RNA silencing of hydrogenase(-like) genes and investigation of their physiological roles in the green alga <i>Chlamydomonas reinhardtii</i>

Godman, James; Molnár, Attila; Baulcombe, David C.; Balk, Janneke

doi:10.1042/bj20100932

Cited by 42 publications

(22 citation statements)

References 40 publications

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“…In support of this, we found that CIA1 could rescue the yeast cia1 mutant. Also, the Nar1 homolog of Chlamydomonas reinhardtii is known to be required for the activities of at least two cytosolic Fe-S enzymes, AO and xanthine dehydrogenase (Godman et al, 2010). In addition, insertion mutants of AE7, CIA1, and NAR1 all died at early reproductive or embryo developmental stages.…”

Section: Discussionmentioning

confidence: 99%

The DUF59 Family Gene AE7 Acts in the Cytosolic Iron-Sulfur Cluster Assembly Pathway to Maintain Nuclear Genome Integrity in Arabidopsis

et al. 2012

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Eukaryotic organisms have evolved a set of strategies to safeguard genome integrity, but the underlying mechanisms remain poorly understood. Here, we report that ASYMMETRIC LEAVES1/2 ENHANCER7 (AE7), an Arabidopsis thaliana gene encoding a protein in the evolutionarily conserved Domain of Unknown Function 59 family, participates in the cytosolic ironsulfur (Fe-S) cluster assembly (CIA) pathway to maintain genome integrity. The severe ae7-2 allele is embryo lethal, whereas plants with the weak ae7 (ae7-1) allele are viable but exhibit highly accumulated DNA damage that activates the DNA damage response to arrest the cell cycle. AE7 is part of a protein complex with CIA1, NAR1, and MET18, which are highly conserved in eukaryotes and are involved in the biogenesis of cytosolic and nuclear Fe-S proteins. ae7-1 plants have lower activities of the cytosolic [4Fe-4S] enzyme aconitase and the nuclear [4Fe-4S] enzyme DNA glycosylase ROS1. Additionally, mutations in the gene encoding the mitochondrial ATP binding cassette transporter ATM3/ABCB25, which is required for the activity of cytosolic Fe-S enzymes in Arabidopsis, also result in defective genome integrity similar to that of ae7-1. These results indicate that AE7 is a central member of the CIA pathway, linking plant mitochondria to nuclear genome integrity through assembly of Fe-S proteins.

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Section: Discussionmentioning

confidence: 99%

The DUF59 Family Gene AE7 Acts in the Cytosolic Iron-Sulfur Cluster Assembly Pathway to Maintain Nuclear Genome Integrity in Arabidopsis

et al. 2012

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“…In humans, IOP1 is involved in cytosolic FeS cluster assembly (465). In Chlamydomonas, the IOP homolog is named Hyd3 and also appears to be involved in cytosolic FeS cluster biogenesis (162). Several maturase proteins are required for FeS cluster formation specific for [Fe]-Hyd; these proteins are called HydG and HydEF, the eukaryotic versions of which were first characterized for Chlamydomonas (392).…”

Section: Archaeplastidamentioning

confidence: 99%

“…Narf, also called Nar1 or Hyd3, is a eukaryotespecific derivative of [Fe]-Hyd that has conserved all but one (the H-cluster) of the FeS clusters of [Fe]-Hyd (199) and is present in all eukaryotes sampled so far. In Chlamydomonas, the Hyd3 protein, like its homologs in yeast and humans, is involved in FeS cluster biogenesis (162). This indicates that [Fe]-Hyd was present in the eukaryote common ancestor, where it duplicated to give rise to Narf (Hyd3), which then acquired an essential role in FeS biogenesis that has remained conserved across eukaryotes, even after the loss of the ancestral [Fe]-hydrogenase gene in many oxygenadapted lineages.…”

Section: Anaerobic Energy Metabolism: Present In the Eukaryote Commonmentioning

confidence: 99%

“…Abbreviations: CI to CIV, respiratory complexes I to IV; UQ, ubiquinone; C, cytochrome c; A, ATPase; Fd, ferredoxin; [1], pyruvate:ferredoxin oxidoreductase; [2], acetate:succinate CoA-transferase; [3], succinylCoA synthetase; [4], hydrogenase; [5], malic enzyme; [6], pyruvate dehydrogenase complex. involved in FeS cluster biogenesis (162,199). In addition, the chloroplasts of some eukaryotic algae have been found to produce copious amounts of H 2 under certain conditions, a development of immense biotechnological interest (184,322,323).…”

