Identification of a New Class of 5′-Adenylylsulfate (APS) Reductases from Sulfate-Assimilating Bacteria

Bick, Julie Ann; Dennis, Jonathan J.; Zylstra, Gerben J.; Nowack, Jason; Leustek, Thomas

doi:10.1128/jb.182.1.135-142.2000

Cited by 119 publications

(120 citation statements)

References 27 publications

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“…The enzyme produces sulfite from APS but not from PAPS, and the activity is stimulated by thioredoxin m but is not absolutely dependent on this compound. The reported V max of the Pseudomonas APR, 5.8 mol min Ϫ1 mg Ϫ1 (19), is almost identical to that of the N-domain of APR from Arabidopsis, 5.1 mol min Ϫ1 mg Ϫ1 , 2 being ϳ8 times lower than the V max of recombinant APR from Lemna minor (13). tive site, exactly like the enzyme from higher plants (14).…”

Section: Discussionmentioning

confidence: 85%

“…The properties of APS reductase from P. aeruginosa are very similar to those of the C-terminally truncated plant APR, lacking the thioredoxin-like domain (12,14,19,33). The enzyme produces sulfite from APS but not from PAPS, and the activity is stimulated by thioredoxin m but is not absolutely dependent on this compound.…”

Section: Discussionmentioning

confidence: 86%

“…From the bacterial species included in the phylogenetic analysis (Fig. 2), preferential reduction of APS over PAPS was confirmed in the ␥-proteobacteria Pseudomonas, A. ferrooxidans (34), and A. vinosum (9); ␤-proteobacteria Burkholderia and Ralstonia (19); and ␣-proteobacteria S. meliloti and R. tropici (18). Furthermore, because no homologues of APS kinase are present in the completely sequenced genomes of Neisseria meningitidis (␤-proteobacteria) and Geobacter sulfurreducens (␦-proteobacteria), one can conclude that these species also possess an APS reductase.…”

Section: Discussionmentioning

confidence: 99%

“…the tentative APR cluster: the Archae, Firmicutes, and ␣-proteobacteria. In these organisms, either both APS and PAPS reductase activities were measured or nothing is known about the sulfonucleotide utilized for reduction (9,19). The hypothesis that this large cluster represents APS reductases was strengthened by the cloning of the CysH gene from the APSreducing cyanobacterium Plectonema.…”

Section: Fig 2 Phylogenetic Analysis Of Aps and Paps Reductasesmentioning

confidence: 99%

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The Presence of an Iron-Sulfur Cluster in Adenosine 5′-Phosphosulfate Reductase Separates Organisms Utilizing Adenosine 5′-Phosphosulfate and Phosphoadenosine 5′-Phosphosulfate for Sulfate Assimilation

Kopriva¹,

Büchert

Fritz

et al. 2002

Journal of Biological Chemistry

103

122

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It was generally accepted that plants, algae, and phototrophic bacteria use adenosine 5-phosphosulfate (APS) for assimilatory sulfate reduction, whereas bacteria and fungi use phosphoadenosine 5-phosphosulfate (PAPS). The corresponding enzymes, APS and PAPS reductase, share 25-30% identical amino acids. Phylogenetic analysis of APS and PAPS reductase amino acid sequences from different organisms, which were retrieved from the GenBank TM , revealed two clusters. The first cluster comprised known PAPS reductases from enteric bacteria, cyanobacteria, and yeast. On the other hand, plant APS reductase sequences were clustered together with many bacterial ones, including those from Pseudomonas and Rhizobium. The gene for APS reductase cloned from the APS-reducing cyanobacterium Plectonema also clustered together with the plant sequences, confirming that the two classes of sequences represent PAPS and APS reductases, respectively. Compared with the PAPS reductase, all sequences of the APS reductase cluster contained two additional cysteine pairs homologous to the cysteine residues involved in binding an iron-sulfur cluster in plants. Mö ssbauer analysis revealed that the recombinant APS reductase from Pseudomonas aeruginosa contains a [4Fe-4S] cluster with the same characteristics as the plant enzyme. We conclude, therefore, that the presence of an iron-sulfur cluster determines the APS specificity of the sulfatereducing enzymes and thus separates the APS-and PAPSdependent assimilatory sulfate reduction pathways.For all living organisms, sulfur is an essential element with many different functions. It is found in reduced form in amino acids, peptides, and proteins and in iron-sulfur clusters, lipoic acid, and other cofactors and in oxidized form as sulfonate group-modifying proteins, polysaccharides, and lipids. Reduced sulfur compounds, such as hydrogen sulfide, serve as electron donors for chemotrophic or phototrophic growth in a large and diverse group of Archae and bacteria, including purple and green sulfur bacteria (1). On the other hand, oxidized sulfur compounds such as sulfate can function as a terminal electron acceptor in respiration to support the growth of sulfate-reducing bacteria (2).The majority of sulfur in living organisms is present in the reduced form of organic thiols. For their synthesis, inorganic sulfate is reduced and incorporated into bioorganic compounds in a pathway named assimilatory sulfate reduction. Before reduction, sulfate is activated with ATP to adenosine 5Ј-phosphosulfate (APS), 1 which can subsequently be converted into phosphoadenosine 5Ј-phosphosulfate (PAPS) using a second ATP. Either form of activated sulfate can be reduced to sulfite and reduced further to sulfide by sulfite reductase. Sulfide is incorporated into an activated amino acid acceptor, such as O-acetylserine, O-acetylhomoserine, or O-succinylhomoserine, to form cysteine or homocysteine (3-5).The assimilatory sulfate reduction pathway is present in plants, fungi, and yeast and in a wide range of eubacteria but is mi...

