of symbiosis between the evolving nucleated cell and prokaryotic microorganicsms that subsequently transform into mitochondria and chloroplasts. Apoptosis of cells of the present day multicellular eukaryotic organisms is supposed to be an evolutionary altered response of mitochondrian predecessors to the influence of factors, which are able to damage eukaryotic host cell. The initial biological significance of this reaction pertained to attempts of endosymbionts to leave the host cell as soon as possible, if the probability of its irreversible injury was very high, and by this to escape from their death. It is possible that numerous proteins, known as sensors or transducers of proapoptotic signals in Bcl-2--p53-dependent apoptotic pathway, were initially encoded by mitochondrial genome, whereas antiapoptotic factors and also components of receptor-mediated and granzyme B perforin dependent apoptotic pathways have cellular origin.     

The number of symbiotic origins of organelles.

Mitochondria and chloroplasts both originated from bacterial endosymbionts. The available evidence strongly supports a single origin for mitochondria and only somewhat less strongly a single, slightly later, origin for chloroplasts. The arguments and evidence that have sometimes been presented in favor of the alternative theories of the multiple or polyphyletic origins of these two organelles are evaluated and the kinds of data that are needed to test more rigorously the monophyletic theory are discussed. Although chloroplasts probably originated only once, eukaryotic algae are polyphyletic because chloroplasts have been secondarily transferred to new lineages by the permanent incorporation of a photosynthetic eukaryotic algal cell into a phagotrophic protozoan host. How often this has happened is much less clear. It is particularly unclear whether or not the chloroplasts of typical dinoflagellates and euglenoids originated in this way from a eukaryotic symbiont: their direct divergence from the ancestral chloroplast cannot be ruled out and indeed has several arguments in its favor. The evidence for and against the view that the chloroplast of the kingdom Chromista was acquired in a single endosymbiotic event is discussed. The possibility that even the chloroplast of Chlorarachnion might have been acquired during the same symbiosis that created the cryptomonad cell, if the symbiont was a primitive alga that had chlorophyll a, b and c as well as phycobilins, is also considered. An alga with such a combination of pigments might have been ancestral to all eukaryote algae.     

Calcium regulation in endosymbiotic organelles of plants

In plant cells calcium-dependent signaling pathways are involved in a large array of biological processes in response to hormones, biotic/abiotic stress signals and a variety of developmental cues. This is generally achieved through binding of calcium to diverse calcium-sensing proteins, which subsequently control downstream events by activating or inhibiting biochemical reactions. Regulation by calcium is considered as a eukaryotic trait and has not been described for prokaryotes. Nevertheless, there is increasing evidence indicating that organelles of prokaryotic origin, such as chloroplasts and mitochondria, are integrated into the calcium-signaling network of the cell. An important transducer of calcium in these organelles appears to be calmodulin. In this review we want to give an overview over present data showing that endosymbiotic organelles harbour calcium-dependent biological processes with a focus on calmodulin-regulation.Key words: mitochondria, chloroplasts, calcium, calmodulin, EF-hand proteins     

Origin and evolution of the peroxisomal proteome

Background  

Peroxisomes are ubiquitous eukaryotic organelles involved in various oxidative reactions. Their enzymatic content varies between species, but the presence of common protein import and organelle biogenesis systems support a single evolutionary origin. The precise scenario for this origin remains however to be established. The ability of peroxisomes to divide and import proteins post-translationally, just like mitochondria and chloroplasts, supports an endosymbiotic origin. However, this view has been challenged by recent discoveries that mutant, peroxisome-less cells restore peroxisomes upon introduction of the wild-type gene, and that peroxisomes are formed from the Endoplasmic Reticulum. The lack of a peroxisomal genome precludes the use of classical analyses, as those performed with mitochondria or chloroplasts, to settle the debate. We therefore conducted large-scale phylogenetic analyses of the yeast and rat peroxisomal proteomes.     

Coordination of gene expression between organellar and nuclear genomes

Following the acquisition of chloroplasts and mitochondria by eukaryotic cells during endosymbiotic evolution, most of the genes in these organelles were either lost or transferred to the nucleus. Encoding organelle-destined proteins in the nucleus allows for host control of the organelle. In return, organelles send signals to the nucleus to coordinate nuclear and organellar activities. In photosynthetic eukaryotes, additional interactions exist between mitochondria and chloroplasts. Here we review recent advances in elucidating the intracellular signalling pathways that coordinate gene expression between organelles and the nucleus, with a focus on photosynthetic plants.     

