Structure of a putative BenF-like porin from Pseudomonas fluorescens Pf-5 at 2.6 A resolution

Sampathkumar, P; Swaminathan, S; Lu, F; Zhao, X; Li, Z; Gilmore, J; Bain, K; Rutter, M E; Gheyi, T; Schwinn, D; Bonanno, J B; Pieper, U; Fajardo, J E; Fiser, A; Almo, S C; Chance, M R; Baker, D; Atwell, S; Thompson, D A; Emtage, J S; Wasserman, S R; Sali, A; Sauder, J M; Burley, S K

doi:10.1002/prot.22829

Title: Structure of a putative BenF-like porin from Pseudomonas fluorescens Pf-5 at 2.6 A resolution

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Abstract

Gram-negative bacteria typically overcome poor permeability of outer membranes through general porins like OmpF and OmpC, which form water-filled transmembrane pores permitting diffusion of hydrophilic molecules with no particular selectivity. Many bacteria lacking such general porins use substrate-specific porins to overcome growth-limiting conditions and facilitate selective transport of metabolites. Exclusive reliance on substrate-specific porins yields lower membrane permeability to small molecules (<600 Da) versus that seen for Escherichia coli. In Pseudomonads, transit of most small molecules across the cell membrane is thought to be mediated by substrate-specific channels of the OprD superfamily. This property explains, at least in part, the high incidence of Pseudomonas aeruginosa antibiotic resistance. High-throughput DNA sequencing of the P. aeruginosa chromosome revealed the presence of 19 genes encoding structurally related, substrate-specific porins (with 30-45% pairwise amino acid sequence identity) that mediate transmembrane passage of small, water-soluble compounds. The OprD superfamily encompasses the eponymous OprD subfamily, which includes 9 P. aeruginosa proteins that convey basic amino acids and carbapenem antibiotics, and the OpdK subfamily, which includes 11 P. aeruginosa proteins that convey aromatic acids and other small aromatic compounds. Genome sequencing of other gram-negative bacteria has revealed additional members of the OprD and OpdK subfamilies in variousmore »« less

Authors:: Sampathkumar, P; Swaminathan, S; Lu, F; Zhao, X; Li, Z; Gilmore, J; Bain, K; Rutter, M E; Gheyi, T; Schwinn, D; Bonanno, J B; Pieper, U; Fajardo, J E; Fiser, A; Almo, S C; Chance, M R; Baker, D; Atwell, S; Thompson, D A; Emtage, J S more »« less

Publication Date:: Mon Nov 01 00:00:00 EDT 2010

Research Org.:: Brookhaven National Lab. (BNL), Upton, NY (United States)

Sponsoring Org.:: ELI LILLY & COMPANY

OSTI Identifier:: 1014327

Report Number(s):: BNL-93987-2010-JA
Journal ID: ISSN 0887-3585; 600301010; TRN: US201111%%280

DOE Contract Number:: DE-AC02-98CH10886

Resource Type:: Journal Article

Journal Name:: Proteins: Structure, Function, Bioinformatics

Additional Journal Information:: Journal Volume: 78; Journal Issue: 14; Journal ID: ISSN 0887-3585

Country of Publication:: United States

Language:: English

Subject:: 59 BASIC BIOLOGICAL SCIENCES; 60 APPLIED LIFE SCIENCES; AMINO ACID SEQUENCE; AMINO ACIDS; ANTIBIOTICS; AROMATICS; AZOTOBACTER; BACTERIA; CARBOXYLIC ACIDS; CATABOLISM; CELL MEMBRANES; CHROMOSOMES; CRYSTAL STRUCTURE; CRYSTALLOGRAPHY; DNA SEQUENCING; ESCHERICHIA COLI; GENES; METABOLITES; PORINS; PROTEINS; PSEUDOMONAS; RESOLUTION; BenF-like; substrate-specific porin; OprD superfamily; OprD subfamily; OpdK subfamily; benzoate; Pseudomonas; integral membrane protein

Citation Formats


                    Sampathkumar, P, Swaminathan, S, Lu, F, Zhao, X, Li, Z, Gilmore, J, Bain, K, Rutter, M E, Gheyi, T, Schwinn, D, Bonanno, J B, Pieper, U, Fajardo, J E, Fiser, A, Almo, S C, Chance, M R, Baker, D, Atwell, S, Thompson, D A, Emtage, J S, Wasserman, S R, Sali, A, Sauder, J M, and Burley, S K. Structure of a putative BenF-like porin from Pseudomonas fluorescens Pf-5 at 2.6 A resolution.  United States: N. p., 2010. 
        Web.  doi:10.1002/prot.22829.

