Characterization of a novel thermostable NAD+-dependent formate dehydrogenase from Methylacidiphilum kamchatkense Kam1 (MkaFDH)

Metal-independent NAD+-dependent formate dehydrogenases (FDHs) are enzymes responsible for catalyzing the conversion of formate (HCOO–) to carbon dioxide (CO2), a biological reaction involved in microbial carbon processing and cofactor regeneration. These enzymes show large potential for environment...

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Main Authors: Khouloud Zribi, Matteo Ciciani, Agata Sofia Assunção Carreira, Martina Paganin, Sara Pozzo, Lucio Cinà, Baris Binay, Francesco Secundo, Nicola Segata, Alessandro Provenzani
Format: Article
Language:English
Published: Elsevier 2025-01-01
Series:Current Research in Biotechnology
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Online Access:http://www.sciencedirect.com/science/article/pii/S2590262825000371
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author Khouloud Zribi
Matteo Ciciani
Agata Sofia Assunção Carreira
Martina Paganin
Sara Pozzo
Lucio Cinà
Baris Binay
Francesco Secundo
Nicola Segata
Alessandro Provenzani
author_facet Khouloud Zribi
Matteo Ciciani
Agata Sofia Assunção Carreira
Martina Paganin
Sara Pozzo
Lucio Cinà
Baris Binay
Francesco Secundo
Nicola Segata
Alessandro Provenzani
author_sort Khouloud Zribi
collection DOAJ
description Metal-independent NAD+-dependent formate dehydrogenases (FDHs) are enzymes responsible for catalyzing the conversion of formate (HCOO–) to carbon dioxide (CO2), a biological reaction involved in microbial carbon processing and cofactor regeneration. These enzymes show large potential for environmental bioremediation and biotechnological uses. However, FDHs applications are hampered by the enzymes’ limited stability under extreme conditions, such as high temperatures or extreme pH. Therefore, we aimed to identify and characterize novel metal-independent FDHs with improved activity and thermostability compared to known FDHs. By using four different FDH protein sequences, CtFDH (from Chaetomium thermophilum), MtFDH (from Myceliophthora thermophile), OpFDH (from Ogata parapolymorpha DL-1) and PseFDH (from Pseudomonas sp.101) we retrieved 18,850 FDHs sequences from the NCBI database and matched against the species present in the database of thermophilic bacteria, ThermoBase. Our phylogenetic analysis identified four distinct FDHs in thermophilic bacteria: Methylocaldum szegediense (MszFDH), Methylacidiphilum kamchatkense (MkaFDH), Mycobacterium arosiense (MarFDH) and Mycobacterium genavense (MgeFDH). We selected and characterized the MkaFDH as it was expressed in the thermophilic bacterium with the highest optimum growth (55 °C) among the four bacteria. The MkaFDH was cloned, and the recombinant protein was expressed in E. coli and purified. The conditions for the optimal catalytic activity for formate oxidations were screened and identified, revealing metal-independent, NAD+-restricted activity in phosphate buffer, pH 8. Importantly, the enzyme showed remarkable thermal stability and catalytic activity, showing a melting temperature (Tm) of 60.15 °C, as confirmed by far-UV circular dichroism (CD). Finally, the enzyme showed good thermostability for formate oxidation up to 57.5 °C, and its high catalytic efficiency (kcat/Km = 0.44 s−1mM−1) suggested its potential industrial application. Collectively, we describe here a novel FDH with relevant thermostability that can be exploited as a prototype for industrial applications.
