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Biology subjects

Bunzel, H. A.

Publications and source records attributed to Bunzel, H. A..

10 recordsLinked to original sources

Machine learned potentials with electrostatic embedding accurately capture Kemp eliminase reactivity

Kemp elimination has become a benchmark for de novo enzyme design due to its simplicity and detailed mechanistic understanding but accurate barrier calculations are required to understand the difference in activity between designed Kemp eliminases. QM/MM MD simulations are capable of calculating reaction barriers, but are limited by a cost/accuracy tradeoff in which the most accurate methods are too computationally expensive for extensive screening as would be required in a prospective enzyme design campaign. Recent advances in embedded ML/MM simulations using the electrostatic machine learning embedding (EMLE) method have enabled transferable potentials for ML/MM MD simulations with low computational cost but QM-level accuracy. Here, we trained a MACE MLIP and EMLE embedding model for fast and accurate simulations of the enzymatic, base-catalysed Kemp elimination of 6-nitro benzisoxazole. Applying our EMLE ML/MM scheme to a designed Kemp eliminase and its evolved counterpart captured the {approx}4 kcal/mol difference in barrier between the two observed in experiment. Furthermore, training was done using structures generated from simulations of a single variant and was applied to the second variant, achieving near-experimental barriers, with no further finetuning or computational overhead. Thus, this work establishes EMLE-based ML/MM MD simulations as a potential route for fast and accurate assessment of barriers in computational screening for enzyme design.

biochemistry↗

Evolution promotes transition-state-like conformations with enhanced basicity and electric fields in the substrate complex of a designer enzyme

Enzymes can be computationally designed for an increasing range of reactions, yet the catalytic efficiencies achieved are typically well below those of natural biocatalysts. Directed evolution can narrow this gap, often improving activity through mutations with non-obvious effects on catalysis. Here, we dissect how directed evolution improved a de novo designed Kemp eliminase by comparing the ground-state and transition-state ensembles of the designed and evolved variants. Extensive molecular dynamics simulations and QM/MM reaction barrier calculations identify subtle but important differences that modulate reactivity. Simulations show that reaction proceeds via a specific transition-state-like conformation, characterized by desolvation of the catalytic base and an organized active-site electric field. Barriers correlate strongly with the reaction energy of proton transfer, indicating that desolvating the catalytic base in the ligand-bound complex raises its proton affinity and thereby lowers the barrier. Evolution enriches the ground-state ensemble in reactive conformations, minimizing the reorganization required to reach the transition state. After evolution, formation of the transition-state-like conformation causes less disruption to the protein, which maintains coordinated motions. This is consistent with the emergence of a negative activation heat capacity with evolution. Efficient catalysis requires a ground-state ensemble that resembles the transition state, an objective that enzyme design should pursue alongside geometric and electrostatic complementarity for the transition state.

biochemistry↗

Evolution tunes functional sub-state interconversion to boost enzyme function

Enzymes do not operate as static structures, but continuously fluctuate between different conformations. Enzymes therefore dynamically sample conformations with varying catalytic activity. However, it remains largely unexplored whether evolution can exploit the conformational dynamics between sub-states to improve activity. Here, we dissect the evolutionary trajectory of the {beta}-lactamase OXA-48 toward improved ceftazidime hydrolysis. Evolution relieved conformational bottlenecks by promoting alternate functional sub-states, gradually shifting the rate-limiting step from substrate binding to sub-state interconversion, and finally to the chemical step. Reorganization of the conformational landscape enhanced OXA-48s ability to hydrolyze ceftazidime and introduced a trade-off in its native activity against meropenem. This trade-off stemmed from catalytic incompatibility between the native and the evolved sub-state populations. Our findings highlight the transitions between functional sub-states as a mechanism of natural selection, shaping functional divergence and offering new strategies for enzyme and antibiotic engineering.

