Entamoeba histolytica as a model for the primitive eukaryotic cell

Bakker-Grunwald, Tilly; Wöstmann, Claudia

doi:10.1016/0169-4758(93)90161-8

Cited by 50 publications

(24 citation statements)

References 23 publications

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“…Previous investigators have suggested that the similarity of amebic fermentation enzymes to those of bacteria define E. histolytica as an "ancient" eukaryote (6,9,27,39,44,45,64). In contrast, the phylogenetic analyses performed here for POR, ADHE, ADH1, and FD (and elsewhere for SOD, PPFK, and ADH1) suggest that the E. histolytica genes encoding fermentation enzymes may have been transferred from bacteria and therefore do not represent those of ancient anaerobic eukaryotes (3,31,50).…”

Section: Discussioncontrasting

confidence: 51%

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Evidence for the bacterial origin of genes encoding fermentation enzymes of the amitochondriate protozoan parasite Entamoeba histolytica

Rosenthal¹,

Mai²,

Caplivski³

et al. 1997

J Bacteriol

103

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Entamoeba histolytica is an amitochondriate protozoan parasite with numerous bacterium-like fermentation enzymes including the pyruvate:ferredoxin oxidoreductase (POR), ferredoxin (FD), and alcohol dehydrogenase E (ADHE). The goal of this study was to determine whether the genes encoding these cytosolic E. histolytica fermentation enzymes might derive from a bacterium by horizontal transfer, as has previously been suggested for E. histolytica genes encoding heat shock protein 60, nicotinamide nucleotide transhydrogenase, and superoxide dismutase. In this study, the E. histolytica por gene and the adhE gene of a second amitochondriate protozoan parasite, Giardia lamblia, were sequenced, and their phylogenetic positions were estimated in relation to POR, ADHE, and FD cloned from eukaryotic and eubacterial organisms. The E. histolytica por gene encodes a 1,620-amino-acid peptide that contained conserved iron-sulfur-and thiamine pyrophosphate-binding sites. The predicted E. histolytica POR showed fewer positional identities to the POR of G. lamblia (34%) than to the POR of the enterobacterium Klebsiella pneumoniae (49%), the cyanobacterium Anabaena sp. (44%), and the protozoan Trichomonas vaginalis (46%), which targets its POR to anaerobic organelles called hydrogenosomes. Maximum-likelihood, neighbor-joining, and parsimony analyses also suggested as less likely E. histolytica POR sharing more recent common ancestry with G. lamblia POR than with POR of bacteria and the T. vaginalis hydrogenosome. The G. lamblia adhE encodes an 888-amino-acid fusion peptide with an aldehyde dehydrogenase at its amino half and an iron-dependent (class 3) ADH at its carboxy half. The predicted G. lamblia ADHE showed extensive positional identities to ADHE of Escherichia coli (49%), Clostridium acetobutylicum (44%), and E. histolytica (43%) and lesser identities to the class 3 ADH of eubacteria and yeast (19 to 36%). Phylogenetic analyses inferred a closer relationship of the E. histolytica ADHE to bacterial ADHE than to the G. lamblia ADHE. The 6-kDa FD of E. histolytica and G. lamblia were most similar to those of the archaebacterium Methanosarcina barkeri and the ␦-purple bacterium Desulfovibrio desulfuricans, respectively, while the 12-kDa FD of the T. vaginalis hydrogenosome was most similar to the 12-kDa FD of ␥-purple bacterium Pseudomonas putida. E. histolytica genes (and probably G. lamblia genes) encoding fermentation enzymes therefore likely derive from bacteria by horizontal transfer, although it is not clear from which bacteria these amebic genes derive. These are the first nonorganellar fermentation enzymes of eukaryotes implicated to have derived from bacteria.The endosymbiont hypothesis or serial endosymbiosis theory, one of the most exciting ideas in evolutionary biology, postulates that the mitochondria and chloroplasts of eukaryotic cells derive from an endocytosed ␣-purple bacterium and cyanobacterium, respectively ( Fig. 1) (18,19,35,63). Although bacterial rRNA genes as well as those encoding some structural protei...

