A unique ferredoxin acts as a player in the low-iron response of photosynthetic organisms

Schorsch, Michael; Krämer, Manuela; Goss, Tatjana; Eisenhut, Marion; Robinson, Nigel J.; Osman, Deenah; Wilde, Annegret; Sadaf, Shamaila; Brückler, Hendrik; Walder, Lorenz; Scheibe, Renate; Hase, Toshiharu; Hanke, Guy

doi:10.1073/pnas.1810379115

Cited by 30 publications

(30 citation statements)

References 60 publications

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“…Fdx2 ( sll138 ) has an E m of −243 mV ( 28 ), similar to the E m of the Fld semiquinone. Notably, Fdx2 has a unique intracellular role compared with Fdx1 in mediating iron homeostasis and chlorophyll accumulation, and it is conserved in photosynthetic microbes ( 27 , 29 ).…”

Section: Resultsmentioning

confidence: 92%

The structure and reactivity of the HoxEFU complex from the cyanobacterium Synechocystis sp. PCC 6803

Artz

Tokmina‐Lukaszewska

Mulder

et al. 2020

Journal of Biological Chemistry

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Cyanobacterial Hox is a [NiFe] hydrogenase that consists of the hydrogen (H2)-activating subunits HoxYH, which form a complex with the HoxEFU assembly to mediate reactions with soluble electron carriers like NAD(P)H and ferredoxin (Fdx), thereby coupling photosynthetic electron transfer to energy-transforming catalytic reactions. Researchers studying the HoxEFUYH complex have observed that HoxEFU can be isolated independently of HoxYH, leading to the hypothesis that HoxEFU is a distinct functional subcomplex rather than an artifact of Hox complex isolation. Moreover, outstanding questions about the reactivity of Hox with natural substrates and the site(s) of substrate interactions and coupling of H2, NAD(P)H, and Fdx remain to be resolved. To address these questions, here we analyzed recombinantly produced HoxEFU by electron paramagnetic resonance spectroscopy and kinetic assays with natural substrates. The purified HoxEFU subcomplex catalyzed electron transfer reactions among NAD(P)H, flavodoxin, and several ferredoxins, thus functioning in vitro as a shuttle among different cyanobacterial pools of reducing equivalents. Both Fdx1-dependent reductions of NAD+ and NADP+ were cooperative. HoxEFU also catalyzed the flavodoxin-dependent reduction of NAD(P)+, Fdx2-dependent oxidation of NADH and Fdx4- and Fdx11-dependent reduction of NAD+. MS-based mapping identified an Fdx1-binding site at the junction of HoxE and HoxF, adjacent to iron-sulfur (FeS) clusters in both subunits. Overall, the reactivity of HoxEFU observed here suggests that it functions in managing peripheral electron flow from photosynthetic electron transfer, findings that reveal detailed insights into how ubiquitous cellular components may be used to allocate energy flow into specific bioenergetic products.

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Section: Resultsmentioning

confidence: 92%

The structure and reactivity of the HoxEFU complex from the cyanobacterium Synechocystis sp. PCC 6803

Artz

Tokmina‐Lukaszewska

Mulder

et al. 2020

Journal of Biological Chemistry

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“…Fed2 from Syn. 6803, which was found to be involved in the response to changing environmental iron concentrations [13], as well as Fd3 from T. elongatus. All Fds from this branch contain a Cterminal extension (Supp.…”

Section: Phylogeny Of Cyanobacterial Fdsmentioning

confidence: 99%

“…The phylogenetic analysis of most cyanobacterial Fds revealed that residues Ser/Val of the to play a role in the response to low-level iron, possibly related to its specific C-terminal extension [13]. Unfortunately, no Fd from this group has been studied so far structurally, although one gene copy of such Fd is present in each cyanobacterial strain sequenced to date.…”

Section: Discrimination Of Fd2 Against Fnrmentioning

confidence: 99%

“…Very recently, Fed2 from Syn. 6803 corresponding to Fd3 from T. elongatus has been shown to have a high redox potential (at -243 mV) and not involved in photosynthetic electron transport, but in the response to changing environmental iron concentrations [13]. Data on the structure-function relationships of other minor Fds are lacking for a better understanding of their physiological roles and of the molecular mechanisms that eventually govern the transfer of photosynthetic electrons to different metabolic pathways.…”

Section: Introductionmentioning

confidence: 99%

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An alternative plant-like cyanobacterial ferredoxin with unprecedented structural and functional properties

Motomura

Zuccarello

Sétif

et al. 2019

Biochimica et Biophysica Acta (BBA) - Bioenergetics

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Photosynthetic [2Fe-2S] plant-type ferredoxins have a central role in electron transfer between the photosynthetic chain and various metabolic pathways. Several genes are coding for [2Fe-2S] ferredoxins in cyanobacteria, with four in the thermophilic cyanobacterium Thermosynechococcus elongatus. The structure and functional properties of the major ferredoxin Fd1 are well known but data on the other ferredoxins are scarce. We report the structural and functional properties of a novel minor type ferredoxin, Fd2 of T. elongatus, homologous to Fed4 from Synechocystis sp. PCC 6803. Remarkably, the midpoint potential of Fd2, Em =-440 mV, is lower than that of Fd1, Em =-372 mV. However, while Fd2 can efficiently react with photosystem I or nitrite reductase, time-resolved spectroscopy shows that Fd2 has a very low capacity to reduce ferredoxin-NADP + oxidoreductase (FNR). These unique Fd2 properties are discussed in relation with its structure, solved at 1.38 Å resolution. The Fd2 structure significantly differs from other known ferredoxins structures in loop 2, N-terminal region, hydrogen bonding networks and surface charge distributions. UV-Vis, EPR, and Mid-and Far-IR data also show that the electronic properties of the [2Fe-2S] cluster of Fd2 and its interaction with the protein differ from those of Fd1 both in the oxidized and reduced states. The structural analysis allows to propose that valine in the motif Cys 53 ValAsnCys 56 of Fd2 and the specific orientation of Phe72, explain the electron transfer properties of Fd2. Strikingly, the nature of these residues correlates with different phylogenetic groups of cyanobacterial Fds. With its low redox potential and its discrimination against FNR, Fd2 exhibits a unique capacity to direct efficiently photosynthetic electrons to metabolic pathways not dependent on FNR.