The origin of the eukaryotic cell. III. Principles of the morphofunctional organization of the eukaryotic cell

The eukaryotic plasmalemma, eukaryotic cytoplasm with its usual cytomembranes, and eukaryotic nucleus are obligatory components of the eukaryotic cell. All other structural elements (organelles) are only derivates of the aforesaid cell components and they may be absent sometimes. There are protozoans having simultaneously no flagelles, mitochondria and chloroplasts (all the representatives of phylum Microspora, amoeba Pelomyxa palustris, and others). The following five general principles play the main role in the morphofunctional organization of the cell. The principle of hierarchy of block organization of living systems. Complex morphofunctional blocks (organelles) specific for the eukaryotic cell are formed. The compartmentalization principle. The main cell organelles (nuclei, flagellae, mitochondria, chloroplasts, etc.) undergo a relative morphological isolation from each other and other cell organelles by means of the total or partial surrounding by membranes; this may ensure the originality of their evolution and function. The principle of poly- and oligomerization of morphofunctional blocks. It permits the cell to enlarge its sizes and to raise the level of integration. The principle of heterochrony, including three subprinciples: conservatism of useful signs; a strong acceleration of evolutionary development of the separate blocks; simplification of the structure, reduction or total disappearance of some blocks. It explains a preservation of prokaryotic signs in the eukaryotic cell or in its organelles. The principle of independent origin of similar morphofunctional blocks in the process of evolution of living systems. The parallelism of the signs in unrelated groups of cells (or protists) arises due to this principle.     

Endosymbiosis,cell evolution,and speciation

In 1905, the Russian biologist C. Mereschkowsky postulated that plastids (e.g., chloroplasts) are the evolutionary descendants of endosymbiotic cyanobacteria-like organisms. In 1927, I. Wallin explicitly postulated that mitochondria likewise evolved from once free-living bacteria. Here, we summarize the history of these endosymbiotic concepts to their modern-day derivative, the “serial endosymbiosis theory”, which collectively expound on the origin of eukaryotic cell organelles (plastids, mitochondria) and subsequent endosymbiotic events. Additionally, we review recent hypotheses about the origin of the nucleus. Model systems for the study of “endosymbiosis in action” are also described, and the hypothesis that symbiogenesis may contribute to the generation of new species is critically assessed with special reference to the secondary and tertiary endosymbiosis (macroevolution) of unicellular eukaryotic algae.     

Intracellular compartmentation of CTP synthase in Drosophila

Compartmentation is essential for the localization of biological processes within a eukaryotic cell.ATP synthase localizes to organelles such as mitochondria and chloroplasts.By contrast,little is known about the subcellular distribution of CTP synthase,the critical enzyme in the production of CTP,a high-energy molecule similar to ATP.Here I describe the identification of a novel intracellular structure con-taining CTP synthase,termed the cytoophidium,in Drosophila cells.I find that cytoophidia are present ...     

Evidence for the symbiotic origin of mitochondria

There are numerous characteristics in which mitochondria resemble bacteria and differ from the enveloping eukaryotic cell. These similarities and differences have been offered in support of the symbiotic origin of mitochondria. Such evidence, no matter how striking, can be faulted as representing retained primitive genome if the characteristics being compared evolved prior to the divergence of protoeukaryotes from prokaryotes. In contrast, if a characteristic evolved after this evolutionary divergence, in response to a relatively recent environmental change, it could serve as a clear marker of the symbiotic event. The enzyme superoxide dismutase, which serves as a defense against oxygen toxicity, need not have existed prior to the accumulation of photosynthetic oxygen. It probably evolved after the appearance of blue-green algae and it was apparently evolved independently by prokaryotes and by protoeukaryotes. The superoxide dismutases found in prokaryotes and in mitochondria are remarkably similar in gross properties and in amino acid sequence; whereas the corresponding enzyme of the eukaryotic cytoplasm is entirely different. This represents support for the symbiotic origin of mitochondria which is not easily argued away.     

Metabolic symbiosis at the origin of eukaryotes

Thirty years after Margulis revived the endosymbiosis theory for the origin of mitochondria and chloroplasts, two novel symbiosis hypotheses for the origin of eukaryotes have been put forward. Both propose that eukaryotes arose through metabolic symbiosis (syntrophy) between eubacteria and methanogenic Archaea. They also propose that this was mediated by interspecies hydrogen transfer and that, initially, mitochondria were anaerobic. These hypotheses explain the mosaic character of eukaryotes (i.e. an archaeal-like genetic machinery and a eubacterial-like metabolism), as well as distinct eukaryotic characteristics (which are proposed to be products of symbiosis). Combined data from comparative genomics, microbial ecology and the fossil record should help to test their validity.     

An overview of endosymbiotic models for the origins of eukaryotes, their ATP-producing organelles (mitochondria and hydrogenosomes), and their heterotrophic lifestyle.

The evolutionary processes underlying the differentness of prokaryotic and eukaryotic cells and the origin of the latter's organelles are still poorly understood. For about 100 years, the principle of endosymbiosis has figured into thoughts as to how these processes might have occurred. A number of models that have been discussed in the literature and that are designed to explain this difference are summarized. The evolutionary histories of the enzymes of anaerobic energy metabolism (oxygen-independent ATP synthesis) in the three basic types of heterotrophic eukaryotes those that lack organelles of ATP synthesis, those that possess mitochondria and those that possess hydrogenosomes--play an important role in this issue. Traditional endosymbiotic models generally do not address the origin of the heterotrophic lifestyle and anaerobic energy metabolism in eukaryotes. Rather they take it as a given, a direct inheritance from the host that acquired mitochondria. Traditional models are contrasted to an alternative endosymbiotic model (the hydrogen hypothesis), which addresses the origin of heterotrophy and the origin of compartmentalized energy metabolism in eukaryotes.     

