Reinventing an Organelle: The Reduced Mitochondrion in Parasitic Protists

Santos, Herbert J.; Makiuchi, Takashi; Nozaki, Tomoyoshi

doi:10.1016/j.pt.2018.08.008

Cited by 51 publications

(53 citation statements)

References 143 publications

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“…However, most studies have focused on investigations of anaerobic forms of mitochondria. Genomic and transcriptomic analyses of parasitic, endosymbiotic, and free-living protists revealed a functional continuum from strictly oxygen-dependent mitochondria via mitochondria of facultatively anaerobic organisms adapted to an anaerobic lifestyle to various extents to highly reduced mitosomes in parasitic species (64,65). In contrast, peroxisomes were considered to be present in aerobes and absent in anaerobes based on few examples of anaerobic protists, such as Trichomonas vaginalis, G. intestinalis, and E. histolytica, in which peroxisomes have not been found (2,66,67).…”

Section: Discussionmentioning

confidence: 99%

Anaerobic peroxisomes in Mastigamoeba balamuthi

Lê

Žárský

Nývltová

et al. 2020

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

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The adaptation of eukaryotic cells to anaerobic conditions is reflected by substantial changes to mitochondrial metabolism and functional reduction. Hydrogenosomes belong among the most modified mitochondrial derivative and generate molecular hydrogen concomitant with ATP synthesis. The reduction of mitochondria is frequently associated with loss of peroxisomes, which compartmentalize pathways that generate reactive oxygen species (ROS) and thus protect against cellular damage. The biogenesis and function of peroxisomes are tightly coupled with mitochondria. These organelles share fission machinery components, oxidative metabolism pathways, ROS scavenging activities, and some metabolites. The loss of peroxisomes in eukaryotes with reduced mitochondria is thus not unexpected. Surprisingly, we identified peroxisomes in the anaerobic, hydrogenosome-bearing protist Mastigamoeba balamuthi. We found a conserved set of peroxin (Pex) proteins that are required for protein import, peroxisomal growth, and division. Key membrane-associated Pexs (MbPex3, MbPex11, and MbPex14) were visualized in numerous vesicles distinct from hydrogenosomes, the endoplasmic reticulum (ER), and Golgi complex. Proteomic analysis of cellular fractions and prediction of peroxisomal targeting signals (PTS1/PTS2) identified 51 putative peroxisomal matrix proteins. Expression of selected proteins in Saccharomyces cerevisiae revealed specific targeting to peroxisomes. The matrix proteins identified included components of acyl-CoA and carbohydrate metabolism and pyrimidine and CoA biosynthesis, whereas no components related to either β-oxidation or catalase were present. In conclusion, we identified a subclass of peroxisomes, named “anaerobic” peroxisomes that shift the current paradigm and turn attention to the reductive evolution of peroxisomes in anaerobic organisms.

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Section: Discussionmentioning

confidence: 99%

Anaerobic peroxisomes in Mastigamoeba balamuthi

Lê

Žárský

Nývltová

et al. 2020

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

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“…SLP enables the synthesis of energy without the need of O 2 , hence devoid of the liberation of ROS ( Fig. 3) [24][25][26].…”

Section: Oxidative and Nitrosative Stressmentioning

confidence: 99%

Metabolic manipulation by Pseudomonas fluorescens: a powerful stratagem against oxidative and metal stress

MacLean

Bley

Appanna

2020

Journal of Medical Microbiology

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Metabolism is the foundation of all living organisms and is at the core of numerous if not all biological processes. The ability of an organism to modulate its metabolism is a central characteristic needed to proliferate, to be dormant and to survive any assault. Pseudomonas fluorescens is bestowed with a uniquely versatile metabolic framework that enables the microbe to adapt to a wide range of conditions including disparate nutrients and toxins. In this mini-review we elaborate on the various metabolic reconfigurations evoked by this microbial system to combat reactive oxygen/nitrogen species and metal stress. The fine-tuning of the NADH/NADPH homeostasis coupled with the production of α-keto-acids and ATP allows for the maintenance of a reductive intracellular milieu. The metabolic networks propelling the synthesis of metabolites like oxalate and aspartate are critical to keep toxic metals at bay. The biochemical processes resulting from these defensive mechanisms provide molecular clues to thwart infectious microbes and reveal elegant pathways to generate value-added products.

