Lateral Gene Transfer and Gene Duplication Played a Key Role in the Evolution of Mastigamoeba balamuthi Hydrogenosomes

Nývltová, Eva; Stairs, Courtney W.; Hrdý, Ivan; Rídl, Jakub; Mach, Jan; Pačes, Jan; Roger, Andrew J.; Tachezy, Jan

doi:10.1093/molbev/msu408

Cited by 60 publications

(122 citation statements)

References 59 publications

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“…S7). These findings, together with MRO localizations of two other enzymes in this pathway [AS and inorganic pyrophosphatase (8)], indicate that the sulfate-activation pathway functions in M. balamuthi MROs. However, metabolic labeling shows that, in contrast to Entamoeba, M. balamuthi trophozoites do not produce sulfolipids (Fig.…”

Section: Resultsmentioning

confidence: 83%

“…Mastigamoeba does possess the sulfate-activation pathway in MROs but does not have the capacity for producing sulfolipids, including CS (this study and ref. 8). These results imply that the role of the sulfate-activation pathway has diverged between M. balamuthi and Entamoeba, and thus it is of great importance to unravel the role of the sulfateactivation pathway in Mastigamoeba MROs.…”

Section: Discussionmentioning

confidence: 91%

“…possess MROs, the genomes of these organisms apparently lack genes involved in the sulfate-activation pathway (1). Moreover, phylogenetic analyses revealed that E. histolytica and M. balamuthi appear to have acquired the enzymes in the sulfate-activation pathway from distinct prokaryotic and eukaryotic lineages by LGT (1,8). Therefore sulfate activation is not a conserved function of MROs but may be a unique feature of MROs maintained by the Entamoeba and Mastigamoeba lineages (5).…”

Section: Significancementioning

confidence: 99%

“…MROs are present in a variety of unicellular eukaryotic organisms (2, 4); however, the relationship of sulfate activation to MROs is not clear. In Mastigamoeba balamuthi, a microaerophilic, free-living amoeba, which is a close relative of E. histolytica, the enzymes involved in the sulfate-activation pathway are encoded in the genome, and these proteins possess mitochondrial targeting signals; two of these enzymes are localized in MROs (8). Although other anaerobic/microaerophilic, parasitic organisms, such as Trichomonas vaginalis, Giardia intestinalis, and Cryptosporidium parvum,…”

mentioning

confidence: 99%

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Entamoeba mitosomes play an important role in encystation by association with cholesteryl sulfate synthesis

Mi-ichi

Miyamoto

Takao

et al. 2015

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

114

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Hydrogenosomes and mitosomes are mitochondrion-related organelles (MROs) that have highly reduced and divergent functions in anaerobic/microaerophilic eukaryotes. Entamoeba histolytica, a microaerophilic, parasitic amoebozoan species, which causes intestinal and extraintestinal amoebiasis in humans, possesses mitosomes, the existence and biological functions of which have been a longstanding enigma in the evolution of mitochondria. We previously demonstrated that sulfate activation, which is not generally compartmentalized to mitochondria, is a major function of E. histolytica mitosomes. However, because the final metabolites of sulfate activation remain unknown, the overall scheme of this metabolism and the role of mitosomes in Entamoeba have not been elucidated. In this study we purified and identified cholesteryl sulfate (CS) as a final metabolite of sulfate activation. We then identified the gene encoding the cholesteryl sulfotransferase responsible for synthesizing CS. Addition of CS to culture media increased the number of cysts, the dormant form that differentiates from proliferative trophozoites. Conversely, chlorate, a selective inhibitor of the first enzyme in the sulfate-activation pathway, inhibited cyst formation in a dose-dependent manner. These results indicate that CS plays an important role in differentiation, an essential process for the transmission of Entamoeba between hosts. Furthermore, we show that Mastigamoeba balamuthi, an anaerobic, free-living amoebozoan species, which is a close relative of E. histolytica, also has the sulfate-activation pathway in MROs but does not possess the capacity for CS production. Hence, we propose that a unique function of MROs in Entamoeba contributes to its adaptation to its parasitic life cycle. mitochondrion-related organelles | protist | sulfolipids | differentiation M itochondrion-related organelles (MROs) are derived from canonical mitochondria and are found in a wide range of anaerobic/microaerophilic eukaryotes (1, 2). During the course of evolution MROs have undergone secondary loss of mitochondrial functions; this loss has occurred independently multiple times, resulting in the broad phylogenetic distribution of organisms possessing MROs (2). Furthermore, MROs occasionally acquire novel functions from other organisms by lateral gene transfer (LGT) (1, 3). Hence, MROs are not simply remnants of mitochondria but rather are organelles that display a variety of unique features (1-5).Unique features have been demonstrated in different types of MRO (2-4). Some anaerobic lineages of eukaryotes possess MROs (hydrogenosomes or hydrogen-producing mitochondria) that have remodeled their mitochondria drastically to couple ATP generation with hydrogen production (2-4). Mitosomes, another type of MRO maintained in some organisms that inhabit anaerobic/microaerophilic environments, do not produce ATP or hydrogen and have lost typical mitochondrial functions, such as the tricarboxylic acid (TCA) cycle, electron transport, oxidative phosphorylation, and β-oxidation...

