A mitochondrial-like chaperonin 60 gene in Giardia lamblia: Evidence that diplomonads once harbored an endosymbiont related to the progenitor of mitochondria

Abstract

Diplomonads, parabasalids, as represented by trichomonads, and microsporidia are three protist lineages lacking mitochondria that branch earlier than all other eukaryotes in small subunit rRNA and elongation factor phylogenies. The absence of mitochondria and plastids in these organisms suggested that they diverged before the origin of these organelles. However, recent discoveries of mitochondrial-like heat shock protein 70 and͞or chaperonin 60 (cpn60) genes in trichomonads and microsporidia imply that the ancestors of these two groups once harbored mitochondria or their endosymbiotic progenitors. In this report, we describe a mitochondrial-like cpn60 homolog from the diplomonad parasite Giardia lamblia. Northern and Western blots reveal that the expression of cpn60 is independent of cellular stress and, except during excystation, occurs throughout the G. lamblia life cycle. Phylogenetic analyses position the G. lamblia cpn60 in a clade that includes mitochondrial and hydrogenosomal cpn60 proteins. The most parsimonious interpretation of these data is that the cpn60 gene was transferred from the endosymbiotic ancestors of mitochondria to the nucleus early in eukaryotic evolution, before the divergence of the diplomonads and trichomonads from other extant eukaryotic lineages. A more complicated explanation requires that these genes originated from distinct ␣-proteobacterial endosymbioses that formed transiently within these protist lineages.

Mitochondrial-type iron–sulfur cluster biosynthesis genes (IscS and IscU) in the apicomplexan Cryptosporidium parvum

“…[Fe-S] biogenesis also requires reduced iron (Scheffler, 1999), which is highly toxic for cells (Scheffler, 1999;Gerber & Lill, 2002), and therefore a reason for retaining mitochondrial compartments even if they have become altered (Roger et al, 1998;Katinka et al, 2001;Williams et al, 2002). Recent evidence has shown, for example, that 59 Fe can be incorporated into the hydrogenosome of the cattle parasite Tritrichomonas foetus, and that this requires ferredoxin and other peptides within the [Fe-S] machinery (Suchan et al, 2003).…”

On the origins of cells: a hypothesis for the evolutionary transitions from abiotic geochemistry to chemoautotrophic prokaryotes, and from prokaryotes to nucleated cells

“…The long-held view that the host was a eukaryote drew support primarily from the existence of eukaryotes without mitochondria (Cavalier-Smith 1987) and from the finding that they branched deeply in the eukaryotic branch of the 'universal tree' of ribosomal RNA (Vossbrink et al 1987;Sogin et al 1989). But all of the mitochondrion-lacking and suspectedly primitive eukaryotes that built the basis for traditional views on the origins of mitochondria, for example microspridians, diplomonads, entamoebids and the like, have turned out either to have possessed mitochondria in their past or to still possess the organelle in reduced form (Embley & Hirt 1998;Roger et al 1998;Roger 1999;Mü ller 2000;Philippe et al 2000). They are thus not direct descendants of an amitochondriate host.…”

Cytoskeletal organization, phylogenetic affinities and systematics in the contentious taxon Excavata (Eukaryota)

“…In the last half of the 1990s, the primitively amitochondriate status of diplomonads was challenged by the discovery of putative mitochondrial isoforms of cpn60, IscS and perhaps HSP70 (Roger et al, 1998;Horner & Embley, 2001;Morrison et al, 2001;Tachezy et al, 2001). Recently, tiny relict mitochondrial organelles have been identified in Giardia (Tovar et al, 2003).…”