Mitochondrion Related Organelles in Amitochondriate Eukaryotes

It is generally accepted that mitochondria evolved from endosymbiotic bacteria most likely of proteobacterial origin (Esser et al. 2004). A debated question of interest is whether the ancestral host was an amitochondriate protoeukaryote, which gained mitochondria at a certain stage of eukaryoge-nesis, or whether the appearance of the mitochondria was directly associated with the origin of the eukaryotic cell. The latter idea was elaborated in two symbiosis hypotheses: the hydrogen hypothesis (Martin and Müller 1998) and the syntrophy hypothesis (Moreira and Lopez-Garcia 1998). Both proposed a symbiotic metabolic association in anaerobic environments between an archaeal methanogen and a proteobacterion, although they provide different views concerning the nature of the eubacterial partners (discussed in Lopez-Garcia and Moreira 1999). Accordingly, the absence of mitochondria in "amitochondriates" was considered to be a result of two possible scenarios: contemporary "amitochondriates" are either (1) descendants of primarily amitochondrial protoeukaryotes, which separated from the main eukaryotic trunk before the mitochondrial endosymbiosis, or (2) they lost their mitochondria in a secondary event owing to their specific adaptation to anaerobic or oxygen-restricted conditions. The first scenario was suggested for organisms long considered most ancient among eukary-otes, such as diplomonads, parabasalids, archamoebae, and microsporidia. The absence of apparent mitochondria was postulated as a "primitive" character, and the amitochondriate organisms were grouped into the taxon named Archezoa to indicate their ancient origin (Cavalier-Smith 1987a, b). Although later phylogenetic analysis eroded the Archezoa hypothesis (Roger et al. 1999), diplomonads and parabasalids still remain among the candidates that might represent the deepest diverging lineages of eukaryotes (Adam 2001; Best et al. 2004). The second scenario may explain amitochondriate status in organisms that belong to the monophyletic taxons together with organisms possessing typical mitochondria such as the apicomplexan Cryptosporidium or microsporidia, which are currently placed among fungi. However, if the appearance of eukaryotes was interrelated with the invention of mitochondria, a secondary loss of mitochondria can be expected even in "early branching" eukaryotes. Indeed, several genes regarded as mitochon-drial in origin, including mitochondrial-type heat shock protein 70 kDa (Hsp70) (Arisue et al. 2002; Bui et al. 1996; Germot et al. 1996), chaperonin 60 kDa (Cpn60) (Horner et al. 1996; Roger et al. 1998), valyl-transfer RNA

synthetase (Hashimoto 1998), and cysteine desulfurase IscS (Tachezy et al. 2001) were identified in genomes of some diplomonads and parabasalids, supporting secondary absence of mitochondria in these organisms. However, do they really lack mitochondria?

6.2.1 Hydrogenosomes

Although organelles corresponding to the textbook definition of mitochondria are not present in amitochondriates, parabasalids and some other protists possess double membrane bounded organelles called hydrogeno-somes. The hydrogenosomes are ATP-generating organelles employing substrate-level phosphorylation and protons as an electron sink. They represent a rather heterogenous group of organelles described in organisms of considerably distant phylogenetic positions. Hydrogenosomes were found in trichomonads and other parabasalids (Cerkasovová et al. 1973; Lindmark et al. 1975; Lindmark and Müller 1973), chytrid fungi (Neocalimastix sp.) (Yarlett et al. 1986a), amoeboflagellates (Psalteriomonas lanterna) (Broers 1992), and some free-living (Embley et al. 1995; Fenchel and Finlay 1994) as well as symbiotic (Paul et al. 1990; Snyers et al. 1982; Yarlett et al. 1981, 1983) ciliates. These organisms belong to separate lineages of protists, some of them forming monophyletic groups with organisms harboring typical mitochondria (Fig. 6.1). Therefore, the hydrogen-producing organelles have been derived repeatedly in various unicellular eukaryotes (Embley et al. 1995; Yarlett and Hackstein 2005).

The biogenesis and core metabolism of hydrogenosomes have been studied mainly in trichomonads and fungi, while information about the hydrogenosomes in other organisms is scanty (Dyall and Johnson 2000; Hackstein et al. 1999; Müller 2003). The main similarities between hydrogenosomes and mitochondria are (1) the presence of a double membrane surrounding the organelles, (2) the generation of ATP, (3) catalytic components of respiratory complex I (NADH dehydrogenase), (4) calcium storage, (5) mechanism of organelle division, (6) mode of protein targeting and maturation, and (7) mechanism of FeS cluster assembly. The main differences are (1) the absence of a hydrogenosomal genome with the exception of hydrogenosomes in some ciliates, (2) the absence of oxidative phos-phorylation, citric acid cycle, and P-oxidation of fatty acids, and (3) the production of hydrogen under anaerobic conditions.