molecular biology↗

AI.zymes - A modular platform for evolutionary enzyme design

The ability to create new-to-nature enzymes would substantially advance bioengineering, medicine, and the chemical industry. Despite recent breakthroughs in protein design and structure prediction, designing biocatalysts with activities rivaling those of natural enzymes remains challenging. Here, we present AI.zymes, a modular platform integrating cutting-edge protein engineering algorithms within an evolutionary framework. By combining programs such as Rosetta, ESMFold, ProteinMPNN, and FieldTools in iterative rounds of design and selection, AI.zymes optimizes a broad range of catalytically relevant properties, such as transition state affinity and protein stability. Notably, AI.zymes can also improve properties that are not targeted by the employed design algorithms. For instance, AI.zymes enhanced electrostatic catalysis by iteratively selecting variants with stronger catalytic electric fields. AI.zymes was benchmarked by improving the promiscuous Kemp eliminase activity of ketosteroid isomerase, yielding a 7.7-fold increase in activity after zero-shot experimental validation of only 7 variants. Due to its modularity, AI.zymes can readily incorporate emerging design algorithms, paving the way for a unifying framework for enzyme design. O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=114 SRC="FIGDIR/small/633707v1_ufig1.gif" ALT="Figure 1"> View larger version (26K): org.highwire.dtl.DTLVardef@f2ac2eorg.highwire.dtl.DTLVardef@61b2aorg.highwire.dtl.DTLVardef@e176edorg.highwire.dtl.DTLVardef@46d692_HPS_FORMAT_FIGEXP M_FIG C_FIG

bioengineering↗

Electric fields determine carbapenemase activity in class A β-lactamases

Antimicrobial resistance is a public health crisis. Limited understanding of the catalytic drivers in resistance-mediating enzymes such as {beta}-lactamases hinders our ability to combat this crisis. Here, we dissect the catalytic contributions of active-site electric fields in class A {beta}-lactamases. We studied the enzymatic hydrolysis of a carbapenem antibiotic by QM/MM molecular dynamics simulations and quantified active-site fields with a custom-made script. We discovered that the fields correlate well with activity and identified seven positions, some distal, that distinguish efficient carbapenemases. Electric-field analysis may help predict the activity of {beta}-lactamases and guide antibiotic and enzyme design. O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=109 SRC="FIGDIR/small/565607v1_ufig1.gif" ALT="Figure 1"> View larger version (27K): org.highwire.dtl.DTLVardef@15ee41aorg.highwire.dtl.DTLVardef@d1a11corg.highwire.dtl.DTLVardef@a83bd7org.highwire.dtl.DTLVardef@f0abdf_HPS_FORMAT_FIGEXP M_FIG C_FIG Electric field script: www.github.com/bunzela/FieldTools

biochemistry↗

Epistasis Arises from Shifting the Rate-Limiting Step during Enzyme Evolution

The molecular mechanisms by which epistasis boosts enzyme activity remain elusive, undermining our ability to predict the evolution of pathogens and engineer novel biocatalysts. Here, we reveal how directed evolution of a {beta}-lactamase yielded highly epistatic activity enhancements. Evolution selected four mutations that increase antibiotic resistance 40-fold, despite their marginal individual effects ([≤] 2-fold). Synergistic improvements coincided with the introduction of super-stochiometric burst kinetics, indicating that epistasis is rooted in the enzymes conformational dynamics. Kinetic, structural, and dynamical analyses reveal that epistasis was driven by distinct effects of each mutation on the catalytic cycle. The first mutation acquired during evolution increases protein flexibility and accelerates substrate binding, which is rate-limiting in the wild-type enzyme. The ensuing mutations predominantly boosted the chemical steps by fine-tuning substrate interactions. Our work identifies an overlooked cause for epistasis: changing the rate-limiting step can result in substantial positive synergy boosting enzyme activity.

evolutionary biology↗

Antibodies generated in vitro and in vivo elucidate design of a thermostable ADDomer COVID-19 nasal nanoparticle vaccine

