Key Early Ideas

Mitochondria and chloroplasts did not have a purely symbiotic origin but are chimaeric structures incorporating proteins from the host as well as the symbiont. (Cavalier-Smith 1987c) The origin of mitochondria by the essentially permanent internal enslavement of a purple non-sulphur bacterium (a-proteobacterium) (John and Whatley 1975, 1977) by a host protoeukaryotic cell (Whatley et al. 1979) is now well established. There are, however, still many differences of opinion about the details of...

Maternal Inheritance of Mitochondria

As discussed previously, the mitochondrial theory of ageing rests on the observation that mitochondrial DNA is exposed to high levels of reactive oxygen species when the mitochondrion is performing its redox chemistry. These reactive oxygen species cause mutation. These mutations accumulate, gradually damaging the mitochondrion's ability to function. This happens in all the cells of an organism, leading to the symptoms we know as ageing, and eventually to death. One of the problems facing any...

Mitochondrial Origin and Eukaryogenesis

9.4.1 Common Ancestry of Rickettsiae and Mitochondria As stated before, most detailed phylogenetic data based on Cpn60 and SSU rRNA sequences (Fig. 9.1) point to the common origin of mitochondria and Rickettsiaceae-Anaplasmataceae families from within endosymbiotic a-Proteobacteria, whose closest extant relatives are the RLE group of endosymbionts. Within the Rickettsiaceae-Anaplasmataceae assemblage, the genus Rickettsia is the least divergent group (Emelyanov and Sinitsyn 1999, Emelyanov...

Genic Scale Tempo and Timing of Mitochondrial Enslavement and Eukaryote Origin

Mitochondria might therefore have originated and diversified as recently as 800 My ago. (p. 277 in Cavalier-Smith 1983a) This still seems to me the best lower-bound estimate to the nearest 100 million years. The upper bound is harder to place, but about 900 million years ago is perhaps most reasonable (Cavalier-Smith 2006a). Elsewhere I explained why I think the remarkably well preserved Bangiomorpha fossils are probably cyanobacteria not red algae and why I do not accept that any fossils...

Allometric Scaling of Metabolic Rate and Complexity

Metabolic syntrophy, such as posited by the hydrogen hypothesis, explains why only endosymbiosis is stable enough over evolutionary time to enable multiple core contingents of genes controlling redox poise to be co-localised with a wide area of bioenergetic membranes. Although such endosymbiosis is common in eukaryotes, it is far less common in bacterial communities, which tend to live together but not inside one another. A major obstacle to endosymbiosis in bacteria is the absence of...

Dynamics of Gene Gain and Gene Loss in Bacteria

Reductive evolution is now thought to play a pervasive role in bacteria. The classic examples are obligate intracellular parasites such as Rickettsia prowazekii (Frank et al. 2002 Andersson and Kurland 1998), but the rule is general. Many facets of prokaryotic genome organisation attest to selection for small genomes, including the prevalence of haploid genomes, the low proportion of non-coding DNA, the rarity of introns, the existence of a single copy most genes, and the organisation of...

References

Abrahamsen MS, Templeton TJ, Enomoto S, Abrahante JE, Zhu G, Lancto CA, Deng M, Liu C, Widmer G, Tzipori S, Buck GA, Xu P, Bankier AT, Dear PH, Konfortov BA, Spriggs HF, Iyer L, Anantharaman V, Aravind L, Kapur V (2004) Complete genome sequence of the Apicomplexan, Cryptosporidium parvum. Science 304 441-445 Akhmanova A, Voncken FG, van Alen A, van Hoek A, Boxma B, Vogels GD, Veenhuis M, Hackstein JHP (1998a) A hydrogenosome with a genome. Nature 396 527-528 Akhmanova A, Voncken FGJ, Harhangi...