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                    Sampathkumar, P, Swaminathan, S, Lu, F, Zhao, X, Li, Z, Gilmore, J, Bain, K, Rutter, M E, Gheyi, T, Schwinn, D, Bonanno, J B, Pieper, U, Fajardo, J E, Fiser, A, Almo, S C, Chance, M R, Baker, D, Atwell, S, Thompson, D A, Emtage, J S, Wasserman, S R, Sali, A, Sauder, J M, & Burley, S K. Structure of a putative BenF-like porin from Pseudomonas fluorescens Pf-5 at 2.6 A resolution.  United States.  https://doi.org/10.1002/prot.22829

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                    Sampathkumar, P, Swaminathan, S, Lu, F, Zhao, X, Li, Z, Gilmore, J, Bain, K, Rutter, M E, Gheyi, T, Schwinn, D, Bonanno, J B, Pieper, U, Fajardo, J E, Fiser, A, Almo, S C, Chance, M R, Baker, D, Atwell, S, Thompson, D A, Emtage, J S, Wasserman, S R, Sali, A, Sauder, J M, and Burley, S K. 2010.  
        "Structure of a putative BenF-like porin from Pseudomonas fluorescens Pf-5 at 2.6 A resolution".  United States.  https://doi.org/10.1002/prot.22829.

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@article{osti_1014327,

  title        = {Structure of a putative BenF-like porin from Pseudomonas fluorescens Pf-5 at 2.6 A resolution},

  author       = {Sampathkumar, P and Swaminathan, S and Lu, F and Zhao, X and Li, Z and Gilmore, J and Bain, K and Rutter, M E and Gheyi, T and Schwinn, D and Bonanno, J B and Pieper, U and Fajardo, J E and Fiser, A and Almo, S C and Chance, M R and Baker, D and Atwell, S and Thompson, D A and Emtage, J S and Wasserman, S R and Sali, A and Sauder, J M and Burley, S K},

  abstractNote = {Gram-negative bacteria typically overcome poor permeability of outer membranes through general porins like OmpF and OmpC, which form water-filled transmembrane pores permitting diffusion of hydrophilic molecules with no particular selectivity. Many bacteria lacking such general porins use substrate-specific porins to overcome growth-limiting conditions and facilitate selective transport of metabolites. Exclusive reliance on substrate-specific porins yields lower membrane permeability to small molecules (<600 Da) versus that seen for Escherichia coli. In Pseudomonads, transit of most small molecules across the cell membrane is thought to be mediated by substrate-specific channels of the OprD superfamily. This property explains, at least in part, the high incidence of Pseudomonas aeruginosa antibiotic resistance. High-throughput DNA sequencing of the P. aeruginosa chromosome revealed the presence of 19 genes encoding structurally related, substrate-specific porins (with 30-45% pairwise amino acid sequence identity) that mediate transmembrane passage of small, water-soluble compounds. The OprD superfamily encompasses the eponymous OprD subfamily, which includes 9 P. aeruginosa proteins that convey basic amino acids and carbapenem antibiotics, and the OpdK subfamily, which includes 11 P. aeruginosa proteins that convey aromatic acids and other small aromatic compounds. Genome sequencing of other gram-negative bacteria has revealed additional members of the OprD and OpdK subfamilies in various organisms, including other pseudomonads. Among the many bacteria in which OprD superfamily members have been identified are P. putida, P. fluorescens Pf-5, P. syringae, and Azotobacter vinelandii, all of which share closely related genes that encode the so-called BenF-like porins. In P. putida, benF is part of an operon involved in benzoate catabolism regulated by benR. Within this operon, benK, benE, and benF genes have been suggested to contribute toward either influx or efflux of benzoate. BLAST analysis of the amino acid sequence of P. fluorescens Pf-5 gene PFL1329 (Uniprot id: http://www.uniprot.org/uniprot/Q4KH25) against P. putida KT2440 strain identified 20 related porins. The top six hits include P. putida KT2440 genes PP1383 (annotated as BenF-like), PP2517 (annotated as BenF-like), and PP3168 (annotated as BenF), which share sequence identities of 76%, 66%, and 44% with PFL1329, respectively. The precise functions of these genes are not yet known. Therefore, we refer to the protein product of gene PFL1329 as PflBenF-like, which reflects its current annotation in the Uniprot database. Crystal structures of OprD and OpdK (vanillate specific porin), both from P. aeruginosa (designated below as PaOprD and PaOpdK, respectively) have been determined. Herein, we report the crystal structure of a putative BenF-like porin from P. fluorescens Pf-5 (PflBenF-like). For the sake of brevity, all subsequent references to the PflBenF-like porin will be made using PflBenF. X-ray crystallography revealed a canonical 18-stranded {beta}-barrel fold that forms a central pore with a diameter of {approx}4.6 E. We describe detailed comparisons of the PflBenF structure with those of PaOprD and PaOpdK.},

  doi          = {10.1002/prot.22829},

  url          = {https://www.osti.gov/biblio/1014327},
  journal      = {Proteins: Structure, Function, Bioinformatics},

  issn         = {0887-3585},

  number       = 14,

  volume       = 78,

  place        = {United States},

  year         = {Mon Nov 01 00:00:00 EDT 2010},

  month        = {Mon Nov 01 00:00:00 EDT 2010}

}

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