Evidence for a hydrogenosomal-type anaerobic ATP generation pathway in Acanthamoeba castellanii.

Diverse, distantly-related eukaryotic lineages have adapted to low-oxygen environments, and possess mitochondrion-related organelles that have lost the capacity to generate adenosine triphosphate (ATP) through oxidative phosphorylation. A subset of these organelles, hydrogenosomes, has acquired a se...

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Main Authors: Michelle M Leger, Ryan M R Gawryluk, Michael W Gray, Andrew J Roger
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2013-01-01
Series:PLoS ONE
Online Access:https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0069532&type=printable
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author Michelle M Leger
Ryan M R Gawryluk
Michael W Gray
Andrew J Roger
author_facet Michelle M Leger
Ryan M R Gawryluk
Michael W Gray
Andrew J Roger
author_sort Michelle M Leger
collection DOAJ
description Diverse, distantly-related eukaryotic lineages have adapted to low-oxygen environments, and possess mitochondrion-related organelles that have lost the capacity to generate adenosine triphosphate (ATP) through oxidative phosphorylation. A subset of these organelles, hydrogenosomes, has acquired a set of characteristic ATP generation enzymes commonly found in anaerobic bacteria. The recipient of these enzymes could not have survived prior to their acquisition had it not still possessed the electron transport chain present in the ancestral mitochondrion. In the divergence of modern hydrogenosomes from mitochondria, a transitional organelle must therefore have existed that possessed both an electron transport chain and an anaerobic ATP generation pathway. Here, we report a modern analog of this organelle in the habitually aerobic opportunistic pathogen, Acanthamoeba castellanii. This organism possesses a complete set of enzymes comprising a hydrogenosome-like ATP generation pathway, each of which is predicted to be targeted to mitochondria. We have experimentally confirmed the mitochondrial localizations of key components of this pathway using tandem mass spectrometry. This evidence is the first supported by localization and proteome data of a mitochondrion possessing both an electron transport chain and hydrogenosome-like energy metabolism enzymes. Our work provides insight into the first steps that might have occurred in the course of the emergence of modern hydrogenosomes.
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spelling doaj-art-90a1e2b8307542bfa7b6d6389b945b962025-08-20T03:47:05ZengPublic Library of Science (PLoS)PLoS ONE1932-62032013-01-0189e6953210.1371/journal.pone.0069532Evidence for a hydrogenosomal-type anaerobic ATP generation pathway in Acanthamoeba castellanii.Michelle M LegerRyan M R GawrylukMichael W GrayAndrew J RogerDiverse, distantly-related eukaryotic lineages have adapted to low-oxygen environments, and possess mitochondrion-related organelles that have lost the capacity to generate adenosine triphosphate (ATP) through oxidative phosphorylation. A subset of these organelles, hydrogenosomes, has acquired a set of characteristic ATP generation enzymes commonly found in anaerobic bacteria. The recipient of these enzymes could not have survived prior to their acquisition had it not still possessed the electron transport chain present in the ancestral mitochondrion. In the divergence of modern hydrogenosomes from mitochondria, a transitional organelle must therefore have existed that possessed both an electron transport chain and an anaerobic ATP generation pathway. Here, we report a modern analog of this organelle in the habitually aerobic opportunistic pathogen, Acanthamoeba castellanii. This organism possesses a complete set of enzymes comprising a hydrogenosome-like ATP generation pathway, each of which is predicted to be targeted to mitochondria. We have experimentally confirmed the mitochondrial localizations of key components of this pathway using tandem mass spectrometry. This evidence is the first supported by localization and proteome data of a mitochondrion possessing both an electron transport chain and hydrogenosome-like energy metabolism enzymes. Our work provides insight into the first steps that might have occurred in the course of the emergence of modern hydrogenosomes.https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0069532&type=printable
spellingShingle Michelle M Leger
Ryan M R Gawryluk
Michael W Gray
Andrew J Roger
Evidence for a hydrogenosomal-type anaerobic ATP generation pathway in Acanthamoeba castellanii.
PLoS ONE
title Evidence for a hydrogenosomal-type anaerobic ATP generation pathway in Acanthamoeba castellanii.
title_full Evidence for a hydrogenosomal-type anaerobic ATP generation pathway in Acanthamoeba castellanii.
title_fullStr Evidence for a hydrogenosomal-type anaerobic ATP generation pathway in Acanthamoeba castellanii.
title_full_unstemmed Evidence for a hydrogenosomal-type anaerobic ATP generation pathway in Acanthamoeba castellanii.
title_short Evidence for a hydrogenosomal-type anaerobic ATP generation pathway in Acanthamoeba castellanii.
title_sort evidence for a hydrogenosomal type anaerobic atp generation pathway in acanthamoeba castellanii
url https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0069532&type=printable
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