Review
Mitochondria as we don't know them

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Abstract

Biochemistry textbooks depict mitochondria as oxygen-dependent organelles, but many mitochondria can produce ATP without using any oxygen. In fact, several other types of mitochondria exist and they occur in highly diverse groups of eukaryotes – protists as well as metazoans – and possess an often overlooked diversity of pathways to deal with the electrons resulting from carbohydrate oxidation. These anaerobically functioning mitochondria produce ATP with the help of proton-pumping electron transport, but they do not need oxygen to do so. Recent advances in understanding of mitochondrial biochemistry provide many surprises and furthermore, give insights into the evolutionary history of ATP-producing organelles.

Section snippets

Anaerobic mitochondria in protists and metazoa

The list of eukaryotes with anaerobic mitochondria spans unicellular (protists) and multicellular organisms, including flatworms (platyhelminths), parasitic nematodes and invertebrates such as mussels and snails (see Table 1). Anaerobic mitochondria are known to exist in some algae, such as Euglena (see below), but are not found in land plants. It is not known whether this possible absence has an evolutionary relevance or whether it is a mere fluke of sampling.

Anaerobically functioning

Fumarate-respiring mitochondria – a closer look at metabolism

The best studied examples of the second class of anaerobic mitochondria, those that use an endogenously produced final electron acceptor, are the anaerobic mitochondria of parasitic helminths such as Fasciola hepatica and Ascaris suum 12., 13., 14., 15. (Table 1). Whereas free-living and some larval stages possess mitochondria that use oxygen, the adult stages of most parasitic helminths are able to survive the anaerobic conditions in their habitat by using a pathway called malate dismutation.

Succinate dehydrogenase versus fumarate reductase

In aerobic energy metabolism, electrons coming from succinate generated in the Krebs cycle are transferred to ubiquinone through complex II (succinate dehydrogenase) of the respiratory chain (Fig. 1). However, in anaerobic energy metabolism fumarate serves as the terminal electron acceptor and electrons are transferred in the reverse direction, from a quinone to fumarate (Fig. 1). Succinate oxidation and fumarate reduction are generally carried out by separate enzymes in vivo. Accordingly, in

Other oddball mitochondria

The facultatively anaerobic mitochondria of Euglena gracilis have a unique ATP-producing biochemistry 31., 32., 33.. They perform the oxidative decarboxylation of pyruvate using an oxygen-sensitive enzyme – pyruvate:NADP+ oxidoreductase (PNO) – which is closely related to pyruvate:ferredoxin oxidoreductase (PFO) from hydrogenosomes [34]. Mitochondria from aerobically grown Euglena cells also have PDH activity [35], but PNO is active [33] and expressed [34] under both aerobic and anaerobic

A new chapter in mitochondrial ATP synthesis: chemolithoheterotrophy

Despite their differences, all the various mitochondria described above have one thing in common, which they also share with aerobic mitochondria: all the electrons involved in mitochondrial ATP synthesis always stem from organic compounds. This rule is so general that almost nobody would think of looking for an exception. But there is an exception, an exciting one.

Many aquatic invertebrates inhabit oxygen-poor, sulfide-rich sediments 41., 42., 43.. The mitochondria of these organisms, for

Evolutionary origin of anaerobic mitochondria

The diversity of anaerobic mitochondria (and hydrogenosomes) raises the question of the diversity of the underlying evolutionary routes. Two explanatory principles appear to account for the origin of anaerobic mitochondria and hydrogenosomes: 1) inheritance and 2) lateral acquisition 46., 47.. Both views include the possibility of evolutionary modification of either inherited or acquired genes.

In the inheritance model, the genes for the enzymes specific to anaerobic mitochondria (and

Acknowledgements

We thank Paul Deley for preparing the figures. C.R. is the recipient of a Ph.D. stipend from the Studienstiftung des deutschen Volkes. Work in the laboratory of W.M. is supported by the Deutsche Forschungsgemeinschaft and Sonderforschungsbereich-Transregio 1. Work in the laboratory of A.G.M.T. and J.J.vH. is supported by The Netherlands Organization for Scientific Research: The Netherlands Foundation for Chemical Research, and the Life Science Foundation.

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