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Section: Discussioncontrasting

confidence: 51%

“…In both locations, E. histolytica is an obligate fermenter, as it lacks mitochondria and enzymes of oxidative phosphorylation (6,39,44). However, several observations suggest the lineage giving rise to E. histolytica once possessed mitochondria and acquired other bacterial genes via endosymbiosis or transfection (Fig.…”

mentioning

confidence: 99%

Evidence for the bacterial origin of genes encoding fermentation enzymes of the amitochondriate protozoan parasite Entamoeba histolytica

Rosenthal¹,

Mai²,

Caplivski³

et al. 1997

J Bacteriol

103

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“…It is a structurally simple eukaryote, lacking mitochondria and peroxisomes and having no recognizable Golgi complex or rough endoplasmic reticulum (ER) (6,11,16). Some have hypothesized that E. histolytica diverged from other eukaryotic lineages prior to the development of these structures (2). However, there is strong evidence for the secondary loss of mitochondria in E. histolytica, and small-subunit rRNA sequence analyses suggest that it diverged more recently than several lineages with typical eukaryotic features (3,17).…”

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confidence: 95%

Evidence of a Continuous Endoplasmic Reticulum in the Protozoan Parasite Entamoeba histolytica

Teixeira

Huston

2008

Eukaryot Cell

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“…These are dramatically different in their morphology and biology. One of the most striking differences is that D. discoideum is a typical mitochondrion-containing eukaryote, whereas M. balamuthi and E. histolytica are amitochondriate (14)(15)(16)(17). Not surprisingly, the three species are assigned to separate lineages in most taxonomic schemes (3).…”

mentioning

confidence: 99%

The analysis of 100 genes supports the grouping of three highly divergent amoebae: Dictyostelium , Entamoeba , and Mastigamoeba

Bapteste

Brinkmann

Lee

et al. 2002

Proc. Natl. Acad. Sci. U.S.A.

348

222

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The phylogenetic relationships of amoebae are poorly resolved. To address this difficult question, we have sequenced 1,280 expressed sequence tags from Mastigamoeba balamuthi and assembled a large data set containing 123 genes for representatives of three phenotypically highly divergent major amoeboid lineages: Pelobionta, Entamoebidae, and Mycetozoa. Phylogenetic reconstruction was performed on Ϸ25,000 aa positions for 30 species by using maximum-likelihood approaches. All well-established eukaryotic groups were recovered with high statistical support, validating our approach. Interestingly, the three amoeboid lineages strongly clustered together in agreement with the Conosa hypothesis [as defined by T. Cavalier-Smith (1998) Biol. Rev. Cambridge Philos. Soc. 73, 203-266]. Two amitochondriate amoebae, the free-living Mastigamoeba and the human parasite Entamoeba, formed a significant sister group to the exclusion of the mycetozoan Dictyostelium. This result suggested that a part of the reductive process in the evolution of Entamoeba (e.g., loss of typical mitochondria) occurred in its free-living ancestors. Applying this inexpensive expressed sequence tag approach to many other lineages will surely improve our understanding of eukaryotic evolution.

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Entamoeba histolytica as a model for the primitive eukaryotic cell

Cited by 50 publications

References 23 publications

Evidence for the bacterial origin of genes encoding fermentation enzymes of the amitochondriate protozoan parasite Entamoeba histolytica

Evidence for the bacterial origin of genes encoding fermentation enzymes of the amitochondriate protozoan parasite Entamoeba histolytica

Evidence of a Continuous Endoplasmic Reticulum in the Protozoan Parasite Entamoeba histolytica

The analysis of 100 genes supports the grouping of three highly divergent amoebae: Dictyostelium , Entamoeba , and Mastigamoeba

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