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Title: Structural implications of the C-terminal tail in the catalytic and stability properties of manganese peroxidases from ligninolytic fungi

Journal Article · · Acta Crystallographica. Section D: Biological Crystallography (Online)
 [1];  [2];  [1];  [1];  [1];  [1];  [3];  [1]
  1. Spanish National Research Council (CSIC), Madrid (Spain). Center for Biological Research
  2. Barcelona Supercomputing Center, Barcelona (Spain)
  3. Barcelona Supercomputing Center, Barcelona (Spain); Inst. Catalana de Recerca i Estudis Avancats (ICREA), Barcelona (Spain)
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The genome ofCeriporiopsis subvermisporaincludes 13 manganese peroxidase (MnP) genes representative of the three subfamilies described in ligninolytic fungi, which share an Mn2+-oxidation site and have varying lengths of the C-terminal tail. We expressed short, long and extralong MnPs heterologously and biochemically characterized, and the first structure of an extralong MnP was solved. Its C-terminal tail surrounds the haem-propionate access channel, contributing to Mn2+oxidation by the internal propionate, but prevents the oxidation of 2,2'-azino-bis(3-ethylbenzothiazoline-6-sulfonate) (ABTS), which is only oxidized by short MnPs and by shortened-tail variants from site-directed mutagenesis. Furthermore, the tail, which is anchored by numerous contacts, not only affects the catalytic properties of long/extralong MnPs but is also associated with their high acidic stability. Cd2+binds at the Mn2+-oxidation site and competitively inhibits oxidation of both Mn2+and ABTS. Moreover, mutations blocking the haem-propionate channel prevent substrate oxidation. This agrees with molecular simulations that position ABTS at an electron-transfer distance from the haem propionates of anin silicoshortened-tail form, while it cannot reach this position in the extralong MnP crystal structure. Small differences exist between the long and the extralong MnPs, which do not justify their classification as two different subfamilies, but they significantly differ from the short MnPs, with the presence/absence of the C-terminal tail extension being implicated in these differences.

Research Organization:
USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
Sponsoring Organization:
USDOE
Grant/Contract Number:
AC02-05CH11231
OSTI ID:
1344118
Journal Information:
Acta Crystallographica. Section D: Biological Crystallography (Online), Vol. 70, Issue 12; ISSN 1399-0047
Publisher:
International Union of CrystallographyCopyright Statement
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 28 works
Citation information provided by
Web of Science

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Cited By (10)

Improving the pH-stability of Versatile Peroxidase by Comparative Structural Analysis with a Naturally-Stable Manganese Peroxidase journal October 2015
Description of the first fungal dye-decolorizing peroxidase oxidizing manganese(II) journal May 2015
A secretomic view of woody and nonwoody lignocellulose degradation by Pleurotus ostreatus journal February 2016
Evolutionary convergence in lignin-degrading enzymes journal June 2018
Redesign of a New Manganese Peroxidase Highly Expressed in Pichia pastoris towards a Lignin‐Degrading Versatile Peroxidase journal November 2018
Binding and Catalytic Mechanisms of Veratryl Alcohol Oxidation by Lignin Peroxidase: A Theoretical and Experimental Study journal January 2019
Integrative visual omics of the white-rot fungus Polyporus brumalis exposes the biotechnological potential of its oxidative enzymes for delignifying raw plant biomass journal July 2018
Peroxidase evolution in white-rot fungi follows wood lignin evolution in plants journal August 2019
Experimental recreation of the evolution of lignin-degrading enzymes from the Jurassic to date journal March 2017
Computational Modeling Methods for Understanding the Interaction of Lignin and Its Derivatives with Oxidoreductases as Biocatalysts book March 2018

Figures / Tables (10)

Table 1(p. 3)table Table 1
Figure 1(p. 5)figure Figure 1
Figure 2(p. 6)figure Figure 2
Figure 3(p. 7)figure Figure 3
Figure 4(p. 8)figure Figure 4
Table 2(p. 8)table Table 2
Figure 5(p. 9)figure Figure 5
Figure 6(p. 10)figure Figure 6
Figure 7(p. 10)figure Figure 7
Figure 8(p. 11)figure Figure 8

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Related Subjects

59 BASIC BIOLOGICAL SCIENCES
Ceriporiopsis subvermispora
manganese peroxidase
C-terminal tail