Consensus model of a cyanobacterial light-dependent protochlorophyllide oxidoreductase in its pigment-free apo-form and photoactive ternary complex

Schneidewind, Judith; Krause, Frank; Bocola, Marco; Stadler, Andreas M.; Davari, Mehdi D.; Schwaneberg, Ulrich; Jaeger, Karl‐Erich; Krauß, Ulrich

doi:10.1038/s42003-019-0590-4

Cited by 10 publications

(16 citation statements)

References 76 publications

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“…To rule out that the flexible N-terminal His-tag contributes to the obtained ab initio models, we also included an El LPOR sample, which possessed an eight-amino acid-long His-tag at the C-terminus instead of the N-terminus ( El LPOR-cHis). The corresponding molecular masses estimated from the SAXS data ( table 2 ) are in good agreement with the theoretical molecular masses, indicating that all studied apo LPORs are monomeric, as also previously shown for Te LPOR ( Schneidewind et al. 2019 ).…”

Section: Resultssupporting

confidence: 86%

“…4 , lower panels; see Materials and Methods for details). As previously shown for Te LPOR ( Schneidewind et al. 2019 ), the overall shape of the molecule resembles a bowling-pin appearing to consist of a larger and smaller subdomain ( fig.…”

Section: Resultssupporting

confidence: 75%

“…To identify whether AABP LPORs show a globally conserved structure when compared with cyanobacterial LPORs, we elucidated the solution structure of the apo form (protein without NADPH and Pchlide) of two AAPB LPORs ( Ds LPOR and El LPOR) in comparison to the cyanobacterial Te LPOR ( Schneidewind et al. 2019 ) enzyme by using small-angle X-ray scattering (SAXS).…”

Section: Resultsmentioning

confidence: 99%

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Complex Evolution of Light-Dependent Protochlorophyllide Oxidoreductases in Aerobic Anoxygenic Phototrophs: Origin, Phylogeny, and Function

Chernomor

Peters

Schneidewind

et al. 2020

Molecular Biology and Evolution

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Light-dependent and dark-operative protochlorophyllide oxidoreductases (LPORs and DPORs) are evolutionary and structurally distinct enzymes that are essential for the synthesis of (bacterio)chlorophyll, the primary pigment needed for both anoxygenic and oxygenic photosynthesis. In contrast to the long-held hypothesis that LPORs are only present in oxygenic phototrophs, we recently identified a functional LPOR in the aerobic anoxygenic phototrophic bacterium (AAPB) Dinoroseobacter shibae, and attributed its presence to a single horizontal gene transfer (HGT) event from cyanobacteria. Here, we provide evidence for the more widespread presence of genuine LPOR enzymes in AAPBs. An exhaustive bioinformatics search identified 36 putative LPORs outside of oxygenic phototrophic bacteria (cyanobacteria) with the majority being AAPBs. Using in vitro and in vivo assays, we show that the large majority of the tested AAPB enzymes are genuine LPORs. Solution structural analyses, performed for two of the AAPB LPORs, revealed a globally conserved structure when compared to a well-characterized cyanobacterial LPOR. Phylogenetic analyses suggest that LPORs were transferred not only from cyanobacteria, but also subsequently between proteobacteria and from proteobacteria to Gemmatimonadetes. Our study thus provides another interesting example for the complex evolutionary processes that govern the evolution of bacteria, involving multiple HGT events that likely occurred at different time points and involved different donors.

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Section: Resultssupporting

confidence: 86%

Section: Resultssupporting

confidence: 75%

Section: Resultsmentioning

confidence: 99%

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Complex Evolution of Light-Dependent Protochlorophyllide Oxidoreductases in Aerobic Anoxygenic Phototrophs: Origin, Phylogeny, and Function

Chernomor

Peters

Schneidewind

et al. 2020

Molecular Biology and Evolution

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“…LPOR is encoded by one or several nuclear genes ( POR genes) and uses NADPH as an electron donor in the presence of light for the reduction of the C17-C18 double bond (reviewed in [ 65 ]). The holocomplex is proposed to be dimeric [ 66 ]. The DPOR protein is a complex formed by the L, N and B subunits encoded in the chloroplast genome by the chlL , chlN and chlB genes.…”

