Structural and enzymatic characterization of a nucleoside diphosphate sugar hydrolase from Bdellovibrio bacteriovorus

Andres H. De La Peña; Allison Suarez; Krisna C. Duong-Ly; Andrew J. Schoeffield; Mario A. Pizarro-Dupuy; Melissa Zarr; Silvia A. Pineiro; L. Mario Amzel; Sandra B. Gabelli

doi:10.1371/journal.pone.0141716

Structural and enzymatic characterization of a nucleoside diphosphate sugar hydrolase from Bdellovibrio bacteriovorus

Andres H. De La Peña, Allison Suarez, Krisna C. Duong-Ly, Andrew J. Schoeffield, Mario A. Pizarro-Dupuy, Melissa Zarr, Silvia A. Pineiro, L. Mario Amzel, Sandra B. Gabelli

School of Medicine

Research output: Contribution to journal › Article › peer-review

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Abstract

Given the broad range of substrates hydrolyzed by Nudix (nucleoside diphosphate linked to X) enzymes, identification of sequence and structural elements that correctly predict a Nudix substrate or characterize a family is key to correctly annotate the myriad of Nudix enzymes. Here, we present the structure determination and characterization of Bd3179 - a Nudix hydrolase from Bdellovibrio bacteriovorus-that we show localized in the periplasmic space of this obligate Gram-negative predator. We demonstrate that the enzyme is a nucleoside diphosphate sugar hydrolase (NDPSase) and has a high degree of sequence and structural similarity to a canonical ADP-ribose hydrolase and to a nucleoside diphosphate sugar hydrolase (1.4 and 1.3 Å Cα RMSD respectively). Examination of the structural elements conserved in both types of enzymes confirms that an aspartate-X-lysine motif on the C-terminal helix of the α-β-α NDPSase fold differentiates NDPSases from ADPRases.

Original language	English (US)
Article number	e141716
Journal	PloS one
Volume	10
Issue number	11
DOIs	https://doi.org/10.1371/journal.pone.0141716
State	Published - Nov 2 2015

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@article{a04e30bc0d724b99afebf17e6c98350d,

title = "Structural and enzymatic characterization of a nucleoside diphosphate sugar hydrolase from Bdellovibrio bacteriovorus",

abstract = "Given the broad range of substrates hydrolyzed by Nudix (nucleoside diphosphate linked to X) enzymes, identification of sequence and structural elements that correctly predict a Nudix substrate or characterize a family is key to correctly annotate the myriad of Nudix enzymes. Here, we present the structure determination and characterization of Bd3179 - a Nudix hydrolase from Bdellovibrio bacteriovorus-that we show localized in the periplasmic space of this obligate Gram-negative predator. We demonstrate that the enzyme is a nucleoside diphosphate sugar hydrolase (NDPSase) and has a high degree of sequence and structural similarity to a canonical ADP-ribose hydrolase and to a nucleoside diphosphate sugar hydrolase (1.4 and 1.3 {\AA} Cα RMSD respectively). Examination of the structural elements conserved in both types of enzymes confirms that an aspartate-X-lysine motif on the C-terminal helix of the α-β-α NDPSase fold differentiates NDPSases from ADPRases.",

author = "{De La Pe{\~n}a}, {Andres H.} and Allison Suarez and Duong-Ly, {Krisna C.} and Schoeffield, {Andrew J.} and Pizarro-Dupuy, {Mario A.} and Melissa Zarr and Pineiro, {Silvia A.} and Amzel, {L. Mario} and Gabelli, {Sandra B.}",

note = "Funding Information: Data collection was carried out partially at beam line X4A at NSLS, Brookhaven National Laboratory which is supported by the US Department of energy under contract No. DE AC02-98CH10886.We acknowledge the use and services of the JHU SOM Mass Spectrometry and Proteomics Core, supported by NIH NIDDK center grant P30 DK089502. We thank Carol Cooke for the preparation of immunoelectron microscopy samples and collection of images. Special thanks to Dr. Maurice J. Bessman for introducing us to the Nudix enzymes. SBG is an Alexander and Margaret Stewart trust fellow. ",

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doi = "10.1371/journal.pone.0141716",

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T1 - Structural and enzymatic characterization of a nucleoside diphosphate sugar hydrolase from Bdellovibrio bacteriovorus

AU - De La Peña, Andres H.

AU - Suarez, Allison

AU - Duong-Ly, Krisna C.

AU - Schoeffield, Andrew J.

AU - Pizarro-Dupuy, Mario A.

AU - Zarr, Melissa

AU - Pineiro, Silvia A.

AU - Amzel, L. Mario

AU - Gabelli, Sandra B.

N1 - Funding Information: Data collection was carried out partially at beam line X4A at NSLS, Brookhaven National Laboratory which is supported by the US Department of energy under contract No. DE AC02-98CH10886.We acknowledge the use and services of the JHU SOM Mass Spectrometry and Proteomics Core, supported by NIH NIDDK center grant P30 DK089502. We thank Carol Cooke for the preparation of immunoelectron microscopy samples and collection of images. Special thanks to Dr. Maurice J. Bessman for introducing us to the Nudix enzymes. SBG is an Alexander and Margaret Stewart trust fellow.

PY - 2015/11/2

Y1 - 2015/11/2

N2 - Given the broad range of substrates hydrolyzed by Nudix (nucleoside diphosphate linked to X) enzymes, identification of sequence and structural elements that correctly predict a Nudix substrate or characterize a family is key to correctly annotate the myriad of Nudix enzymes. Here, we present the structure determination and characterization of Bd3179 - a Nudix hydrolase from Bdellovibrio bacteriovorus-that we show localized in the periplasmic space of this obligate Gram-negative predator. We demonstrate that the enzyme is a nucleoside diphosphate sugar hydrolase (NDPSase) and has a high degree of sequence and structural similarity to a canonical ADP-ribose hydrolase and to a nucleoside diphosphate sugar hydrolase (1.4 and 1.3 Å Cα RMSD respectively). Examination of the structural elements conserved in both types of enzymes confirms that an aspartate-X-lysine motif on the C-terminal helix of the α-β-α NDPSase fold differentiates NDPSases from ADPRases.

AB - Given the broad range of substrates hydrolyzed by Nudix (nucleoside diphosphate linked to X) enzymes, identification of sequence and structural elements that correctly predict a Nudix substrate or characterize a family is key to correctly annotate the myriad of Nudix enzymes. Here, we present the structure determination and characterization of Bd3179 - a Nudix hydrolase from Bdellovibrio bacteriovorus-that we show localized in the periplasmic space of this obligate Gram-negative predator. We demonstrate that the enzyme is a nucleoside diphosphate sugar hydrolase (NDPSase) and has a high degree of sequence and structural similarity to a canonical ADP-ribose hydrolase and to a nucleoside diphosphate sugar hydrolase (1.4 and 1.3 Å Cα RMSD respectively). Examination of the structural elements conserved in both types of enzymes confirms that an aspartate-X-lysine motif on the C-terminal helix of the α-β-α NDPSase fold differentiates NDPSases from ADPRases.

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Structural and enzymatic characterization of a nucleoside diphosphate sugar hydrolase from Bdellovibrio bacteriovorus

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