Hydrogen hypothesis

Abstract: 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.

Abstract: Published data suggest that hydrogenosomes, organelles found in diverse anaerobic eukaryotes that make energy and hydrogen, were once mitochondria. As hydrogenosomes generally lack a genome, the conversion is probably one way. The sources of the key hydrogenosomal enzymes, pyruvate : ferredoxin oxidoreductase (PFO) and hydrogenase, are not resolved by current phylogenetic analyses, but it is likely that both were present at an early stage of eukaryotic evolution. Once thought to be restricted to a few unusual anaerobic eukaryotes, the proteins are intimately integrated into the fabric of diverse eukaryotic cells, where they are targeted to different cell compartments, and not just hydrogenosomes. There is no evidence supporting the view that PFO and hydrogenase originated from the mitochondrial endosymbiont, as posited by the hydrogen hypothesis for eukaryogenesis. Other organelles derived from mitochondria have now been described in anaerobic and parasitic microbial eukaryotes, including species that were once thought to have diverged before the mitochondrial symbiosis. It thus seems possible that all eukaryotes may eventually be shown to contain an organelle of mitochondrial ancestry, to which different types of biochemistry can be targeted. It remains to be seen if, despite their obvious differences, this family of organelles shares a common function of importance for the eukaryotic cell, other than energy production, that might provide the underlying selection pressure for organelle retention.

Abstract: It is now common knowledge that mitochondria originated about one billion years ago from a symbiotic α-Proteobacterium that resided inside a host cell. Yet, two fundamental questions remain unanswered: (1) what is the exact nature of this host organism? and (2) when did distinctive eukaryotic features emerge – simultaneously with or well before mitochondrial symbiosis? These questions have been the subject of extensive speculation due to limited phylogenetic evidence for evolutionary events that long ago. The two most influential theories on the origin of eukaryotes are the Serial Endosymbiont theory and the symbiogenesis hypotheses, both with multiple variants. According to the first, eukaryotes evolved gradually from an ancient lineage devoid of mitochondria (termed Archezoa), and eventually acquired an endosymbiotic α-Proteobacterium that was transformed into a subcellular organelle. In contrast, the more recent symbiogenesis theory posits that eukaryotes originated by metabolic syntrophy of an archaeal cell and a bacterial cell. The merger of two simple prokaryotic organisms would have given rise to the highly complex eukaryotic cell with its subcellular structures such as nucleus and cytoskeleton, and, according to one variant of the symbiogenesis theory, the hydrogen hypothesis, simultaneously to mitochondria. The unquestioned tenet of this hypothesis is that evolution proceeds from simple (primitive) to complex (higher in an Aristotelian sense) life forms. This review confronts these theories with known evolutionary principles and results from rigorous molecular phylogenies. Although all theories on eukaryotic origins lack evidence for one or more of the predicted evolutionary intermediates (in the form of modern descendants), symbiogenesis scenarios have an additional shortcoming: they do not account for the evolutionary time span required for creating thousands of genes that encode eukaryotic subcellular structures.

Abstract: Publisher Summary This chapter discusses the origin of eukaryote and mitochondria. On the issue of eukaryote origins, biologists are divided into various camps. The camps express and defend fundamentally different views about how eukaryotes are linked to prokaryotes in both the phylogenetic sense and in the sense of evolutionary mechanisms. The chapter examines hypotheses concerning the origin of mitochondria and hydrogenosomes, the kind of host that might have acquired their common ancestral endosymbiont, how “Canfield” oceans fit into the picture at mitochondrial origin, and how the origin of mitochondria might have precipitated the origin of the nucleus, had the host been a bona fide prokaryote. The standard model of how and why the mitochondrion becomes established is discussed. Substantial problems with the standard model are described. The chapter also discusses the same issues from the standpoint of an alternative theory. The standard model is couched in an older view of Earth history that entails an oxygen catastrophe, during which a radical transition from globally anoxic habitats to globally oxic habitats is assumed. There are many suggestions in the literature for the origin of mitochondria besides the standard model and the hydrogen hypothesis, but all of them except one operate with a heterotrophic host for the origin of mitochondria.