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Development of Biocatalytic Approach Using Fungal Laccase

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Development of Biocatalytic Approach Using Fungal Laccase DEVELOPMENT OF BIOCATALYTIC APPROACH USING FUNGAL LACCASE TO PRODUCE NOVEL FUNCTIONAL INGREDIENTS VIA PROTEIN CROSS- LINKING AND PROTEIN/POLYSACCHARIDE CONJUGATION by Mingqin Li Department of Food Science and Agricultural Chemistry MacDonald Campus, McGill University Quebec, Canada May, 2020 A thesis submitted to McGill University in partial fulfillment of the requirements of the degree of Doctor of Philosophy in Food Science © Mingqin Li, 2020 SUGGESTED SHORT TITLE PROTEIN MODIFICATION CATALYZED BY LACCASE II ABSTRACT Laccase (E.C 1.3.10.2) is a versatile biocatalyst, which can be used for protein modification. Kinetics of biocatalytic conversions of protein-related substrate models by laccases were studied in order to contribute to the understanding of mechanistic actions of laccase in protein cross-linking. Fungal laccases exhibited higher substrate specificity towards the peptide -1 -1 models (Km=0.17-0.67 mM, kcat/Km=0.56-0.81 s mM ) ST-10 (SYMTDYYLST), derived from potato patatin, and AG-10 (AKKIVSDGNG), derived from egg white lysozyme (LZM), -1 -1 than tyrosine (Y) (Km= 1.10-1.12 mM, kcat/Km=0.01-0.31 s mM ). This was confirmed by the molecular docking study, in which substrate/enzyme binding modes with better affinity were observed for laccase/peptides than for laccase/tyrosine. Laccase-catalyzed reaction resulted in the cross-linking of tyrosine-containing peptide ST-10 via the formation of di- and oligo- tyrosine linkages; while the cross-linking of peptide AG-10, which does not contain tyrosine residues, was achieved only in the presence of ferulic acid (FA) as reaction mediator. Grafting of FA reactive sites on proteins via amidation followed by Trametes versicolor laccase -catalyzed cross-linking was performed on compact globular proteins, LZM and ovalbumin (OVA). The substrate reactivity and cross-linking efficiency of FA-modified LZM and OVA was improved as compared to their native forms. Polymerization was achieved by FA-modified LZM, whereas oligomers were the main cross-linked products of FA-OVA. The grafted FA- associated cross-links of the products were characterized using mass spectrometry, which were predominated by the form of 8-5’ dehydrodiferulic acid. FA grafting/laccase-cross-linking treatment enhanced the emulsification performance of LZM and the foaming capacity of OVA. Furthermore, the cross-linked proteins (particularly LZM) exhibited lower immunoglobulin E binding capacity (up to 50% reduction) than the native forms, indicating current cross-linking treatment is able to decrease their allergenicity. In light of our findings on the crosslinking of ST-10 peptides derived from potato patatin, a study on the cross-linking of potato proteins was carried out using laccases from T. versicolor and Coriolus hirsutus with or without the presence of FA. Higher catalytic efficiency of laccases was shown towards potato protein fraction (PAT) containing patatin, whereas smaller- sized potato protease inhibitor fraction (PIs) were faster in forming oxidative cross-linked products. The cross-linking extent was impacted by the type of laccase and the use of FA. The increase in reaction time up to 24h resulted in the shifting of the cross-linked products towards higher molecular weight, while the extended treatments (48h) led to precipitation or oxidative fragmentation. III The conjugation of PAT with selected pectic polysaccharides via laccase-catalyzed reaction was further investigated and modulated using response surface methodology (RSM) to achieve product with defined conjugation extent and emulsification performance. The highest hetero- conjugation efficiency was shown by C. hirsutus laccase-PAT/sugar beet pectin (SBP) reaction system. The developed predictive models revealed that PAT ratio in PAT/SBP mixture was correlated negatively with the conjugation extent but positively with the emulsification performance, and these correlations were affected by the interaction between PAT ratio and enzyme concentration or reaction time The effect of laccase-catalyzed modification on functionality profile of potato proteins was assessed by correlating the interfacial properties with cross-linking/conjugation extent, product profile, protein unfolding, secondary structure composition and incorporation of ferulic acid. The oxidative cross-linking improved the emulsifying property of both PAT and PIs, while short time treatment and product profile with enriched 60-80 kDa fraction was associated with enhanced foaming property in PAT. The PATs conjugated with SBP had relatively low surface tension as compared to the native and cross-linked PATs at neutral pH; however, the resulted interfaces were characterized by low elasticity. The highest surface dilatational elasticity of the protein samples at neutral pH was observed with cross-linked PAT obtained from 24h reaction without FA. Extended treatments for 48h led to both cross-linking and fragmentation of PAT; the resulted products showed a