From nuclear genes to chloroplast localized proteins

There is broad evidence that an endosymbiotic uptake of a cyanobacterial-type organism was the point of origin for the evolution of chloroplasts. During organelle evolution extensive gene transfer from the symbiont to the host genome occurred, which raises the question of how these gene products, namely proteins, which are still functional in chloroplasts, find their way back ‘home’. Nuclear-encoded proteins enter plastids via a complex import machinery that requires the coordinate interplay of a variety of soluble and membrane-bound factors on the cytosolic site as well as on the stromal side of the chloroplast envelope membranes. We define that the process called ‘import of chloroplast precursor proteins’ begins with the release of the polypeptide from the ribosomes and binding to cytosolic factors, such as a guidance complex, which accompanies (chaperones) proteins to chloroplasts. The translocation across the envelope membranes engages distinct translocation machineries at the outer and the inner envelope membranes. Additionally subsequent sorting events to different subcompartments within the plastids are operated by a number of distinct pathways, all of which seem to involve multiple subunits, which are largely of bacterial (symbiotic) origin. The evolutionary history of proteins mediating the import of chloroplast constituents across the envelope membranes seems more diverse. Since cyanobacteria lack a protein import pathway, it is not surprising that only a few subunits of the chloroplast translocon seem to be of symbiotic origin while others seem to be eukaryotic additions.     

Endosymbiosis and the design of eukaryotic electron transport

The bioenergetic organelles of eukaryotic cells, mitochondria and chloroplasts, are derived from endosymbiotic bacteria. Their electron transport chains (ETCs) resemble those of free-living bacteria, but were tailored for energy transformation within the host cell. Parallel evolutionary processes in mitochondria and chloroplasts include reductive as well as expansive events: On one hand, bacterial complexes were lost in eukaryotes with a concomitant loss of metabolic flexibility. On the other hand, new subunits have been added to the remaining bacterial complexes, new complexes have been introduced, and elaborate folding patterns of the thylakoid and mitochondrial inner membranes have emerged. Some bacterial pathways were reinvented independently by eukaryotes, such as parallel routes for quinol oxidation or the use of various anaerobic electron acceptors. Multicellular organization and ontogenetic cycles in eukaryotes gave rise to further modifications of the bioenergetic organelles. Besides mitochondria and chloroplasts, eukaryotes have ETCs in other membranes, such as the plasma membrane (PM) redox system, or the cytochrome P450 (CYP) system. These systems have fewer complexes and simpler branching patterns than those in energy-transforming organelles, and they are often adapted to non-bioenergetic functions such as detoxification or cellular defense.     

From extracellular to intracellular: the establishment of mitochondria and chloroplasts.

Paracoccus and Rhodopseudomonas are unusual among bacteria in having a majority of the biochemical features of mitochondria; blue-green algae have many of the features of chloroplasts. The theory of serial endosymbiosis proposes that a primitive eukaryote successively took up bacteria and blue-green algae to yield mitochondria and chloroplasts respectively. Possible characteristics of transitional forms are indicated both by the primitive amoeba, Pelomyxa, which lacks mitochondria but contains a permanent population of endosymbiotic bacteria, and by several anomalous eukaryotic algae, e.g. Cyanophora, which contain cyanelles instead of chloroplasts. Blue-green algae appear to be obvious precursors of red algal chloroplasts but the ancestry of other chloroplasts is less certain, though the epizoic symbiont, Prochloron, may resemble the ancestral green algal chloroplast. We speculate that the chloroplasts of the remaining algae may have been a eukaryotic origin. The evolution or organelles from endosymbiotic precursors would involve their integration with the host cell biochemically, structurally and numerically.     

Genetic-evolutionary basis of symbiosis doctrine

The author presents the current notion of symbiosis as one of the main adaptation of an organism to changeable environment. Symbiosis is considered as a super organism genetic system within which there are different interactions (including mutualism and antagonism). Genetic integration of symbiotic partners can be realized as cross regulation of their genes, exchange of gene products (proteins, RNA), gene amplification and sometimes gene transfer between organisms. On the phenotypic level these processes result in signal interactions, integration of partner metabolic systems and development of symbiotic organs. Co-evolution is considered as an assemblage of micro- and macroevolution processes basing on pre-adaptations and proceeding under influence of different forms of natural selection (individual, frequency-depended and kin selection). Symbiosis can be compared with sexual process since both are the forms of organism integration characterized by different genetic mechanisms and evolutionary consequences. The genome evolution in symbiotic microorganisms can proceed by: 1) simplification of genome in obligate symbiosis (loss of genes that are necessary for independent existence, transfer of some genes to the host organism); 2) complication of genome in facultative symbiosis (increase in genome plasticity, structural and functional differentiation of genome into systems controlling free-living and symbiotic parts of life cycle). Most of symbiotic interactions are correlated to an increase in genetic plasticity of an organism that can lead to evolutionary saltations and origin of new forms of life.