Introduction

Hydrogenosomes are membrane-bounded organelles, approximately 1-2 m in size, that compartmentalize the terminal reactions of anaerobic cellular energy metabolism in eukaryotes. They were first described in the parabasilid flagellate, Tritrichomonas foetus, in an influential publication by Lindmark and M ller (1973) as subcellular particles that produce hydrogen and ATP. Since that time hydrogenosomes have been described in a number of rather different unicellular eukaryotes adapted to...

Before the Word

A symbiotic theory for the origin of all nucleated cells from two phylogenet-ically distinct kinds of organisms had been proposed before the reality of mitochondria was established. Although he is typically overlooked today, Japanese zoologist Shosaburo Watase (1862-1929) was perhaps the first to advocate it (Sapp 1994). Watase had visited the USA as a student in 1886 and he completed his Ph.D. in 1890 under William Keith Brooks at Johns Hopkins University. Between 1890 and 1899, he was a...

Kingdom Come Kingdom Go

By the early 1980s it was generally assumed that the protomitochondrion was an aerobic a-proteobacterium that had entered a strictly anaerobic amito-chondriate eukaryote. Such amitochondriate protists existed. There were more than 1,000 species of them (Fenchel and Finlay 1995). Cavalier-Smith (1983) grouped them into a subkingdom, the Archezoa, a primitive form of life that had emerged before the acquisition of chloroplasts and mitochondria. It included four phyla Metamonads, Microsporidia,...

Chytrid Fungi

There has never been any doubt that anaerobic chytridiomycetes (fungal symbionts such as Neocallimastix or Piromyces that colonize the gastrointestinal tract of herbivorous mammals) evolved from mitochondrion-bearing ancestors, as phylogenetic analyses demonstrated that they form a mono-phyletic group with the aerobic chytridiomycetes and all other fungi (Akhmanova et al. 1998a van der Giezen et al. 2002 Voncken et al. 2002a Fig. 10.3). Thus, anaerobic chytrid fungi have secondarily lost their...

Possible Variants in Anaerobic Metabolism

When organisms have to function (temporarily) without oxygen as terminal electron acceptors, they have to maintain redox balance without aerobic respiration hence, the reduced cofactors produced by the catabolic pathways have to be oxidized by an alternative process. Organisms with an anaerobic energy metabolism can be broadly divided into two different classes those that perform anaerobic respiration using an alternative electron acceptor present in the environment, such as nitrate, and those...

The Origin of Mitochondria the Symbiont

The evidence that modern mitochondria are derived from a eubacterial ancestor is sufficient that no reasonable argument can be made to the contrary however, the identity of the closest extant relatives to mitochondria is a more contentious issue. Phylogenetic analyses indicate that mitochondria likely emerged from among the a-proteobacteria, a diverse group with lifestyles ranging from autotrophic to parasitic. Most studies have suggested that, within the a-proteobacteria, the sister group to...

Did Syntrophy or Endosymbiosis Precede Enslavement

Syntrophic consortia of prokaryotes (Overmann and Schubert 2002) were probably not important in the origin of eukaryotes, despite frequent suggestions of this (Margulis 1981 Martin and M ller 1998), because unlike phagotrophy (Cavalier-Smith 1987b, 2002b) they would not have provided sufficient impetus and means for the origin of the major eukaryote innovations. Symbiotic associations between protozoa and prokaryotes are much more common (Finlay and Esteban 2001) and once the protoeukaryote...

Origins of Mitochondria

All developments seem to progress from simple to more complex forms. Whether this is true or just an imaginary chain of events that fits more comfortably with our way of thinking remains to be seen. The anthropocentric view comes naturally to us. Cars, for example, evolved from simple horseless carriages to high-performance automotive vehicles. This evolution, according to some proponents, is similar to the evolution of living organisms, including parameters such as natural selection....