COVID-19 continues to damage populations, communities and economies worldwide. Vaccines have reduced COVID-19-related hospitalisations and deaths, primarily in developed countries. Persisting infection rates, and highly transmissible SARS-CoV-2 Variants of Concern (VOCs) causing repeat and breakthrough infections, underscore the ongoing need for new treatments to achieve a global solution. Based on ADDomer, a self-assembling protein nanoparticle scaffold, we created ADDoCoV, a thermostable COVID-19 candidate vaccine displaying multiple copies of a SARS-CoV-2 receptor binding motif (RBM)-derived epitope. In vitro generated neutralising nanobodies combined with molecular dynamics (MD) simulations and electron cryo-microscopy (cryo-EM) established authenticity and accessibility of the epitopes displayed. A Gigabody comprising multimerized nanobodies prevented SARS-CoV-2 virion attachment with picomolar EC50. Antibodies generated by immunising mice cross-reacted with VOCs including Delta and Omicron. Our study elucidates nasal administration of ADDomer-based nanoparticles for active and passive immunisation against SARS-CoV-2 and provides a blueprint for designing nanoparticle reagents to combat respiratory viral infections.

biochemistry↗

Photovoltaic enzymes by design and evolution

The global energy crisis challenges us to develop more efficient strategies for the sustainable production of energy. Given the excellent efficiency of the natural photosynthetic apparatus, biohybrid photovoltaic devices present an attractive solution for solar energy conversion. However, their composition, stability, and complexity can limit their inclusion into photovoltaic devices. Here, we combined computational design and directed evolution to overcome these limitations and create tailor-made photoenzymes. Photo-biocatalysts were designed by introducing photosensitizer binding sites into heme-containing helical bundle proteins. The designed binding sites were specific for the target photosensitizer and readily transplanted into other helical bundles. The best design was highly evolvable and reached nanomolar ligand affinity after mutagenesis and screening. The evolved enzyme generated 2.6 times higher photocurrents than the photosensitizer alone, primarily driven by increased photostability. Evolvability is a unique advantage of our protein-based approach over abiological photovoltaic and will be critical to developing efficient biohybrid systems. O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=114 SRC="FIGDIR/small/521207v1_ufig1.gif" ALT="Figure 1"> View larger version (31K): org.highwire.dtl.DTLVardef@2b6031org.highwire.dtl.DTLVardef@1b83f69org.highwire.dtl.DTLVardef@14b39a4org.highwire.dtl.DTLVardef@1b569bb_HPS_FORMAT_FIGEXP M_FIG C_FIG

synthetic biology↗

Beneficial substrate partitioning boosts non-aqueous catalysis in de novo enzyme-alginate beads

Synthetic reactions often require solvents incompatible with biocatalysts. Here, we encapsulate a de novo heme-containing enzyme, C45, in calcium-alginate hydrogel beads to facilitate heterogeneous biocatalysis in neat organic solvents. Post-encapsulation, C45 retains activity even when the beads are suspended in organic solvents. In particular, the carbene transferase activity of C45 is enhanced when reactions are performed in aprotic, non-polar solvents such as hexane and toluene. Activity-solvent dependencies reveal that this activity boost is likely due to beneficial partitioning of the substrate into the beads from the organic phase. Furthermore, encapsulation facilitates enzyme recovery and recycling after the reaction. Such encapsulation opens up novel opportunities for biocatalysis in organic solvent systems, combining desired solvent properties of organic chemistry with enzymatic selectivity and proficiency.

synthetic biology↗

Evolution of dynamical networks enhances catalysis in a designer enzyme

Activation heat capacity is emerging as a crucial factor in enzyme thermoadaptation, as shown by non-Arrhenius behaviour of many natural enzymes1,2. However, its physical origin and relationship to evolution of catalytic activity remain uncertain. Here, we show that directed evolution of a computationally designed Kemp eliminase introduces dynamical changes that give rise to an activation heat capacity absent in the original design3. Extensive molecular dynamics simulations show that evolution results in the closure of solvent exposed loops and better packing of the active site with transition state stabilising residues. Remarkably, these changes give rise to a correlated dynamical network involving the transition state and large parts of the protein. This network tightens the transition state ensemble, which induces an activation heat capacity and thereby nonlinearity in the temperature dependence. Our results have implications for understanding enzyme evolution (e.g. in explaining the role of distal mutations and evolutionary tuning of dynamical responses) and suggest that integrating dynamics with design and evolution will accelerate the development of efficient novel enzymes.

biochemistry↗