The [FeFe] hydrogenase of Nyctotherus ovalis has a chimeric origin

Boxma, Brigitte; Ricard, Guénola; Hoek, Angela H.A.M. van; Severing, Edouard; Staay, Seung-Yeo Moon-van der; Staay, G.W.M. van der; Alen, Theo A. van; Graaf, R.M. de; Cremers, Geert; Kwantes, Michiel; McEwan, Neil R.; Newbold, C. J.; Jouany, J. P.; Michałowski, Tadeusz; Pristaš, Peter; Huynen, Martijn A.; Hackstein, J.H.P.

doi:10.1186/1471-2148-7-230

Cited by 32 publications

(27 citation statements)

References 47 publications

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“…This is consistent with studies of T. vaginalis hydrogenosomes that showed that homologues of these CI subunits (responsible for oxidation of NADH) can reduce ferredoxin that is then oxidized by HYD [23] or possibly even shuttle electrons directly to HYD [24]. Interestingly, other anaerobic protists with MRO-targeted HYDs have retained the same two subunits of CI (figure 3), and in Nyctotherus bacterial homologues of these proteins are fused to HYD [103]. This suggests that coupling of NADH oxidation with H 2 production (ferredoxin) could also occur in these organisms [18].…”

Section: (C) a New Scenariosupporting

confidence: 88%

Diversity and origins of anaerobic metabolism in mitochondria and related organelles

Stairs

Leger

Roger

2015

Phil. Trans. R. Soc. B

135

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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Section: (C) a New Scenariosupporting

confidence: 88%

Diversity and origins of anaerobic metabolism in mitochondria and related organelles

Stairs

Leger

Roger

2015

Phil. Trans. R. Soc. B

135

172

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“…Characterizations of respiratory chain components of this hydrogen-producing organelle uncovered biochemical features characteristic of anaerobic mitochondria (49). Furthermore, the organelle was shown to possess a typical ciliate mitochondrial genome (48,49,101); this finding established once and for all the evolutionary identity of mitochondria and hydrogenosomes as different manifestations of one and the same organelle.…”

Section: Alveolates and Stramenopilesmentioning

confidence: 81%

“…Electron microscopy revealed the presence of methanogenic bacteria in close association with these organelles, which demonstrates the in vivo production of hydrogen in these Nyctotherus organelles (158). The presence of a gene encoding an [Fe]-hydrogenase in the genome of Nyctotherus further indicated hydrogen production (48). On the other hand, the Nyctotherus organelle was shown to contain DNA (7,534).…”

Section: Alveolates and Stramenopilesmentioning

confidence: 99%

“…The potential involvement of NADH in H 2 production, as de- (48). However, not all eukaryotic hydrogenases will be trimeric, because the 51-and 24-kDa subunits of complex I are lacking in some eukaryotic anaerobes (Giardia, for example), but they are present in others.…”

Section: Fig 11mentioning

confidence: 99%

“…The oxidation of NADH in Nyctotherus is thought to occur in part by a truncated electron transport chain in which complex I passes the electrons from NADH through rhodoquinone to complex II, which then uses fumarate as an electron acceptor to produce succinate. Another part of NADH is possibly reoxidized by the [Fe]-hydrogenase, involving the 51-and 24-kDa subunits of complex I that are C-terminally fused to the [Fe]-Hyd catalytic subunit (48,448), thereby releasing molecular hydrogen. The hydrogen-producing mitochondrion of Nyctotherus appears to generate a proton gradient (49), possibly involving complex I of the electron transport chain.…”

Section: Alveolates and Stramenopilesmentioning

confidence: 99%

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Biochemistry and Evolution of Anaerobic Energy Metabolism in Eukaryotes

Müller

Mentel

Hellemond

et al. 2012

Microbiol Mol Biol Rev

695

904

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SUMMARY Major insights into the phylogenetic distribution, biochemistry, and evolutionary significance of organelles involved in ATP synthesis (energy metabolism) in eukaryotes that thrive in anaerobic environments for all or part of their life cycles have accrued in recent years. All known eukaryotic groups possess an organelle of mitochondrial origin, mapping the origin of mitochondria to the eukaryotic common ancestor, and genome sequence data are rapidly accumulating for eukaryotes that possess anaerobic mitochondria, hydrogenosomes, or mitosomes. Here we review the available biochemical data on the enzymes and pathways that eukaryotes use in anaerobic energy metabolism and summarize the metabolic end products that they generate in their anaerobic habitats, focusing on the biochemical roles that their mitochondria play in anaerobic ATP synthesis. We present metabolic maps of compartmentalized energy metabolism for 16 well-studied species. There are currently no enzymes of core anaerobic energy metabolism that are specific to any of the six eukaryotic supergroup lineages; genes present in one supergroup are also found in at least one other supergroup. The gene distribution across lineages thus reflects the presence of anaerobic energy metabolism in the eukaryote common ancestor and differential loss during the specialization of some lineages to oxic niches, just as oxphos capabilities have been differentially lost in specialization to anoxic niches and the parasitic life-style. Some facultative anaerobes have retained both aerobic and anaerobic pathways. Diversified eukaryotic lineages have retained the same enzymes of anaerobic ATP synthesis, in line with geochemical data indicating low environmental oxygen levels while eukaryotes arose and diversified.

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Eukaryotic Microorganisms are Part of Holobionts

Rosenberg

2021

Microbiomes

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The [FeFe] hydrogenase of Nyctotherus ovalis has a chimeric origin

Cited by 32 publications

References 47 publications

Diversity and origins of anaerobic metabolism in mitochondria and related organelles

Diversity and origins of anaerobic metabolism in mitochondria and related organelles

Biochemistry and Evolution of Anaerobic Energy Metabolism in Eukaryotes

Eukaryotic Microorganisms are Part of Holobionts

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