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Section: Discussionmentioning

confidence: 85%

Section: Discussionmentioning

confidence: 86%

Section: Discussionmentioning

confidence: 99%

Section: Fig 2 Phylogenetic Analysis Of Aps and Paps Reductasesmentioning

confidence: 99%

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The Presence of an Iron-Sulfur Cluster in Adenosine 5′-Phosphosulfate Reductase Separates Organisms Utilizing Adenosine 5′-Phosphosulfate and Phosphoadenosine 5′-Phosphosulfate for Sulfate Assimilation

Kopriva¹,

Büchert

Fritz

et al. 2002

Journal of Biological Chemistry

103

122

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“…The metabolic organization of sulfur assimilation varies among plants and microbes ( Fig. 1) (1)(2)(3)(4)(5)(6)(7)(8). In yeast, fungi, and enterobacteria, including Escherichia coli, sulfate is incorporated into adenosine-5′-phosphate (APS), then converted to 3′-phospho-APS (PAPS) as a biologically "activated" compound that is reduced to sulfide (6,7).…”

mentioning

confidence: 99%

Structural basis and evolution of redox regulation in plant adenosine-5′-phosphosulfate kinase

Ravilious

Nguyen

Francois

et al. 2011

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

101

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Adenosine-5′-phosphosulfate (APS) kinase (APSK) catalyzes the phosphorylation of APS to 3′-phospho-APS (PAPS). In Arabidopsis thaliana, APSK is essential for reproductive viability and competes with APS reductase to partition sulfate between the primary and secondary branches of the sulfur assimilatory pathway; however, the biochemical regulation of APSK is poorly understood. The 1.8-Å resolution crystal structure of APSR from A. thaliana (AtAPSK) in complex with β,γ-imidoadenosine-5′-triphosphate, Mg 2+ , and APS provides a view of the Michaelis complex for this enzyme and reveals the presence of an intersubunit disulfide bond between Cys86 and Cys119. Functional analysis of AtAPSK demonstrates that reduction of Cys86-Cys119 resulted in a 17-fold higher k cat / K m and a 15-fold increase in K i for substrate inhibition by APS compared with the oxidized enzyme. The C86A/C119A mutant was kinetically similar to the reduced WT enzyme. Gel-and activity-based titrations indicate that the midpoint potential of the disulfide in AtAPSK is comparable to that observed in APS reductase. Both cysteines are invariant among the APSK from plants, but not other organisms, which suggests redox-control as a unique regulatory feature of the plant APSK. Based on structural, functional, and sequence analyses, we propose that the redox-sensitive APSK evolved after bifurcation of the sulfur assimilatory pathway in the green plant lineage and that changes in redox environment resulting from oxidative stresses may affect partitioning of APS into the primary and secondary thiol metabolic routes by having opposing effects on APSK and APS reductase in plants.enzyme kinetics | sulfur metabolism | X-ray crystallography | metabolic evolution S ulfur is an essential element for all living organisms and is required for the biosynthesis of a diverse array of metabolites and macromolecules (1-4). Plants and prokaryotes are the primary assimilatory organisms that convert inorganic sulfate (SO 4 2− ), the predominant form of environmental sulfur, into physiologically useful forms of sulfur (5, 6). The metabolic organization of sulfur assimilation varies among plants and microbes ( Fig. 1) (1-8). In yeast, fungi, and enterobacteria, including Escherichia coli, sulfate is incorporated into adenosine-5′-phosphate (APS), then converted to 3′-phospho-APS (PAPS) as a biologically "activated" compound that is reduced to sulfide (6, 7). In other sulfate-assimilating bacteria, such as Pseudomonas aeruginosa, APS can be used for reduction of sulfide (8). Plants possess bifurcated thiol metabolism pathways, which may reflect the metabolic needs of sessile organisms adapted to a range of environmental stresses and nutrient fluctuations (Fig. 1) (5). These pathways branch after formation of APS. The primary sulfur metabolic route in plants uses APS as the activated highenergy compound for sulfur reduction and the production of cysteine, which is crucial for the synthesis of proteins, methionine, iron-sulfur clusters, vitamin cofactors, and compounds that prote...

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Electronic Structure, Bonding, Spin Coupling, and Energetics of Polynuclear Iron–Sulfur Clusters – A Broken Symmetry Density Functional Theory Perspective

Hopmann

Pelmenschikov

et al. 2015

Spin States in Biochemistry and Inorganic Chemistry

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Identification of a New Class of 5′-Adenylylsulfate (APS) Reductases from Sulfate-Assimilating Bacteria

Cited by 119 publications

References 27 publications

The Presence of an Iron-Sulfur Cluster in Adenosine 5′-Phosphosulfate Reductase Separates Organisms Utilizing Adenosine 5′-Phosphosulfate and Phosphoadenosine 5′-Phosphosulfate for Sulfate Assimilation

The Presence of an Iron-Sulfur Cluster in Adenosine 5′-Phosphosulfate Reductase Separates Organisms Utilizing Adenosine 5′-Phosphosulfate and Phosphoadenosine 5′-Phosphosulfate for Sulfate Assimilation

Structural basis and evolution of redox regulation in plant adenosine-5′-phosphosulfate kinase

Electronic Structure, Bonding, Spin Coupling, and Energetics of Polynuclear Iron–Sulfur Clusters – A Broken Symmetry Density Functional Theory Perspective

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