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spelling doaj-art-aa1d1c27fc0a4b91839f996cd6472b032025-08-20T03:24:08ZengElsevierCurrent Research in Biotechnology2590-26282025-01-011010030610.1016/j.crbiot.2025.100306Characterization of a novel thermostable NAD+-dependent formate dehydrogenase from Methylacidiphilum kamchatkense Kam1 (MkaFDH)Khouloud Zribi0Matteo Ciciani1Agata Sofia Assunção Carreira2Martina Paganin3Sara Pozzo4Lucio Cinà5Baris Binay6Francesco Secundo7Nicola Segata8Alessandro Provenzani9Department of Cellular, Computational and Integrative Biology, University of Trento, Trento, ItalyDepartment of Cellular, Computational and Integrative Biology, University of Trento, Trento, ItalyDepartment of Cellular, Computational and Integrative Biology, University of Trento, Trento, ItalyDepartment of Cellular, Computational and Integrative Biology, University of Trento, Trento, Italy“Giulio Natta” Institute of Chemical Sciences and Technologies, National Research Council, Milan, ItalyCicci Research, Grosseto, ItalyGebze Technical University, Gebze,Turkey“Giulio Natta” Institute of Chemical Sciences and Technologies, National Research Council, Milan, ItalyDepartment of Cellular, Computational and Integrative Biology, University of Trento, Trento, ItalyDepartment of Cellular, Computational and Integrative Biology, University of Trento, Trento, Italy; Corresponding author.Metal-independent NAD+-dependent formate dehydrogenases (FDHs) are enzymes responsible for catalyzing the conversion of formate (HCOO–) to carbon dioxide (CO2), a biological reaction involved in microbial carbon processing and cofactor regeneration. These enzymes show large potential for environmental bioremediation and biotechnological uses. However, FDHs applications are hampered by the enzymes’ limited stability under extreme conditions, such as high temperatures or extreme pH. Therefore, we aimed to identify and characterize novel metal-independent FDHs with improved activity and thermostability compared to known FDHs. By using four different FDH protein sequences, CtFDH (from Chaetomium thermophilum), MtFDH (from Myceliophthora thermophile), OpFDH (from Ogata parapolymorpha DL-1) and PseFDH (from Pseudomonas sp.101) we retrieved 18,850 FDHs sequences from the NCBI database and matched against the species present in the database of thermophilic bacteria, ThermoBase. Our phylogenetic analysis identified four distinct FDHs in thermophilic bacteria: Methylocaldum szegediense (MszFDH), Methylacidiphilum kamchatkense (MkaFDH), Mycobacterium arosiense (MarFDH) and Mycobacterium genavense (MgeFDH). We selected and characterized the MkaFDH as it was expressed in the thermophilic bacterium with the highest optimum growth (55 °C) among the four bacteria. The MkaFDH was cloned, and the recombinant protein was expressed in E. coli and purified. The conditions for the optimal catalytic activity for formate oxidations were screened and identified, revealing metal-independent, NAD+-restricted activity in phosphate buffer, pH 8. Importantly, the enzyme showed remarkable thermal stability and catalytic activity, showing a melting temperature (Tm) of 60.15 °C, as confirmed by far-UV circular dichroism (CD). Finally, the enzyme showed good thermostability for formate oxidation up to 57.5 °C, and its high catalytic efficiency (kcat/Km = 0.44 s−1mM−1) suggested its potential industrial application. Collectively, we describe here a novel FDH with relevant thermostability that can be exploited as a prototype for industrial applications.http://www.sciencedirect.com/science/article/pii/S2590262825000371Formate dehydrogenase (FDH)Formate oxidationFDH thermostabilityFDH melting pointFDH phylogenetic tree
spellingShingle Khouloud Zribi
Matteo Ciciani
Agata Sofia Assunção Carreira
Martina Paganin
Sara Pozzo
Lucio Cinà
Baris Binay
Francesco Secundo
Nicola Segata
Alessandro Provenzani
Characterization of a novel thermostable NAD+-dependent formate dehydrogenase from Methylacidiphilum kamchatkense Kam1 (MkaFDH)
Current Research in Biotechnology
Formate dehydrogenase (FDH)
Formate oxidation
FDH thermostability
FDH melting point
FDH phylogenetic tree
title Characterization of a novel thermostable NAD+-dependent formate dehydrogenase from Methylacidiphilum kamchatkense Kam1 (MkaFDH)
title_full Characterization of a novel thermostable NAD+-dependent formate dehydrogenase from Methylacidiphilum kamchatkense Kam1 (MkaFDH)
title_fullStr Characterization of a novel thermostable NAD+-dependent formate dehydrogenase from Methylacidiphilum kamchatkense Kam1 (MkaFDH)
title_full_unstemmed Characterization of a novel thermostable NAD+-dependent formate dehydrogenase from Methylacidiphilum kamchatkense Kam1 (MkaFDH)
title_short Characterization of a novel thermostable NAD+-dependent formate dehydrogenase from Methylacidiphilum kamchatkense Kam1 (MkaFDH)
title_sort characterization of a novel thermostable nad dependent formate dehydrogenase from methylacidiphilum kamchatkense kam1 mkafdh
topic Formate dehydrogenase (FDH)
Formate oxidation
FDH thermostability
FDH melting point
FDH phylogenetic tree
url http://www.sciencedirect.com/science/article/pii/S2590262825000371
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