Hydrogenosomes and Mitochondrial Remnant Organelles Evolved Repeatedly

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

Tree Mitochondria

Fig. 1. Illustration displaying the phylogenetic relationships between aerobic and anaerobic protists (based on a variety of molecular data) together with a tentative evolutionary tree of mitochondria, modified mitochondria, mitochondrial remnants, and hydrogenosomes. The solid lines indicate phylogenetic relationships that are based on the analysis of "mitochondrial" genomes. Dashed lines indicate the loss of organellar genomes. The tentative phylogenetic relationships between the various types of organelles belonging to the "mitochondrial" family are therefore based on the analysis of nuclear genes encoding organellar proteins. These parts of the tree might be flawed by lateral gene transfers, evolutionary changes in the targeting to the various subcellular compartments, and biased evolutionary rates. See Table 1 and the text for details

Fig. 1. Illustration displaying the phylogenetic relationships between aerobic and anaerobic protists (based on a variety of molecular data) together with a tentative evolutionary tree of mitochondria, modified mitochondria, mitochondrial remnants, and hydrogenosomes. The solid lines indicate phylogenetic relationships that are based on the analysis of "mitochondrial" genomes. Dashed lines indicate the loss of organellar genomes. The tentative phylogenetic relationships between the various types of organelles belonging to the "mitochondrial" family are therefore based on the analysis of nuclear genes encoding organellar proteins. These parts of the tree might be flawed by lateral gene transfers, evolutionary changes in the targeting to the various subcellular compartments, and biased evolutionary rates. See Table 1 and the text for details trichomonads, diplomonads, sarcodina (entamoebids), flagellates, ciliates and chytrids (Fig. 1; Biagini et al. 1997; Embley et al. 1997; Roger 1999).

In addition, the presence of an anaerobic mitochondrion-like organelle in Blastocystis hominis (Straminopiles) has been proposed - mainly based upon redox sensitive dyes (Nasirudeen and Tan 2004). However, since most of these organelles did not retain a genome, the only common diagnostic characters seemed to be (i) the presence of "mitochondrial-type" chaperonines (Clark and Roger 1995; Bui et al. 1996, Germot et al. 1996), (ii) the fact that these organelles were membrane bounded, and (iii), in the case of hydrogenosomes, that these organelles produced ATP (Müller 1993). The phylogenetic analysis of HSP(cpn) 60 supported different "mitochondrial" origins of the various organelles (Voncken 2001; Voncken et al. 2002a; van der Giezen et al. 2003).

Phylum

Order

Species

Organelle

HSP60

Hydrogenase

Pyruvate metab.

Comp. Energy metab.

Organelle genome

Methanogenic endosymbiont

Mastigophora

Trichomonadida

Trichomonas (Trichomonadinae)

Hydrogenosome

HSP60

[Fe]

PFO

Yes

No

No

Diplomonadida

Giardia (Giardiinae)

Crypton

cytopl.HSP60

[Fe] cytopl.

PFO

No

No

No

Spironucleus (Hexamitidae)

None identified

cytopl.HSP60

[Fe]

PFO

No

No

No

Pelobiontida

Mastigam oeba (Mastigamoebidae)

None identified

ND

[Fe]

PFO

ND

No

No

Ciliophora

Armophorida

Nyctotherus (Clevelandellidae)

Hydrogenosome

HSP60

[Fe] 24kD+51kD

PDH

Yes

Yes

Yes

Metopus (Armophoridae)

Hydrogenosome

ND

[Fe]

ND

Yes

Yes

Yes

Vestibuliferida

Dasytricha (Isotrichidae)

Hydrogenosome

ND

[Fe]

PFO

Yes

No

No

Plagiopylea

Trimyema (Plagiopylidae)

Hydrogenosome

ND

Yes

PFL

Yes

ND

Yes

Plagiopyla (Plagiopylidae)

Hydrogenosome

ND

Yes

ND

ND

ND

Yes

Sarcodina

Amoebida

Entamoeba (Lobosea)

Mitosome

HSP60

[Fe] cytopl.