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Section: Resultsmentioning

confidence: 83%

Section: Discussionmentioning

confidence: 91%

Section: Significancementioning

confidence: 99%

mentioning

confidence: 99%

See 2 more Smart Citations

Entamoeba mitosomes play an important role in encystation by association with cholesteryl sulfate synthesis

Mi-ichi

Miyamoto

Takao

et al. 2015

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

114

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“…R. Soc. B 370: 20140326 multiple times in different eukaryote lineages via LGT [34,41,89,90,99,[118][119][120][121].…”

Section: Anaerobic Metabolism: Ancestral or Acquired?mentioning

confidence: 99%

Diversity and origins of anaerobic metabolism in mitochondria and related organelles

Stairs

Leger

Roger

2015

Phil. Trans. R. Soc. B

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134

172

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One contribution of 17 to a theme issue 'Eukaryotic origins: progress and challenges'. Across the diversity of life, organisms have evolved different strategies to thrive in hypoxic environments, and microbial eukaryotes ( protists) are no exception. Protists that experience hypoxia often possess metabolically distinct mitochondria called mitochondrion-related organelles (MROs). While there are some common metabolic features shared between the MROs of distantly related protists, these organelles have evolved independently multiple times across the breadth of eukaryotic diversity. Until recently, much of our knowledge regarding the metabolic potential of different MROs was limited to studies in parasitic lineages. Over the past decade, deep-sequencing studies of free-living anaerobic protists have revealed novel configurations of metabolic pathways that have been co-opted for life in low oxygen environments. Here, we provide recent examples of anaerobic metabolism in the MROs of free-living protists and their parasitic relatives. Additionally, we outline evolutionary scenarios to explain the origins of these anaerobic pathways in eukaryotes.

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Mitochondrion-Related Organelles in Free-Living Protists

Leger

Kolísko

Stairs

et al. 2019

Microbiology Monographs

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Mitochondrion-related organelles (MROs) are a set of functionally diverse organelles that have independently evolved from mitochondria in eukaryotes that live in low-oxygen conditions. These organelles are functionally diverse, possessing a range of ancestrally mitochondrial or horizontally-acquired biochemical pathways. Early studies of MROs focused mainly on parasitic organisms; however, the past decade has seen a growing body of work on the MROs of free-living eukaryotes based on comparative genomics, making it possible to tease apart adaptations to low-oxygen conditions from adaptations to parasitism. Here, we review current knowledge of MROs in free-living eukaryotes. 2

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Lateral Gene Transfer and Gene Duplication Played a Key Role in the Evolution of Mastigamoeba balamuthi Hydrogenosomes

Cited by 60 publications

References 59 publications

Entamoeba mitosomes play an important role in encystation by association with cholesteryl sulfate synthesis

Entamoeba mitosomes play an important role in encystation by association with cholesteryl sulfate synthesis

Diversity and origins of anaerobic metabolism in mitochondria and related organelles

Mitochondrion-Related Organelles in Free-Living Protists

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