higher structural stability and contributed to the low susceptibility of the interfacial behaviour of PAT to acidic pH and to relatively high surface dilatational elasticity. IV RESUME La laccase (E.C 1.3.10.2) est un biocatalyseur polyvalent, qui peut être utilisé pour la modification des protéines. Les cinétiques des bioconversions des substrats-modèles dérivés des protéines par les laccases ont été étudiées, afin de contribuer à la compréhension du mécanisme d’action de la laccase pendant la réticulation des protéines. Les laccases fongiques ont été caractérisées par une spécificité plus élevée vis-à-vis des substrats modèles peptidiques -1 -1 (Km=0,17-0,67mM, kcat/Km=0,56-0,81s mM ) ST-10 (SYMTDYYLST), dérivé de la patatine de pomme de terre, et AG-10 (AKKIVSDGNG), dérivé du lysozyme de blanc d'oeuf (LZM), -1 -1 en comparaison avec la tyrosine (Y) (Km =1,10-1,12 mM, kcat/Km=0,01-0,31 s mM ). Ces résultats ont été confirmés par l'étude moléculaire « Docking », dans laquelle des modes de liaison substrat/enzyme ayant une meilleure affinité ont été observés pour laccase/peptides que pour laccase/tyrosine. La réaction catalysée par la laccase a conduit à une réticulation du peptide ST-10 contenant de la tyrosine via la formation des liaisons de di- et oligo-tyrosine ; tandis que la réticulation du peptide AG-10, qui ne contient pas de résidu tyrosine, n'a pas pu être accomplis qu'en présence d'acide férulique (AF) comme médiateur de réaction. Le greffage des sites réactifs du AF sur les protéines via amidation suivi d'une réticulation catalysée par la laccase de Trametes versicolor ont été réalisés sur des protéines globulaires compactes, LZM et ovalbumine (OVA). La réactivité du substrat et l'efficacité de la réticulation des LZM et OVA modifiées par AF étaient plus élevées en comparaison avec leurs formes natives. LZM modifiée par AF a été polymérisée, tandis que des oligomères étaient les principaux produits réticulés de AF-OVA. Les réticulations formées au niveau des greffés AF ont été caractérisées par la spectrométrie de masse, par laquelle la forme d'acide 8-5’ déhydrodiférulique était identifiée comme étant la plus prédominante. Le traitement de greffage avec AF suivi de la réticulation avec laccase a amélioré la performance émulsifiante du LZM et la capacité moussante de l'OVA. De plus, les protéines réticulées présentaient une capacité de liaison aux immunoglobulines E plus faible (jusqu'à 50% de réduction pour LZM) que les formes natives, ce qui indique que le traitement de réticulation des protéines modifiés est capable de diminuer l'allergénicité. À la lumière de nos résultats sur la réticulation des peptides ST-10 dérivés de la patatine de pomme de terre, une étude sur la réticulation des protéines de pomme de terre a été réalisée en utilisant des laccases de T. versicolor et Coriolus hirsutus avec ou sans présence d'AF. Les laccases ont montré une efficacité catalytique plus élevée vis-à-vis de la fraction de protéine de pomme de terre (PAT) contenant de la patatine, alors que l’utilisation de la fraction V contenant des inhibiteurs de protéase de pomme de terre (IP) a conduit à une formation rapide des produits de la réticulation oxydative. Le dégrée de réticulation a été affectée par le type de laccase et la présence de AF. L'augmentation du temps de réaction jusqu'à 24h a entraîné le déplacement des produits réticulés vers un poids moléculaire plus élevé, tandis qu’un traitement prolongé (48h) a entraîné une précipitation ou une fragmentation oxydative. La conjugaison de PAT avec des polysaccharides pectiques sélectionnés à travers une réaction catalysée par la laccase a été étudiée et modulée en utilisant une méthodologie de surface de réponse (RSM) pour obtenir un produit avec un dégrée de conjugaison et de performance émulsifiante bien définie. L'hétéro-conjugaison la plus élevée a été obtenue lors de l’utilisation du système réactionnel composé de C. hirsutus laccase-PAT/pectine de betterave sucrière (SBP). Les modèles prédictifs développés ont révélé que la proportion de PAT dans le mélange PAT/SBP était corrélée négativement avec l'étendue de la conjugaison mais positivement avec la performance émulsifiante, et ces corrélations étaient affectées par l'interaction entre la proportion de PAT et la concentration enzymatique ou le temps de réaction L'effet de la modification catalysée par la laccase sur le profil de fonctionnalité des protéines de pomme de terre a été évalué en corrélant les propriétés interfaciales avec l'étendue de la réticulation/conjugaison, le profil du produit, le déploiement des protéines, la composition de la structure secondaire et l'incorporation d'acide férulique. La réticulation oxydative a amélioré la propriété émulsifiante du PAT et d’IP. Un traitement de courte durée et l’enrichissement avec des produits ayant 60 - 80 kDa ont été associés avec l’amélioration de la propriété moussante de PAT. À pH neutre, PAT conjugué avec SBP a montré une tension superficielle relativement faible par rapport aux autres PAT natif et réticulés. Cependant, les interfaces résultantes ont été caractérisés par une faible élasticité.
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