PFO

No

No

No

Percolozoa

Schizopyrenida

Psalteriomonas (V ahlkamphiidae)

Hydrogenosome

ND

[Fe]

ND

Yes

No

Yes

Alveolata

Apicomplexa

Cryptosporidia (Cryptosporidiidae)

Relict-mitochondrion

Cpn60

NARF

PNOR

No

No

No

Stramenopiles

Blastocystis (Stramenopiles)

Modified mitotochondrion

cytopl.HSP70

No

Unknown

ND

Yes

No

Microsporidia

Pansporablastina

Track ipleistophora (P leistophoridae)

Relict-mitotochondrion

No HSP70

No

Rudiment PDH

No

No

No

Chytridiomycota

Spizellomycetales

Piromyces (Neomasticalligales)

Hydrogenosome

HSP60

[Fe]

PFL

Yes

No

No

Neocallimastix (Neomasticalligales)

Hydrogenosome

HSP60

[Fe]

PFL

Yes

No

No

Abbreviations:; Pyruvate ferredoxin oxidoreductase (PFO); Pyruvate dehydrogenase (PDH); Pyruvate formate lyase (PFL);

Heat shock protein (HSP); Chaperonin (Cpn); Pyruvate NADH oxidoreductase (PNOR); Hydrogenosomal membrane protein (HMP);

Not determined (ND).

However, a functional and phylogenetic analysis of hydrogenosomal ADP/ATP carriers (AAC) so far revealed that only the hydrogenosomes of chy-trids and ciliates possess genuine mitochondrial AAC's, which cluster with the mitochondrial homologues of their aerobic, mitochondria-bearing relatives (Voncken 2001; Voncken et al. 2002a; Haferkamp et al. 2002; van der Giezen et al. 2002). Trichomonas uses alternative - potentially pre-mitochondrial - AACs for the transport of ATP across its hydrogenosomal membranes (Dyall et al. 2000; Tjaden et al. 2004). Furthermore, there is no evidence for the presence of true mitochondrial AACs in any of the mitosomes/cryptons or mitochondrial remnant organelles until now. Of course, the latter do not produce ATP, and therefore, might not require mitochondrial-type AACs (Tovar et al. 1999, 2003; Katinka et al. 2001; Williams et al. 2002). Also, the genome projects of Giardia and Entamoeba could not reveal the presence of true mitochondrial AACs, see http://www.NCBI.nih.gov. Thus, these observations might either argue for a deep evolutionary divergence of these organelles from a (facultatively) anaerobic, hydrogen-producing, pre-mitochondrial ancestor, or, alternatively, for a secondary loss of true mitochondrial AACs in all of these organelles (Tjaden et al. 2004). In any case, the available evidence strongly supports at least three to four (but potentially much more) independent origins of hydrogenosomes and mi-tochondrial-remnant organelles from organelles belonging to the "mitochondrial" family - regardless whether these ancestral organelles were strictly aerobic or facultatively anaerobic (Fig. 1; Embley et al. 2003).

Assuming an aerobic, mitochondrial ancestor, the host could rely on a splendid supply with ATP generated with the aid of the mitochondrial electron transport chain. Under anaerobic conditions, however, the mitochondrial electron transport chain cannot use oxygen as a terminal electron acceptor and the energy conservation function by the generation of ATP cannot be fulfilled (Hackstein et al. 1999, 2001). Such a cell faces a dramatic accumulation of reduction equivalents in the mitochondrion, and, consequently, it has to rely on glycolysis in the cytoplasm, which can provide only a very limited amount of ATP. Notably, certain mitochondria can cope with an anoxic environment maintaining certain mitochondrial functions even under such adverse conditions. These mitochondria are able to use alternative environmental electron acceptors (e.g., nitrate), or metabolic (Krebs cycle) intermediates such as fu-marate as an endogenous electron acceptor allowing a rudimentary function of the electron transport chain even in the complete absence of oxygen (Tielens et al. 2002). In other eukaryotes, however, the adaptation to anoxic niches caused a degeneration of the mitochondrion to rather inconspicuous cellular compartments with a concomitant loss of the electron transport chain and its energy conservation capacities, as discussed earlier (Embley and Martin 1998; Rotte et al. 2000). Certain mitochondrial functions such as the production of acetyl-CoA and keto-acids for lipid and carbohydrate biosynthesis, respectively, were maintained even in the absence of a functioning electron transport chain - albeit in an alternative subcellular compartment (Akhmanova et al.

1998b; Müller 1998; Hackstein et al. 1999; Henze and Martin 2003; Dyall et al. 2004).

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