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A critique on the endosymbiotic theory for the origin of mitochondria
by Mike Gene
The following essay was written by Albert de Roos and the views/arguments contained within do not necessarily reflect the views of Mike Gene. Mike Gene hosts such essays simply to provoke thought and promote discussion and communication.

The endosymbiotic theory for the origin of mitochondria claims that our mitochondria were derived from an engulfed bacterium that was enslaved to become the current powerhouse of most eukaryotic cells. This endosymbiotic theory has become consensus among evolutionary biologists to such an extent that it is considered a fact and forms the basis for most research on molecular evolution. In fact, a falsification of the endosymbiotic theory would shake the scientific world and would have to lead to the reinterpretation of virtually all phylogenetic data. I argue that the mechanistic basis of the endosymbiotic theory is not sound and even contradictive to our current concepts of evolution. Therefore, there seems to be no reason to consider the endosymbiotic theory a fact.

All evolutionary theories must offer an explanation in mechanistic terms of how it should or could have happened in order to be tested. The difficult thing with the endosymbiotic theory is that it proposes no real mechanism and most textbooks show the simplistic picture of a cell that swallows another cell that becomes a mitochondrion. Unfortunately, it is not so simple as that. There is a difference between the process of endosymbiosis and its incorporation in the germline, necessitating genetic changes. What were those changes? What was the host? Was it a fusion, was it engulfment, how did the mitochondrion get its second membrane, how did two genomes in one cell integrate and coordinate? The theory is also strongly teleological, illustrated by the widely used term "˜enslavement'. But how do you enslave another cell, how do you replace its proteins and genes without affecting existing functions? The existence of obligate bacterial endosymbionts in some present eukaryotes is often presented as a substitute for a mechanism, but they remain bacteria and give not rise to new organelles. So, before we can speak of the endosymbiotic as a testable scientific theory, we need a mechanistic scenario which is lacking at the moment.

When we do try to envision a mechanistic scenario based on the endosymbiotic theory, we quickly run into problems. Genetic mutations that allow bacteria to thrive in the cytoplasm would not be strategic for survival. Anaerobic cells normally do not survive in environment that contains oxygen, while the endosymbiont would need oxygen in order to present fitness advantage. The two organisms would initially compete for energy sources since bacteria are users of ATP and do not export it. The extensive gene transfer that is needed in the endosymbiotic theory would wreak havoc in a complex genome since frequent insertion of random pieces of mitochondrial DNA would disrupt existing functions. Furthermore, gene transfer is a multi-step process were genes need to be moved to the nucleus, the different genetic code of mitochondria needs to be circumvented, the genes need to be expressed correctly, as well as imported back into the mitochondria in order to be functional. All in all, mechanistic scenarios for the endosymbiotic theory imply many non-functional intermediates or would just be plain harmful to an organism. Therefore, the endosymbiotic theory is in contrast with the concept of gradualism that forms the basis of modern evolutionary theory.

Let's have a look at the evidence that is presented in favor of the endosymbiotic theory. An important part of the evidence consists of similarities between bacteria and mitochondria, although is quite evident that the differences are enormous. Most pictures in textbooks of mitochondria resemble bacteria, but in reality, mitochondria form a dynamic network of interconnecting tubules (reticulum). The bacteria-like EM images of mitochondria that we know from textbooks are really cross-sections of tubules and a closer look reveals connections between the endomembrane system and mitochondria. Moreover, its organization is tightly linked to the cell cycle and is currently under complete eukaryotic control with most genes residing in the nucleus. In some textbooks the Lamarckian acquisition of a double membrane of mitochondria is even presented as evidence for engulfment. It is said that mitochondria, like bacteria, divide by fission, but the mechanisms are completely different and mitochondria use mainly components of unique eukaryotic origin. The use of circular DNA in mitochondria has been taken as evidence, but there are also many organisms that have linear mitochondrial chromosomes with eukaryotic telomeres. So, although we see some characteristics that are shared between mitochondria and bacteria, we see many more examples where mitochondria are actually quite different.

It is also claimed that phylogenetic evidence firmly supports the endosymbiotic theory, for instance by showing relatedness between mitochondria and specific groups of bacteria. Some mitochondrial proteins show indeed a similarity with specific bacterial proteins, both at the structural and at the gene level. However, this does not show that mitochondria are derived from bacteria, but only that these proteins have a common descent. Next to an origin from bacteria, it can also be that these related proteins descended from a common ancestor, that only the genes were transferred or that bacteria picked up the genes from either the nucleus or the mitochondria. In general, large mitochondrial genomes contain a mix of presumed eukaryotic, archaeal and eubacterial genes, in contrast to what you expect if mitochondria are of eubacterial origin. Furthermore, a priori assumptions in phylogenetic analyses, such as long-branch attraction can bias phylogenetic tree analysis. This is illustrated by the amitochondriate organisms that can be either placed ancestral in the eukaryotic tree or derived, depending on whether you assume they once possessed mitochondria or not. Thus, as long as we do not have a clear picture of the last common ancestor and its relationship with eukaryotes, it will be difficult to interpret gene similarity as evidence for the endosymbiotic theory.

There are alternative explanations for the origin of mitochondria that can compete with the endosymbiotic theory and that are in line with the phylogenetic data. In an autogenic origin, mitochondria are evolutionary derived from the eukaryotic endomembrane system. Its evolution can be driven by the advantages to sequester metabolic activity in specialized compartments. As extensions to existing functionality, the targeting and import mechanisms could be developed gradually and based on existing eukaryotic functions, for instance already existing ER or organelle targeting. The acquisition of DNA would enable the metabolic vesicles to become relatively independent by expressing proteins that cannot be imported through normal organelle targeting or that facilitate mitochondrial functions. The mitochondrial genes could be derived from transposable elements, plastids or viruses and could come from either the nuclear genome or a bacterial genome. The components of the essential ATP-generating cascades suggest a gradual evolution based on expanding on an existing proton motive force coupled to ATP generation. Intermediates exist in the form of hydrogenosomes and mitosomes from amitochondriate primitive eukaryotes. Thus, we do have an alternative hypothesis that defines a gradual mechanism that includes intermediates fitness advantages for these steps, in line with Darwinian theory.

In order for an evolutionary theory to be considered a scientific fact or a valid scientific theory, there are some basic requirements. First, it is necessary to have a reasonably detailed mechanism that explains the basic steps in the endosymbiotic scenario. Second, this mechanism should be placed in the context of current Darwinian evolutionary theory and should contain no fundamental problems or falsifications. Third, a substantial body of empirical evidence that directly supports this scenario should be present. Fourth, no credible or logically sound alternatives should exist. If these criteria are not met, the endosymbiotic theory cannot be considered to be a scientific fact that has been proven beyond reasonable doubt. Remarkably, the endosymbiotic theory fails all points.
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  1. I agree with Albert de Roos that there is no proof for the endosybiotic theory, and that it is more likely that organelles were created locally.

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