Section: Introductionmentioning

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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“…HydA2 [18,19], HydA1 being responsible for the major hydrogenase activity under anaerobic conditions [20,21]. To date, two assembly factors (HydEF and HydG) belonging to the "Sadenosylmethionine radical" protein super-family have been proved to be required for the proper maturation of the H-cluster of [FeFe] hydrogenase [22].…”

Section: The Green Algal Model Chlamydomonas Reinhardtii Possesses Twmentioning

confidence: 99%

A novel screening method for hydrogenase-deficient mutants in Chlamydomonas reinhardtii based on in vivo chlorophyll fluorescence and photosystem II quantum yield

Godaux

Emonds-Alt

Berne

et al. 2013

International Journal of Hydrogen Energy

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In Chlamydomonas reinhardtii, prolonged anaerobiosis leads to the expression of enzymes belonging to various fermentative pathways. Among them, oxygen-sensitive hydrogenases (HydA1/2) catalyze the synthesis of molecular hydrogen from protons and reduced ferredoxin in the stroma. In this work, by analyzing wild type and mutants affected in H2 production, we show that maximal PSII photosynthetic electron transfer during the first seconds of illumination after a prolonged darkanaerobiosis period is linearly related to hydrogenase capacity. Based on the specific chlorophyll fluorescence induction kinetics typical of hydrogenase-deficient mutants, we set up an in vivo fluorescence imaging screening protocol allowing to isolate mutants impaired in hydrogenase expression or activity, as well as mutants altered in related metabolic pathways required for energy production in anaerobiosis. Compared to previously described screens for mutants impaired in H2 production, our screening method is remarkably fast, sensitive and non invasive. Out of 3000 clones from a small-sized insertional mutant library, five mutants were isolated and the most affected one was analyzed and shown to be defective for the hydrogenase HydG assembly factor.Pierre Cardol, PhD, FNRS research associate Génétique des microorganismes -Institut de Botanique B22 Boulevard du Rectorat, 27 -Université de Liège-B-4000 Liège, Belgique Tel/Fax +32 4 3663840 e-mail: Pierre.cardol@ulg.ac.be Liège, 07 november 2012 Dear Editor, Please find here enclosed a revised version of our manuscript entitled 'A novel screening method for hydrogenase-deficient mutants in Chlamydomonas reinhardtii based on in vivo chlorophyll fluorescence and photosystem II quantum yield.' that had received a positive feedback from the first round of reviewing.We are grateful to you for having encouraged us to resubmit quickly a modified manuscript. We have addressed all the comments raised by the reviewers on our first submission. A point to point answer has been submitted along with the MS. Main changes are : (i) the addition of a new experimental set of data (hydrogen evolution measurements in all mutant strain and some control experiments) and (ii) all data that were previously not shown are now included in the manuscript in main tables or as supplemental figures.We hope that we have now improved our manuscript so you'll find it suitable for publication in International Journal of Hydrogen Energy. Sincerely yours,On behalf all coauthors, Pierre Cardol *Cover LetterReviewer #1:Major points:I. Please measure and show, respectively, the hydrogenase activity of the wild types or control strains (like respiratory mutants, pfl1-mutant) in your setup. Available literature shows that absolute values can differ significantly depending on exact experimental setup and strain. As the correlation between PSII quantum yield and hydrogenase activity is the major point of your study, this data is essential, and citing hydrogenase activities reported in literature is not sufficient.Answer : the...

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RNA silencing of hydrogenase(-like) genes and investigation of their physiological roles in the green alga Chlamydomonas reinhardtii

Cited by 42 publications

References 40 publications

The DUF59 Family Gene AE7 Acts in the Cytosolic Iron-Sulfur Cluster Assembly Pathway to Maintain Nuclear Genome Integrity in Arabidopsis

The DUF59 Family Gene AE7 Acts in the Cytosolic Iron-Sulfur Cluster Assembly Pathway to Maintain Nuclear Genome Integrity in Arabidopsis

Biochemistry and Evolution of Anaerobic Energy Metabolism in Eukaryotes

A novel screening method for hydrogenase-deficient mutants in Chlamydomonas reinhardtii based on in vivo chlorophyll fluorescence and photosystem II quantum yield

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