Substrate profiling of marine-derived thermotolerant cysteine protease reveals unique cleavage preferences for industrial applications

Abstract Due to their industrial importance, new proteases are constantly being sourced from the marine environment. However, their substrate specificities remain insufficiently studied, restricting the evaluation of their potential applications. Here, we applied multiplex substrate profiling by mas...

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Main Authors: Victoria Røyseth, Brianna M. Hurysz, Hasan Arsın, Julia M. Vazquez, Anna-Karina Kaczorowska, Anita-Elin Fedøy, Daria Biernacka, Sebastian Dorawa, Tadeusz Kaczorowski, Runar Stokke, Anthony J. O’Donoghue, Ida Helene Steen
Format: Article
Language:English
Published: Nature Portfolio 2025-07-01
Series:Scientific Reports
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Online Access:https://doi.org/10.1038/s41598-025-11635-1
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author Victoria Røyseth
Brianna M. Hurysz
Hasan Arsın
Julia M. Vazquez
Anna-Karina Kaczorowska
Anita-Elin Fedøy
Daria Biernacka
Sebastian Dorawa
Tadeusz Kaczorowski
Runar Stokke
Anthony J. O’Donoghue
Ida Helene Steen
author_facet Victoria Røyseth
Brianna M. Hurysz
Hasan Arsın
Julia M. Vazquez
Anna-Karina Kaczorowska
Anita-Elin Fedøy
Daria Biernacka
Sebastian Dorawa
Tadeusz Kaczorowski
Runar Stokke
Anthony J. O’Donoghue
Ida Helene Steen
author_sort Victoria Røyseth
collection DOAJ
description Abstract Due to their industrial importance, new proteases are constantly being sourced from the marine environment. However, their substrate specificities remain insufficiently studied, restricting the evaluation of their potential applications. Here, we applied multiplex substrate profiling by mass spectrometry (MSP-MS) to globupain, a marine thermotolerant clostripain-like protease and show that it has a novel substrate specificity. Globupain is an endopeptidase with a preference for cleavage of substrates on the C-terminal side of norleucine (Nle), Leu, Asn, Arg and Lys. While it can hydrolyze gelatin and collagen, its reaction rate is lower than that of papain, a commercial cysteine protease. The precise knowledge of substrate specificity of globupain led to the discovery that the calpain inhibitors MG101 and leupeptin inactivate globupain activity with IC50 values of 23.79 and 138.7 nM, respectively. Further investigation of additive effects revealed that globupain activity was stimulated by Triton X-100 and Tween 40 at concentrations of up to 1%. Globupain exhibited tolerance to elevated DTT concentrations and retained most of its activity in the presence of Mg2+ or Mn2+ compared to its preferred cation, Ca2+. In conclusion, globupain is a novel clostripain-like cysteine protease with a distinct substrate cleavage profile and remarkable stability in the presence of various additives, highlighting its potential for industrial applications.
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institution Kabale University
issn 2045-2322
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publishDate 2025-07-01
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spelling doaj-art-7b4c19fb10ab47608b75ecd696342b812025-08-20T04:02:46ZengNature PortfolioScientific Reports2045-23222025-07-0115111010.1038/s41598-025-11635-1Substrate profiling of marine-derived thermotolerant cysteine protease reveals unique cleavage preferences for industrial applicationsVictoria Røyseth0Brianna M. Hurysz1Hasan Arsın2Julia M. Vazquez3Anna-Karina Kaczorowska4Anita-Elin Fedøy5Daria Biernacka6Sebastian Dorawa7Tadeusz Kaczorowski8Runar Stokke9Anthony J. O’Donoghue10Ida Helene Steen11Department of Biological Sciences, Center for Deep Sea Research, University of BergenSkaggs School of Pharmacy and Pharmaceutical Sciences, University of CaliforniaDepartment of Biological Sciences, Center for Deep Sea Research, University of BergenSkaggs School of Pharmacy and Pharmaceutical Sciences, University of CaliforniaCollection of Plasmids and Microorganisms | KPD, Faculty of Biology, University of GdańskDepartment of Biological Sciences, Center for Deep Sea Research, University of BergenCollection of Plasmids and Microorganisms | KPD, Faculty of Biology, University of GdańskLaboratory of Extremophiles Biology, Department of Microbiology, Faculty of Biology, University of GdańskLaboratory of Extremophiles Biology, Department of Microbiology, Faculty of Biology, University of GdańskDepartment of Biological Sciences, Center for Deep Sea Research, University of BergenSkaggs School of Pharmacy and Pharmaceutical Sciences, University of CaliforniaDepartment of Biological Sciences, Center for Deep Sea Research, University of BergenAbstract Due to their industrial importance, new proteases are constantly being sourced from the marine environment. However, their substrate specificities remain insufficiently studied, restricting the evaluation of their potential applications. Here, we applied multiplex substrate profiling by mass spectrometry (MSP-MS) to globupain, a marine thermotolerant clostripain-like protease and show that it has a novel substrate specificity. Globupain is an endopeptidase with a preference for cleavage of substrates on the C-terminal side of norleucine (Nle), Leu, Asn, Arg and Lys. While it can hydrolyze gelatin and collagen, its reaction rate is lower than that of papain, a commercial cysteine protease. The precise knowledge of substrate specificity of globupain led to the discovery that the calpain inhibitors MG101 and leupeptin inactivate globupain activity with IC50 values of 23.79 and 138.7 nM, respectively. Further investigation of additive effects revealed that globupain activity was stimulated by Triton X-100 and Tween 40 at concentrations of up to 1%. Globupain exhibited tolerance to elevated DTT concentrations and retained most of its activity in the presence of Mg2+ or Mn2+ compared to its preferred cation, Ca2+. In conclusion, globupain is a novel clostripain-like cysteine protease with a distinct substrate cleavage profile and remarkable stability in the presence of various additives, highlighting its potential for industrial applications.https://doi.org/10.1038/s41598-025-11635-1Marine cysteine proteaseGlobupainClostripainMultiplex substrate profiling by mass spectrometryMarine bioprospectingHydrothermal vents
spellingShingle Victoria Røyseth
Brianna M. Hurysz
Hasan Arsın
Julia M. Vazquez
Anna-Karina Kaczorowska
Anita-Elin Fedøy
Daria Biernacka
Sebastian Dorawa
Tadeusz Kaczorowski
Runar Stokke
Anthony J. O’Donoghue
Ida Helene Steen
Substrate profiling of marine-derived thermotolerant cysteine protease reveals unique cleavage preferences for industrial applications
Scientific Reports
Marine cysteine protease
Globupain
Clostripain
Multiplex substrate profiling by mass spectrometry
Marine bioprospecting
Hydrothermal vents
title Substrate profiling of marine-derived thermotolerant cysteine protease reveals unique cleavage preferences for industrial applications
title_full Substrate profiling of marine-derived thermotolerant cysteine protease reveals unique cleavage preferences for industrial applications
title_fullStr Substrate profiling of marine-derived thermotolerant cysteine protease reveals unique cleavage preferences for industrial applications
title_full_unstemmed Substrate profiling of marine-derived thermotolerant cysteine protease reveals unique cleavage preferences for industrial applications
title_short Substrate profiling of marine-derived thermotolerant cysteine protease reveals unique cleavage preferences for industrial applications
title_sort substrate profiling of marine derived thermotolerant cysteine protease reveals unique cleavage preferences for industrial applications
topic Marine cysteine protease
Globupain
Clostripain
Multiplex substrate profiling by mass spectrometry
Marine bioprospecting
Hydrothermal vents
url https://doi.org/10.1038/s41598-025-11635-1
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