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“…6F), thus excluding this possibility. Recently, a cyanobacterial ferredoxin, Fed2, was shown to play a role in iron sensing and regulation of the IsiA antenna protein, a protein which is typically expressed when cells are exposed to low-iron conditions (Schorsch et al 2018). Similar to Fed2, it is possible that CytM plays a regulatory role in the cell, rather than being directly involved in electron transport.…”

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confidence: 99%

Cytochrome c_Mdownscales photosynthesis under photomixotrophy inSynechocystissp. PCC 6803

Solymosi

Muth-Pawlak

Nikkanen

et al. 2019

Preprint

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CytM reduces photosynthesis under photomixotrophy One sentence summaryThe cryptic, highly conserved cytochrome c M completely blocks photosynthesis in Synechocystis under three days of photomixotrophy, possibly by suppressing CO 2 assimilation. AbstractPhotomixotrophy is a metabolic state, which enables photosynthetic microorganisms to simultaneously perform photosynthesis and metabolism of imported organic carbon substrates. This process is complicated in cyanobacteria, since many, including Synechocystis sp. PCC 6803, conduct photosynthesis and respiration in an interlinked thylakoid membrane electron transport chain. Under photomixotrophy, the cell must therefore tightly regulate electron fluxes from photosynthetic and respiratory complexes. In this study, we show via characterization of photosynthetic apparatus and the proteome, that photomixotrophic growth results in a gradual reduction of the plastoquinone pool in wild-type Synechocystis, which fully downscales photosynthesis over three days of growth. This process is circumvented by deleting the gene encoding cytochrome c M (CytM), a cryptic ctype heme protein widespread in cyanobacteria.Δ CytM maintained active photosynthesis over the three day period, demonstrated by high photosynthetic O 2 and CO 2 fluxes and effective yields of Photosystem II and Photosystem I. Overall, this resulted in a higher growth rate than wild-type, which was maintained by accumulation of proteins involved in phosphate and metal uptake, and cofactor biosynthetic enzymes. While the exact role of CytM has not been determined, a mutant deficient in the thylakoid-localised respiratory terminal oxidases and CytM (ΔCox/Cyd/CytM) displayed a similar phenotype under photomixotrophy to Δ CytM, demonstrating that CytM is not transferring electrons to these complexes, which has previously been suggested. In summary, the obtained data suggests that CytM may have a regulatory role in photomixotrophy by reducing the photosynthetic capacity of cells.the intertwined photosynthetic and respiratory electron transport chain, in order to accommodate this new energy source. Results Deletion of CytM confers growth advantage onΔ CytM and Δ Cox/Cyd/CytM in photomixotrophy In order to elucidate the physiological role of CytM and its possible functional association with thylakoid-localised RTOs, we studied the Δ CytM, Δ Cox/Cyd and Δ Cox/Cyd/CytM mutants. Unmarked mutants of Synechocystis lacking CytM were constructed by disrupting the cytM gene (sll1245) in WT (Supplemental Fig. S2) and the Δ CytM nor Δ Cox/Cyd/CytM demonstrated a growth advantage compared to WT and Δ Cox/Cyd, respectively. Under LAHG condition, Δ CytM grew faster than WT as previously reported (Hiraide et al 2015). The Δ Cox/Cyd and Δ Cox/Cyd/CytM mutants were unable to grow under LAHG. Previously it was reported that Cox is indispensable under this condition (Pils et al 1997).

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A unique ferredoxin acts as a player in the low-iron response of photosynthetic organisms

Cited by 30 publications

References 60 publications

The structure and reactivity of the HoxEFU complex from the cyanobacterium Synechocystis sp. PCC 6803

The structure and reactivity of the HoxEFU complex from the cyanobacterium Synechocystis sp. PCC 6803

An alternative plant-like cyanobacterial ferredoxin with unprecedented structural and functional properties

Cytochrome c_Mdownscales photosynthesis under photomixotrophy inSynechocystissp. PCC 6803

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A unique ferredoxin acts as a player in the low-iron response of photosynthetic organisms

Cited by 30 publications

References 60 publications

The structure and reactivity of the HoxEFU complex from the cyanobacterium Synechocystis sp. PCC 6803

The structure and reactivity of the HoxEFU complex from the cyanobacterium Synechocystis sp. PCC 6803

An alternative plant-like cyanobacterial ferredoxin with unprecedented structural and functional properties

Cytochrome cMdownscales photosynthesis under photomixotrophy inSynechocystissp. PCC 6803

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Cytochrome c_Mdownscales photosynthesis under photomixotrophy inSynechocystissp. PCC 6803