On the basis of ultrastructural studies, comparative biochemistry, and molecular phologeny, it is now generally accepted that hydrogenosomes of ciliates and fungi evolved from aerobic mitochondria, and thus represent mitochondrial adaptation to oxygen-poor environments (Hackstein et al. 1999; Yarlett and Hackstein 2005). A rudimentary genome in hydrogenosomes of Nyctotherus ovalis coding for several components of a mitochondrial-type electron transport chain strongly suggests that these organelles represent a very recent adaptation (Akhmanova et al. 1998; Boxma

Cryptomonads Haptophytes

Dinoflagellates M Apicomplexa H Ciliates

Carpediemonas

Retortamonads M Diplomonads

H Parabasalids H Heteroloboseids Kinetoplastids

Cryptomonads Haptophytes

Cercozoa

Foraminifera

H Parabasalids H Heteroloboseids Kinetoplastids

Oxymonads

Trimastix

Slime Molds Acanthamoebae

Fig. 6.1. Distribution of hydrogenosomes (H) and mitosomes (M) in eukaryotes. The organisms harboring putative hydrogenosome- or mitosome-like organelles which have not been characterized are in green. (The eukaryotic tree was adapted according to Dacks et al. 2003)

Euglenoids Core Jakobids

Malawimonas

Oxymonads

Trimastix

Cercozoa

Foraminifera

Land Plants """"Green Algae

Glaucocystophytes

Red Algae Fungi H

Microsporidia M Animals

Choanoflagellates NuclearidAmoebae

Slime Molds Acanthamoebae elobionts Entamoebids M Apusomonads

Fig. 6.1. Distribution of hydrogenosomes (H) and mitosomes (M) in eukaryotes. The organisms harboring putative hydrogenosome- or mitosome-like organelles which have not been characterized are in green. (The eukaryotic tree was adapted according to Dacks et al. 2003)

et al. 2005). The origin of the trichomonad hydrogenosome is less apparent and has been a matter of debate since their discovery in 1973 (Cerkasovova et al. 1973; Lindmark and Müller 1973). The most frequently considered scenario is that they evolved together with mitochondria from a common eubacterial ancestor (Dyall et al. 2004a; Dyall and Johnson 2000; Embley et al. 2003a, 2003b; Yarlett and Hackstein 2005)

6.2.2 Mitosomes

Mitosomes (synonym crypton) is the name given to the double membrane bounded organelles considered to be highly reduced mitochondria. Unlike mitochondria and hydrogenosomes, mitosomes are not involved in ATP synthesis. The mitosomes were first recognized in Entamoeba histolytica as the organelles possessing a mitochondrial marker Cpn60 (Mai et al. 1999; Tovar et al. 1999). Although mostly one mitosome per amoeba cell was originally observed, over 200 mitosomes per cell were reported in a later study (Leon-Avila and Tovar 2004). In addition to Cpn60, the entamoebid mitosomes likely possess Hsp10 (van der Giezen et al. 2005) and a single ADP/ATP carrier (Chan et al. 2005). The function of these organelles, however, remains enigmatic. On the basis of genome analysis, the presence of mitosomes was also predicted in the microsporidian Encephalitozoon cuniculi (Katinka et al. 2001), and was then demonstrated experimentally in another microsporidian Trachipleistophora hominis (Williams et al. 2002) as an organelle in which a Hsp70 protein homologue was localized. Organelles of similar characteristics have been found in Cryptosporidium parvum, originally described as remnant mitochondria (Keithly et al. 2005; Riordan et al. 1999; Slapeta and Keithly 2004), and finally in Giardia intestinalis (Tovar et al. 2003). Like the hydrogenosomes, the mitosomes appear to have lost their own genomes, and genes coding for mitosomal proteins were transferred into the nucleus. The general mode of the protein synthesis, targeting, translocation, and processing seems to operate on a similar molecular basis in mitochondria, hydrogeno-somes, and mitosomes (Dolezal et al. 2005; Regoes et al. 2005).

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