A common evolutionary origin for mitochondria and hydrogenosomes.

Abstract

Trichomonads are among the earliest eukaryotes to diverge from the main line of eukaryotic descent. Keeping with their ancient nature, these facultative anaerobic protists lack two "hallmark" organelles found in most eukaryotes: mitochondria and peroxisomes. Trichomonads do, however, contain an unusual organelle involved in carbohydrate metabolism called the hydrogenosome. Like mitochondria, hydrogenosomes are double-membrane bounded organelles that produce ATP using pyruvate as the primary substrate. Hydrogenosomes are, however, markedly different from mitochondria as they lack DNA, cytochromes and the citric acid cycle. Instead, they contain enzymes typically found in anaerobic bacteria and are capable of producing molecular hydrogen. We show here that hydrogenosomes contain heat shock proteins, Hsp7O, Hsp6O, and HsplO, with signature sequences that are conserved only in mitochondrial and a-Gram-negative purple bacterial Hsps. Biochemical analysis of hydrogenosomal Hsp6O shows that the mature protein isolated from the organelle lacks a short, N-terminal sequence, similar to that observed for most nuclear-encoded mitochondrial matrix proteins. Moreover, phylogenetic analyses of hydrogenosomal Hsp7O, Hsp6O, and HsplO show that these proteins branch within a monophyletic group composed exclusively of mitochondrial homologues. These data establish that mitochondria and hydrogenosomes have a common eubacterial ancestor and imply that the earliest-branching eukaryotes contained the endosymbiont that gave rise to mitochondria in higher eukaryotes.

Hydrogenosomes in the anaerobic fungus Neocallimastix frontalis have a double membrane but lack an associated organelle genome

“…If one assumes a mitochondrial origin for trichomonad hydrogenosomes [22], a scenario which has recently received direct support from protein coding genes [23][24][25][26], then one can speculate that genome loss is through redundancy caused by change of function. Mitochondrial DNA encodes rRNA and tRNA components of the mitochondrial protein synthesizing machinery, which function is to translate a small number of mtDNA-encoded mRNAs that specify essential polypeptide components of the mitochondrial electron transport chain [27,28].…”

FRIENDLY Regulates Mitochondrial Distribution, Fusion, and Quality Control in Arabidopsis

“…Mitochondria are a defining component of eukaryotes: even the few groups of amitochondriate protists are believed to have secondarily lost the organelle (Clark and Roger, 1995;Bui et al, 1996;Gray et al, 1999). The long shared history of eukaryotes has led to considerable conservation of mitochondrial structure and function, although some divergence of both has occurred between plants, fungi, and animals since they split from their most recent common ancestor approximately 1,500 million years ago (Feng et al, 1997;Douzery et al, 2004;Hedges et al, 2004).…”

Presence of a Member of the Mitochondrial Carrier Family in Hydrogenosomes: Conservation of Membrane-Targeting Pathways between Hydrogenosomes and Mitochondria

“…Recently, molecular analyses of hydrogenosomal heat shock proteins from Trichomonas vaginalis (5,11,16,41) have demonstrated a close phylogenetic relationship between the nuclear genes encoding these proteins and their mitochondrial counterparts, suggesting a common symbiotic origin for the two organelles. The latest theory is one based on the metabolic force behind the symbiotic event-the hydrogen hypothesis (29).…”