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Mitochondrial Type Iron-Sulfur Cluster Assembly in the Amitochondriate Eukaryotes Trichomonas vaginalis and Giardia intestinalis, as Indicated by the Phylogeny of IscS (Tachezy et al., 2001)

This article shows a common origin between mitochondria and the amitochondriate organisms that contain either a mitosome or a hydrogenosomes. All organisms use FeS clusters and they show that the proteins involved are similar. This article places it in the context of a loss of function in the mitosomes, while I think it just indicates progressive evolution instead of reductive.

From the abstract: Phylogenetic analysis showed a close relationship among all eukaryotic IscS genes including those of amitochondriates. IscS of proteobacteria formed a sister group to the eukaryotic clade, suggesting that isc-related genes were present in the proteobacterial endosymbiotic ancestor of mitochondria and hydrogenosomes. NifS genes of nitrogen-fixing bacteria, which are IscS homologs required for specific formation of FeS clusters in nitrogenase, formed a more distant group. The phylogeny indicates the presence of a common mechanism for FeS cluster formation in mitochondriates as well as in amitochondriate eukaryotes. Furthermore, the analyses support a common origin of Trichomonas hydrogenosomes and mitochondria, as well as secondary loss of mitochondrion/hydrogenosome-like organelles in Giardia.

 Amitochondriate eukaryotes can be divided into two metabolic types (Martin and Müller 1998 ; Müller 1998 ). Type I organisms such as Giardia and Entamoeba lack organelles involved in core energy metabolism, while type II organisms (trichomonads, some ciliates, and chytrid fungi) harbor a double-membrane limited organelle, the hydrogenosome (Müller 1993 ; Hackstein et al. 1999 ; Kulda 1999 ). The hydrogenosome is the site of the FeS protein-mediated metabolism of pyruvate and the formation of molecular hydrogen, which is accompanied by substrate-level phosphorylation ATP synthesis. In type I amitochondriates, the FeS protein-dependent pyruvate metabolism takes place in the cytosol (Reeves 1984 ; Ellis et al. 1993 ).

It is also interesting if the type I (mitosomes) and type II (hydrogenosomes) and mitochondriate organism (mitochondria) are all unique in the sense that the organelles do not mix. Would be in line with the gradual evolution of mitosome>hydrogenosome and/or mitochondrion.

A common origin of the two organelles [mitochondria and hydrogenosomes] is supported by a number of similarities in their structure, function, and biogenesis (Johnson, Lahti, and Bradley 1993 ; Benchimol, Johnson, and De Souza 1996 ; Bui, Bradley, and Johnson 1996 ; Bradley et al. 1997 ; Dyall et al. 2000 ), as well as by phylogenetic analysis of several hydrogenosomal metabolic enzymes (Länge, Rozario, and Müller 1994 ; Hrd and Müller 1995a, 1995b ) and heat shock proteins (Müller 1997 ; Embley and Hirt 1998 ). Although neither mitochondria nor hydrogenosomes have been found in type I organisms, genes of probable mitochondrial origin have been identified in Giardia (Roger et al. 1998 ) and Entamoeba (Clark and Roger 1995 ). Moreover, a putative mitochondrial “remnant,” the mitosome (Tovar, Fischer, and Clark 1999 ) or crypton (Mai et al. 1999 ), has recently been detected in Entamoeba (Müller 2000 ).

The phylogenetic relationship shows that protists are generally grouped together and they are close to plants and metazoa and fungi.

In all global phylogenetic reconstructions, IscS/NifS-like homologs formed two distinct groups that were previously designated groups I and II (Mihara et al. 1997 ). The IscS sequences of Trichomonas and Giardia and those of the mitochondrial homologs in other eukaryotes formed a single clade (group I) with a high bootstrap value (99%) using the local rearrangement option of the PROTML program (fig. 3 ). Within this clade, Trichomonas and Giardia formed a subgroup together with Plasmodium falciparum and Arabidopsis thaliana. The second eukaryotic subgroup consisted of metazoan IscS, and the third group comprised homologs in fungal mitochondria. The -proteobacterium Rickettsia prowazeki, often considered a close relative to the mitochondrial ancestor, clustered together with metazoan mitochondrial IscS (Andersson and Kurland 1999 ).

 

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