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

Abstract

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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Methionine gamma‐lyase: The unique reaction mechanism, physiological roles, and therapeutic applications against infectious diseases and cancers

“…It was proposed that MGL in extant protozoan parasites was acquired by lateral gene transfer, together with the enzymes related to anaerobic energy metabolism (20,49). Interestingly, the origin of MGL in the two parasitic protozoa was not identical (20).…”

The Entamoeba histolytica genome: something old, something new, something borrowed and sex too?

“…More than two decades ago, Reeves defined the fermentation pathway of E. histolytica [11]. During the ensuing years, as specific enzymes in this pathway were identified by molecular tools, it became clear that many of the pathway components resembled prokaryotic enzymes rather than those found within higher eukaryotes [12,13]. This finding led to the concept that lateral gene transfer from prokaryotes provided the enzymes necessary for fermentation and enabled ameba to dispense with mitochondria [13].…”

“…During the ensuing years, as specific enzymes in this pathway were identified by molecular tools, it became clear that many of the pathway components resembled prokaryotic enzymes rather than those found within higher eukaryotes [12,13]. This finding led to the concept that lateral gene transfer from prokaryotes provided the enzymes necessary for fermentation and enabled ameba to dispense with mitochondria [13]. Similar lateral gene transfer events, although apparently from different prokaryotic donors, seem to have occurred in other amitochondriate protozoans, including G. lamblia and the genitourinary pathogen Trichomonas vaginalis.…”