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“…Two billion years of coevolution have established a complete co-dependence between the host archaeon and its endosymbiont of α-proteobacterial origin, presently known as the mitochondrion [1]. Cells depend on their mitochondria for a multitude of functions including aerobic respiration and metabolisms of carbohydrates, lipids, and amino acids [2]. Mitochondria contain DNA, however, almost all endosymbiont genes encoding mitochondrial proteins have been relocated to the host nuclear genome [3], thereby making them reliant on their host's protein synthesis machinery which occurs in the cytosol.…”

Section: Introductionmentioning

confidence: 99%

“…Reductive evolution and diversification of mitochondria into mitochondrion-related organelles (MROs) occurred in some eukaryotes that inhabit anaerobic or hypoxic niches as a consequence of oxygen-independent respiration and metabolisms [2]. Mitosomes constitute one of the five classes of mitochondria [16] and are present in a few anaerobic protozoan parasites such as Entamoeba histolytica, Giardia intestinalis, and Cryptosporidium parvum.…”

Section: Introductionmentioning

confidence: 99%

“…Mitosomes constitute one of the five classes of mitochondria [16] and are present in a few anaerobic protozoan parasites such as Entamoeba histolytica, Giardia intestinalis, and Cryptosporidium parvum. A comparison with other MROs has shown that mitosomes retain the most minimal components and functions associated with canonical aerobic mitochondria because they lack genomic DNA, cristae structure, the electron transfer chain, and the ability to synthesize ATP [2,12]. In E. histolytica, mitosomes contain enzymes involved in the sulfate activation pathway, a process which usually takes place in the cytoplasm or plastids of other organisms [17].…”

Section: Introductionmentioning

confidence: 99%

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Import of Entamoeba histolytica Mitosomal ATP Sulfurylase Relies on Internal Targeting Sequences

et al. 2020

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Mitochondrial matrix proteins synthesized in the cytosol often contain amino (N)-terminal targeting sequences (NTSs), or alternately internal targeting sequences (ITSs), which enable them to be properly translocated to the organelle. Such sequences are also required for proteins targeted to mitochondrion-related organelles (MROs) that are present in a few species of anaerobic eukaryotes. Similar to other MROs, the mitosomes of the human intestinal parasite Entamoeba histolytica are highly degenerate, because a majority of the components involved in various processes occurring in the canonical mitochondria are either missing or modified. As of yet, sulfate activation continues to be the only identified role of the relic mitochondria of Entamoeba. Mitosomes influence the parasitic nature of E. histolytica, as the downstream cytosolic products of sulfate activation have been reported to be essential in proliferation and encystation. Here, we investigated the position of the targeting sequence of one of the mitosomal matrix enzymes involved in the sulfate activation pathway, ATP sulfurylase (AS). We confirmed by immunofluorescence assay and subcellular fractionation that hemagluttinin (HA)-tagged EhAS was targeted to mitosomes. However, its ortholog in the δ-proteobacterium Desulfovibrio vulgaris, expressed as DvAS-HA in amoebic trophozoites, indicated cytosolic localization, suggesting a lack of recognizable mitosome targeting sequence in this protein. By expressing chimeric proteins containing swapped sequences between EhAS and DvAS in amoebic cells, we identified the ITSs responsible for mitosome targeting of EhAS. This observation is similar to other parasitic protozoans that harbor MROs, suggesting a convergent feature among various MROs in favoring ITS for the recognition and translocation of targeted proteins.

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Reinventing an Organelle: The Reduced Mitochondrion in Parasitic Protists

Cited by 51 publications

References 143 publications

Anaerobic peroxisomes in Mastigamoeba balamuthi

Anaerobic peroxisomes in Mastigamoeba balamuthi

Metabolic manipulation by Pseudomonas fluorescens: a powerful stratagem against oxidative and metal stress

Import of Entamoeba histolytica Mitosomal ATP Sulfurylase Relies on Internal Targeting Sequences

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