The Host Was a Protoeukaryote Not an Archaebacterium

Ever since Woese and Fox (1977) suggested that the last common ancestor of all life was a precellular incompetent 'progenote' and Van Valen and Maiorana (1980) suggested that eukaryotes evolved from archaebacteria there has been confusion over this issue. Woese and Fox's never remotely tenable idea of the cenancestor as a simple precellular entity has been adequately refuted numerous times by many authors (e.g. Cavalier-Smith 1981, 1987a,b Pereto et al. 2004) but to this day continues to...

Iron Sulfur Cluster Assembly Machineries

The study of FeS cluster formation is an emerging field, with FeS cluster assembly first characterized in the nitrogen-fixing bacterium Azotobacter vinelandii in 1992 (Kennedy et al. 1992). In bacteria there are at least three different systems involved in this process (1) the NIF (nitrogen-fixing) system, which is primarily involved in the FeS cluster formation of nitrogenase (Kennedy et al. 1992) (2) the ISC (FeS cluster) assembly machinery, dedicated to forming FeS clusters in proteins...

Iron Sulfur Cluster Biosynthesis and the Evolution of Mitochondria

Eukaryotic cells have several internal compartments, each of which has a discrete metabolic function. There are different evolutionary scenarios attempting to explain the history of these organelles and the selection pressure that propelled their genesis. To further this aim, an important point is to define the essential functions of the organelles conserved in organisms amongst all branches of the eukaryotic tree. Mitochondria were derived some two billion years ago from endosymbi-otic...

The Chimaeric Origin of Mitochondrial Protein Import and Targeting

The idea that mitochondrial and chloroplast protein-import machineries both evolved by 'relatively slight modifications' of the negibacterial proteinexport machinery, with some key novelties provided by the host (Cavalier-Smith 1982, 1983a), has proved essentially correct. Clear relics of four major bacterial export systems have persisted the specifically negibacterial Omp85 system for inserting P-barrel proteins into the OM, and the prokaryotic YidC system for posttranslational insertion into...

The Origins of Mitochondria Mitosomes and Hydrogenosomes

From the foregoing section it should be clear that there is vast diversity in the structure, function and evolutionary history of mitochondrion-derived organelles in anaerobic protists. Although much has yet to be learned about these disparate organellar systems, several evolutionary scenarios regarding their evolutionary history seem possible. The two most likely scenarios are shown in Fig. 10.5 and are discussed next. First, it is possible that enzymes of aerobic and anaerobic energy...

Relative Genomic Contributions of the Two Partners

Each mitochondrial protein will have to be examined in detail for its affinities with purple bacteria on the one hand and posibacteria archaebacteria on the other to determine whether it came from host or symbiont. (p. 66 in Cavalier-Smith 1987c) From the topology of Fig. 8.1 it should be clear that if there were a uniform molecular clock (an idea that I refuted for rRNA 25 years ago, Cavalier-Smith 1980, and have never accepted for any protein either), and if one assumes no nuclear...

Functional Differences Between Mitochondrial and Alternative Adpatp Transporters

The phylogenetic analysis of the various ADP ATP transporters might either argue for a deep evolutionary divergence of these organelles from a (facultatively) anaerobic, premitochondrial ancestor or, alternatively, for a secondary loss of all true mitochondrial AACs in all of these organelles, followed by the evolution of alternative ADP ATP transporters (Tjaden et al. 2004). In any case, phylogenetic evidence supports at least six (but potentially much more) independent origins of...

Chimeric Nature of a Proeukaryote

9.3.1 Energy Metabolism of Eukaryotes and the Hydrogen Hypothesis As noted in Sect. 9.2.1, the energy metabolism of eukaryotes is relatively simple when compared with that of prokaryotes. With the exception of photosynthetic organisms, all eukaryotes are heterotrophs whose energy metabolism relies on oxidative breakdown of reduced compounds. The first steps of carbohydrate utilization proceed along the glycolytic pathway yielding pyruvate. In eukaryotes with mitochondria, pyruvate penetrates...