Section: Fe-s Protein-dependent Metabolic Processes In Algal Chlormentioning

confidence: 99%

Occurrence, Evolution and Specificities of Iron-Sulfur Proteins and Maturation Factors in Chloroplasts from Algae

Przybyla-Toscano

Couturier

Remacle

et al. 2021

IJMS

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Iron-containing proteins, including iron-sulfur (Fe-S) proteins, are essential for numerous electron transfer and metabolic reactions. They are present in most subcellular compartments. In plastids, in addition to sustaining the linear and cyclic photosynthetic electron transfer chains, Fe-S proteins participate in carbon, nitrogen, and sulfur assimilation, tetrapyrrole and isoprenoid metabolism, and lipoic acid and thiamine synthesis. The synthesis of Fe-S clusters, their trafficking, and their insertion into chloroplastic proteins necessitate the so-called sulfur mobilization (SUF) protein machinery. In the first part, we describe the molecular mechanisms that allow Fe-S cluster synthesis and insertion into acceptor proteins by the SUF machinery and analyze the occurrence of the SUF components in microalgae, focusing in particular on the green alga Chlamydomonas reinhardtii. In the second part, we describe chloroplastic Fe-S protein-dependent pathways that are specific to Chlamydomonas or for which Chlamydomonas presents specificities compared to terrestrial plants, putting notable emphasis on the contribution of Fe-S proteins to chlorophyll synthesis in the dark and to the fermentative metabolism. The occurrence and evolutionary conservation of these enzymes and pathways have been analyzed in all supergroups of microalgae performing oxygenic photosynthesis.

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“…A crystal structure of the ternary complex is not yet available, which has been attributed to the oligomerisation of POR when Pchlide is bound. Oligomerisation has also been observed by mass spectrometry and small‐angle X‐ray scattering [28,29].…”

Section: Introductionmentioning

confidence: 99%

Dual role of the active site ‘lid’ regions of protochlorophyllide oxidoreductase in photocatalysis and plant development

et al. 2020

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Protochlorophyllide oxidoreductase (POR) catalyses reduction of protochlorophyllide (Pchlide) to chlorophyllide, a light-dependent reaction of chlorophyll biosynthesis. POR is also important in plant development as it is the main constituent of prolamellar bodies in etioplast membranes. Prolamellar bodies are highly organised, paracrystalline structures comprising aggregated oligomeric structures of POR-Pchlide-NADPH complexes. How these oligomeric structures are formed and the role of Pchlide in oligomerisation remains unclear. POR crystal structures highlight two peptide regions that form a 'lid' to the active site, and undergo conformational change on binding Pchlide. Here, we show that Pchlide binding triggers formation of large oligomers of POR using size exclusion chromatography. A POR 'octamer' has been isolated and its structure investigated by cryoelectron microscopy at 7.7Å resolution. This structure shows that oligomer formation is most likely driven by the interaction of amino acid residues in the highly conserved lid regions. Computational modelling indicates that Pchlide binding stabilises exposure of hydrophobic surfaces formed by the lid regions, which supports POR dimerisation and ultimately oligomer formation. Studies with variant PORs demonstrate that lid residues are involved in substrate binding and photocatalysis. These highly conserved lid regions therefore have a dual function. The lid residues position Pchlide optimally to enable photocatalysis. Following Pchlide binding, they also enable POR oligomerisationa process that is reversed through subsequent photocatalysis in the early stages of chloroplast development.

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Consensus model of a cyanobacterial light-dependent protochlorophyllide oxidoreductase in its pigment-free apo-form and photoactive ternary complex

Cited by 10 publications

References 76 publications

Complex Evolution of Light-Dependent Protochlorophyllide Oxidoreductases in Aerobic Anoxygenic Phototrophs: Origin, Phylogeny, and Function

Complex Evolution of Light-Dependent Protochlorophyllide Oxidoreductases in Aerobic Anoxygenic Phototrophs: Origin, Phylogeny, and Function

Occurrence, Evolution and Specificities of Iron-Sulfur Proteins and Maturation Factors in Chloroplasts from Algae

Dual role of the active site ‘lid’ regions of protochlorophyllide oxidoreductase in photocatalysis and plant development

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