Evolution of a non-mitochondrial eukaryotic organism

Since antiquity, the term "monad" (from Greek monos - unit, single) has been used to denote the fundamental and indivisible element. Francis Taylor in 1982 used this term in a general cytological sense to show the distinction between "monads" (proper cells) and "chimeras" (endosymbiotic systems). The cell-monad is the elementary unit of life and is characterized by a set of structures necessary for reproduction in ontogenesis: Cytoplasmic membrane, or membrane barrier, surrounding the cytoplasmic compartment; Genome or individual coding system based on compacted double-stranded DNA; Population of ribosomes, or universal translation organelles. All the above features are characteristic of mitochondria, endosymbiotic organelles of bacterial origin that function as the cell's "power plants". Endosymbiotic systems represent a fundamentally different type of intercellular association. In this case, a prokaryotic monad resides within a eukaryotic one, resulting in them becoming so interconnected that separate existence is impossible. This is the path by which mitochondria (descendants of chemotrophic prokaryotic monads) arose during evolution (Fig. 1). According to this hypothesis, some ancient cells engulfed others but did not digest them. The engulfed cells received permanent residence and stable conditions, but in return had to provide the host cell with necessary energy. As a result of studying the sequence of bases in mtDNA, evidence was obtained that mitochondria are descendants of aerobic bacteria, related to rickettsia, that once "learned" to live as symbionts in the ancestral eukaryotic cell. Now mitochondria are present in almost all eukaryotic cells; they are no longer capable of reproducing outside the cell. Initially, the endosymbiotic ancestors of mitochondria could neither import proteins nor export ATP. Presumably, they received pyruvate from the host cell, and the benefit for the host consisted in the neutralization of oxygen, which is toxic for the nucleocytoplasm, by aerobic symbionts [1,6].   [IMG_1]   Fig.1 Symbiotic theory of origin of mitochondria (and plastids) (after Margulis L., 1975) However, as discovered in May 2016, mitochondria and any mitochondrial genes associated with their function are not essential components of the eukaryotic cell. Scientists from the Czech Republic and Canada for the first time managed to identify and study a eukaryotic organism that secondarily lost mitochondria and all genes necessary for their functioning. This organism uses genes borrowed from bacteria during horizontal gene transfer (which demonstrates that eukaryotes are not as inaccessible to this process as previously thought), which allow obtaining energy through oxidation of substances in the cytoplasm. This refers to a representative of oxymonads - Monocercomonoides globus. The research results were published in Current Biology. Monocercomonoides is a genus of flagellated parasitic protozoa belonging to the order Oxymonadida. Monocercomonoides species were found in the intestines of small mammals, snakes, and insects and were described as the first eukaryotic organisms that lost mitochondria during the transition to anaerobic respiration and a parasitic lifestyle. They have an oval or pear-shaped form, length of 5-15 μm, 4 flagella gathered in pairs of two. They feed by pinocytosis. Overall, the Monocercomonoides genome has a size of 75 Mb and includes 16,629 protein-coding genes. The genome lacks mitochondrial (mtDNA) or any genes for cardiolipin synthesis. The representative Monocercomonoides sp. PA 203, which was isolated from the intestine of a chinchilla, acquired through horizontal gene transfer from bacteria the genes responsible for the cytosolic mobilization system of sulfur necessary for the construction of iron-sulfur clusters (Fig. 2a,b) [2].   [IMG_2]   [IMG_3]    Fig.2a Monocercomonoides (source)                                Fig.2b Monocercomonoides globus — 15 μm (source) It is known that mitochondria directly played a role in the evolution of eukaryotes, therefore the archaeal and symbiotic theories of mitochondrial origin should be revisited [3]. In the 1980s, there were many candidates for the title of modern archezoa, but in the following years, all of them were found to have organelles similar to mitochondria (mitosomes and peroxisomes) and marker genes of the mitochondrial past: genes for Fe-S protein assembly, mitochondrial transporters and chaperones, and cardiolipin synthetase. The genome of Monocercomonoides sp. contains 16,629 genes; the usual complex of genes associated with mitochondria in eukaryotes (in particular, genes of enzymes that carry out transport and sorting of peptides through mitochondrial membranes, the so-called "sorting and assembly machinery") was not found. There are also no genes for ATP membrane transporters, which are present in metamonads. In them, they pump ATP from hydrogenosomes and mitosomes outward. There were also no genes or proteins providing contact of the endoplasmic reticulum with mitochondria or their derivatives. How then do Monocercomonoides sp. obtain energy if they lack mitochondria? They have enzyme genes borrowed from bacteria that are responsible for metabolism. They obtain energy through anaerobic glycolysis - the decomposition of glucose under anaerobic conditions, then pyruvate to hydrogen or ethanol and acetic acid. They also have another, more efficient way of energy accumulation - the breakdown of the amino acid arginine directly in the cytoplasm (similarly to Giardia and trichomonads). Important for obtaining energy are electron conductors, the function of which is performed by iron-sulfur clusters (Fe—S clusters). They can participate in electron transfer due to mobile bonds. In eukaryotes, these clusters are localized in mitochondria or plastids. For energy synthesis, Monocercomonoides sp. use a bacterial set of enzymes, just like the close relative Paratrimastix pyriformis (Fig. 3).    [IMG_4]    Fig.3 Energy synthesis in organisms (source) At the top: a eukaryotic organism in which the Fe—S cluster assembly enzyme complex functions. Inside: anaerobic eukaryotic organisms with reduced mitochondria (hydrogenosomes, mitosomes), in which oxidative phosphorylation of glycolysis products is absent, Fe—S clusters are synthesized. At the bottom: replacement of the mitochondrial ISC complex with bacterial SUF (Sulfur mobilization) in mitochondria-lacking organisms, which is responsible for the production of iron-sulfur clusters. How then did mitochondria of metamonads evolve? (Fig. 4) Mitochondria can reduce to mitosomes or other similar organelles, but the Fe—S cluster assembly components (ISC) function in them. Ancestors of Monocercomonoides and Paratrimastix acquired the bacterial complex for Fe—S cluster synthesis (SUF), which allowed them to discard the ISC complex enzymes. In Monocercomonoides, mitosomes also disappear. In parallel, in other metamonads that did not receive an additional cytoplasmic complex for Fe—S cluster synthesis, mitosomes or their analogs with the original mitochondrial ISC complex remain.   [IMG_5]    Fig.4 Evolution of mitochondria of metamonads (source) The discoverers believe that Monocercomonoides had mitochondria in their evolutionary past. Evidence for this is the presence of mitosomes in the closely related species Paratrimastix pyriformis. Possibly, these protozoa have undetected mitosomes that have degraded so much that no traces of their presence remain in the genome. And successfully captured bacterial genes enable them to live anaerobically, or in an environment with low oxygen concentration in the presence of high concentrations of organic substances, iron, and sulfur [4]. References A.V. Pinevich. Microbiology. Biology of prokaryotes: Textbook in 3 volumes. Volume 1. - St. Petersburg: Publishing house of St. Petersburg University. -2006. - 352 p. http://eol.org/data_objects/27476785 http://biomolecula.ru/content/1955 Karnkowska et al. A Eukaryote without a Mitochondrial Organelle // Current Biology. – 2016. – 1-11 p. http://elementy.ru/novosti_nauki/432755/ I.O. Mazunin, Volodko N.V. Mitochondria: life in the cell and its consequences // Nature. No. 10. – 201. – 3 p.