Characterization of a consensus-designed trans-cinnamic acid decarboxylase for styrene biosynthesis

ABSTRACT Microbial biosynthesis of aromatic compounds offers significant advantages over petrochemical methods, which rely on fossil fuels and high energy inputs. Microbial fermentations occur at room temperature and ambient pressure, reducing carbon emissions and energy consumption by up to 90%. Ge...

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Main Authors: Ana García-Franco, Jesús de la Torre, Patricia Godoy, Estrella Duque, Carmen López, José A. Gavira, Juan L. Ramos
Format: Article
Language:English
Published: American Society for Microbiology 2025-06-01
Series:mBio
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Online Access:https://journals.asm.org/doi/10.1128/mbio.00714-25
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author Ana García-Franco
Jesús de la Torre
Patricia Godoy
Estrella Duque
Carmen López
José A. Gavira
Juan L. Ramos
author_facet Ana García-Franco
Jesús de la Torre
Patricia Godoy
Estrella Duque
Carmen López
José A. Gavira
Juan L. Ramos
author_sort Ana García-Franco
collection DOAJ
description ABSTRACT Microbial biosynthesis of aromatic compounds offers significant advantages over petrochemical methods, which rely on fossil fuels and high energy inputs. Microbial fermentations occur at room temperature and ambient pressure, reducing carbon emissions and energy consumption by up to 90%. Genetic engineering of microbial chassis is key to optimizing biosynthetic processes, enabling efficient production of aromatic compounds from sugars. However, the intrinsic toxicity of these compounds presents challenges. Pseudomonas putida DOT-T1E, known for its tolerance to solvents, is ideal for producing toxic compounds. Styrene biosynthesis involves converting phenylalanine into trans-cinnamate via phenylalanine ammonia lyase enzymes, followed by decarboxylation to styrene. This second step is challenging, as trans-cinnamate decarboxylases have only been described in fungi. PSC1, a consensus protein designed from multiple alignments of fungal ferulate decarboxylases, enables styrene production in Pseudomonas. PSC1 is a globular dimer with a molecular mass of 104.7 kDa, high thermal stability (Tm 63°C), and activity at temperatures up to 50°C. The crystal structure of PSC1, determined at 2.1 Å, reveals a homodimer with three domains per monomer. A hydrophobic pocket in domain 2, essential for cofactor and substrate binding, was identified. Mutagenesis shows that Arg175, Glu280, and Glu285 are critical for catalysis, as replacing them with alanine abolished the decarboxylation.IMPORTANCEThe petrochemical industry is highly polluting due to its use of extremely high temperatures, high pressure, and toxic catalysts. Synthetic biology offers an alternative by enabling the production of many chemicals through cell factories that operate at room temperature and ambient pressure, potentially reducing CO2 emissions by up to 90%. We have engineered a solvent-tolerant Pseudomonas strain to produce styrene from L-phenylalanine in a two-step process. For the second step, we designed a de novo consensus protein that operates efficiently. In this study, we present its physico-chemical properties and unveil its 3D structure.
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spelling doaj-art-e6851681bde948f59f162d0912b07a2a2025-08-20T02:23:12ZengAmerican Society for MicrobiologymBio2150-75112025-06-0116610.1128/mbio.00714-25Characterization of a consensus-designed trans-cinnamic acid decarboxylase for styrene biosynthesisAna García-Franco0Jesús de la Torre1Patricia Godoy2Estrella Duque3Carmen López4José A. Gavira5Juan L. Ramos6Estación Experimental del Zaidín, Consejo Superior de Investigaciones Científicas, Granada, SpainEstación Experimental del Zaidín, Consejo Superior de Investigaciones Científicas, Granada, SpainEstación Experimental del Zaidín, Consejo Superior de Investigaciones Científicas, Granada, SpainEstación Experimental del Zaidín, Consejo Superior de Investigaciones Científicas, Granada, SpainInstituto Andaluz de Ciencias de la Tierra, Consejo Superior de Investigaciones Científicas, Armilla, SpainInstituto Andaluz de Ciencias de la Tierra, Consejo Superior de Investigaciones Científicas, Armilla, SpainEstación Experimental del Zaidín, Consejo Superior de Investigaciones Científicas, Granada, SpainABSTRACT Microbial biosynthesis of aromatic compounds offers significant advantages over petrochemical methods, which rely on fossil fuels and high energy inputs. Microbial fermentations occur at room temperature and ambient pressure, reducing carbon emissions and energy consumption by up to 90%. Genetic engineering of microbial chassis is key to optimizing biosynthetic processes, enabling efficient production of aromatic compounds from sugars. However, the intrinsic toxicity of these compounds presents challenges. Pseudomonas putida DOT-T1E, known for its tolerance to solvents, is ideal for producing toxic compounds. Styrene biosynthesis involves converting phenylalanine into trans-cinnamate via phenylalanine ammonia lyase enzymes, followed by decarboxylation to styrene. This second step is challenging, as trans-cinnamate decarboxylases have only been described in fungi. PSC1, a consensus protein designed from multiple alignments of fungal ferulate decarboxylases, enables styrene production in Pseudomonas. PSC1 is a globular dimer with a molecular mass of 104.7 kDa, high thermal stability (Tm 63°C), and activity at temperatures up to 50°C. The crystal structure of PSC1, determined at 2.1 Å, reveals a homodimer with three domains per monomer. A hydrophobic pocket in domain 2, essential for cofactor and substrate binding, was identified. Mutagenesis shows that Arg175, Glu280, and Glu285 are critical for catalysis, as replacing them with alanine abolished the decarboxylation.IMPORTANCEThe petrochemical industry is highly polluting due to its use of extremely high temperatures, high pressure, and toxic catalysts. Synthetic biology offers an alternative by enabling the production of many chemicals through cell factories that operate at room temperature and ambient pressure, potentially reducing CO2 emissions by up to 90%. We have engineered a solvent-tolerant Pseudomonas strain to produce styrene from L-phenylalanine in a two-step process. For the second step, we designed a de novo consensus protein that operates efficiently. In this study, we present its physico-chemical properties and unveil its 3D structure.https://journals.asm.org/doi/10.1128/mbio.00714-25Pseudomonassynthetic biologystyrene biosynthesisdecarboxylases
spellingShingle Ana García-Franco
Jesús de la Torre
Patricia Godoy
Estrella Duque
Carmen López
José A. Gavira
Juan L. Ramos
Characterization of a consensus-designed trans-cinnamic acid decarboxylase for styrene biosynthesis
mBio
Pseudomonas
synthetic biology
styrene biosynthesis
decarboxylases
title Characterization of a consensus-designed trans-cinnamic acid decarboxylase for styrene biosynthesis
title_full Characterization of a consensus-designed trans-cinnamic acid decarboxylase for styrene biosynthesis
title_fullStr Characterization of a consensus-designed trans-cinnamic acid decarboxylase for styrene biosynthesis
title_full_unstemmed Characterization of a consensus-designed trans-cinnamic acid decarboxylase for styrene biosynthesis
title_short Characterization of a consensus-designed trans-cinnamic acid decarboxylase for styrene biosynthesis
title_sort characterization of a consensus designed trans cinnamic acid decarboxylase for styrene biosynthesis
topic Pseudomonas
synthetic biology
styrene biosynthesis
decarboxylases
url https://journals.asm.org/doi/10.1128/mbio.00714-25
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