Energy Metabolism in Anaerobically Functioning Mitochondria

Organisms with anaerobic mitochondria can be divided into two different types those which perform anaerobic respiration and use an alternative electron acceptor present in the environment, such as nitrate or nitrite, and those which perform fermentation reactions using an endogenously produced, organic electron acceptor, such as fumarate (Martin et al. 2001 Tielens et al. 2002). An example of the first type is the nitrate respiration that occurs in several ciliates (Finlay et al. 1983), and...

The Mitochondrial Theory of Ageing

Reactive oxygen species, generated largely by the mitochondrial electron transport chain, damage the mitochondrial proteins and DNA, and the mitochondrial theory of ageing, simply put, states that this damage leads to ageing and its associated degenerative diseases (Fig. 3.3). This theory was first put forward by Harman (1956), although earlier observations had linked life span to metabolic rate the higher the metabolic rate, the shorter the life span (Pearl 1928). Although Harman's theory has...

Evolutionary Tinkering in the Evolution of Hydrogenosomes

Hydrogenosome

7.4.1 Hydrogenosomes of Trichomonas vaginalis The hydrogenosomes of the trichomonads Parabasalia have been studied intensively for more than 30 years Lindmark and M ller 1973 M ller 1993 . Upon initial inspection, these organelles were considered, both morpho- Table 7.3. Effects of various inhibitors on a32P ADP uptake into E. coli cells expressing several adenine nucleotide carriers. E. coli cells were preincubated for 10 min with lysozyme 2.5 mg ml to allow penetration of the reagents across...

ATP Regulation of Bacterial Replication

For both bacteria and eukaryotes, ATP subsaturation is the norm. On a global scale it is clear that this is the case. In optimal conditions, E. coli can divide every 20 min, or 72 times in a day. A single E. coli bacterium weighs about 10-12 g, so 72 cell divisions in a day corresponds to an amplification of 272 1072 x log2 10216 , or an increase in weight from 10-12 g to 4,000 t O'Farrell 1992 . In 2 days the mass of exponentially doubling E. coli would be 2,664 times larger than the mass of...

Colocation of Gene and Gene Product Permits Redox Regulation of Gene Expression

This hypothesis states that mitochondria and chloroplasts contain genes whose expression must be under the direct, regulatory control of the redox state of their gene products, or of electron carriers with which their gene products interact Fig. 3.4 . These genes comprise a primary subset of organellar genes. The requirement for redox control of each gene then confers a selective advantage upon location of that gene within the organelle instead of in the cell nucleus. Mitochondrial and...

Discovery of Mitosomes a Brief History

To place the research leading to the discovery of mitosomes in a historical context it is important to remember that all eukaryotic organisms in which typical mitochondria could not be recognised by microscopic or biochemical methods were once grouped within the kingdom Archezoa Cavalier-Smith 1983 . In its original formulation, the Archezoa hypothesis proposed that members of four heterogeneous amitochondriate protist groups - namely Metamonads, Microsporidia, Parabasalia and Archamoebae -...

Hydrogenosomes and Mitochondrial Remnant Organelles Evolved Repeatedly Evidence from Adpatp Carriers

Initially, the arguments that both mitosomes, the mitochondrial-remnant organelles, and hydrogenosomes evolved several times were based on the observation that hydrogenosomes and mitosomes, respectively, were found in a broad spectrum of rather unrelated taxa of unicellular organisms, such as trichomonads, diplomonads, sarcodina entamoebids , flagellates, api-complexa, ciliates, and chytrids Biagini et al. 1997a Embley et al. 1997 Roger 1999 Abrahamsen et al. 2004 Yarlett and Hackstein 2005 van...

The Story

After having spent some years in Budapest exploring protist food vacuoles and lysosomes with histochemical methods, I was given the opportunity of my life by Christian de Duve, who received the Nobel Prize in 1974 for the discovery of lysosomes and peroxisomes. In 1964 he invited me to join his laboratory at the Rockefeller University still called Institute then to explore these organelles with biochemical and cell fractionation methods in protists. My work in New York...