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Evolution of Enzyme Superfamilies: Comprehensive Exploration of Sequence–Function Relationships

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Michael Smith Laboratories, University of British Columbia, Vancouver, BC V6T 1Z4, Canada
*E-mail: [email protected]
Cite this: Biochemistry 2016, 55, 46, 6375–6388
Publication Date (Web):November 1, 2016
https://doi.org/10.1021/acs.biochem.6b00723
Copyright © 2016 American Chemical Society
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    Abstract

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    The sequence and functional diversity of enzyme superfamilies have expanded through billions of years of evolution from a common ancestor. Understanding how protein sequence and functional “space” have expanded, at both the evolutionary and molecular level, is central to biochemistry, molecular biology, and evolutionary biology. Integrative approaches that examine protein sequence, structure, and function have begun to provide comprehensive views of the functional diversity and evolutionary relationships within enzyme superfamilies. In this review, we outline the recent advances in our understanding of enzyme evolution and superfamily functional diversity. We describe the tools that have been used to comprehensively analyze sequence relationships and to characterize sequence and function relationships. We also highlight recent large-scale experimental approaches that systematically determine the activity profiles across enzyme superfamilies. We identify several intriguing insights from this recent body of work. First, promiscuous activities are prevalent among extant enzymes. Second, many divergent proteins retain “function connectivity” via enzyme promiscuity, which can be used to probe the evolutionary potential and history of enzyme superfamilies. Finally, we discuss open questions regarding the intricacies of enzyme divergence, as well as potential research directions that will deepen our understanding of enzyme superfamily evolution.

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    3. Guillermo Bahr, Lisandro J. González, Alejandro J. Vila. Metallo-β-lactamases in the Age of Multidrug Resistance: From Structure and Mechanism to Evolution, Dissemination, and Inhibitor Design. Chemical Reviews 2021, 121 (13) , 7957-8094. https://doi.org/10.1021/acs.chemrev.1c00138
    4. Rory M. Crean, Jasmine M. Gardner, Shina C. L. Kamerlin. Harnessing Conformational Plasticity to Generate Designer Enzymes. Journal of the American Chemical Society 2020, 142 (26) , 11324-11342. https://doi.org/10.1021/jacs.0c04924
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    7. John A. Gerlt . Genomic Enzymology: Web Tools for Leveraging Protein Family Sequence–Function Space and Genome Context to Discover Novel Functions. Biochemistry 2017, 56 (33) , 4293-4308. https://doi.org/10.1021/acs.biochem.7b00614
    8. G.A. TEREGULOVA, N.A. MANUCHAROVA, N.A. URAZBAKHTINA, N.S. ZHEMCHUZHINA, L.I. YEVTUSHENKO, A.L. STEPANOV. ANTIMICROBIAL ACTIVITY OF SPECIALISED METABOLITES OF SOIL STREPTOMYCETES-CHITINOLYTIC. Lomonosov Soil Science Journal 2024, 79 (№1, 2024) https://doi.org/10.55959/MSU0137-0944-17-2024-79-1-51-60
    9. G. A. Teregulova, N. A. Manucharova, N. A. Urazbakhtina, N. S. Zhemchuzhina, L. I. Yevtushenko, A. L. Stepanov. Antimicrobial Activity of Specialized Metabolites of Soil Chitinolytic Streptomycetes. Moscow University Soil Science Bulletin 2024, 79 (1) , 47-55. https://doi.org/10.3103/S0147687424010083
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    11. Ioannis G. Riziotis, António J.M. Ribeiro, Neera Borkakoti, Janet M. Thornton. The 3D Modules of Enzyme Catalysis: Deconstructing Active Sites into Distinct Functional Entities. Journal of Molecular Biology 2023, 435 (20) , 168254. https://doi.org/10.1016/j.jmb.2023.168254
    12. Karol Buda, Charlotte M. Miton, Xingyu Cara Fan, Nobuhiko Tokuriki. Molecular determinants of protein evolvability. Trends in Biochemical Sciences 2023, 48 (9) , 751-760. https://doi.org/10.1016/j.tibs.2023.05.009
    13. Michael Wells, Minjae Kim, Denise M. Akob, Partha Basu, John F. Stolz, . Impact of the Dimethyl Sulfoxide Reductase Superfamily on the Evolution of Biogeochemical Cycles. Microbiology Spectrum 2023, 11 (2) https://doi.org/10.1128/spectrum.04145-22
    14. . EVOLUTION OF ENZYMES. 2023, 455-485. https://doi.org/10.1002/9781119793304.ch16
    15. António J. M. Ribeiro, Ioannis G. Riziotis, Jonathan D. Tyzack, Neera Borkakoti, Janet M. Thornton. Using mechanism similarity to understand enzyme evolution. Biophysical Reviews 2022, 14 (6) , 1273-1280. https://doi.org/10.1007/s12551-022-01022-9
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    18. Mitesh Nagar, Joshua A. Hayden, Einat Sagey, George Worthen, Mika Park, Amar Nath Sharma, Christopher M. Fetter, Oliver P. Kuehm, Stephen L. Bearne. Altering the binding determinant on the interdigitating loop of mandelate racemase shifts specificity towards that of d-tartrate dehydratase. Archives of Biochemistry and Biophysics 2022, 718 , 109119. https://doi.org/10.1016/j.abb.2022.109119
    19. Deeksha Thakur, Shashi Bhushan Pandit. Unusual commonality in active site structural features of substrate promiscuous and specialist enzymes. Journal of Structural Biology 2022, 214 (1) , 107835. https://doi.org/10.1016/j.jsb.2022.107835
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    37. Angelica Jimenez-Rosales, Miriam V. Flores-Merino. Tailoring Proteins to Re-Evolve Nature: A Short Review. Molecular Biotechnology 2018, 60 (12) , 946-974. https://doi.org/10.1007/s12033-018-0122-3
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    41. Lianet Noda-Garcia, Wolfram Liebermeister, Dan S. Tawfik. Metabolite–Enzyme Coevolution: From Single Enzymes to Metabolic Pathways and Networks. Annual Review of Biochemistry 2018, 87 (1) , 187-216. https://doi.org/10.1146/annurev-biochem-062917-012023
    42. Ben E. Clifton, Joe A. Kaczmarski, Paul D. Carr, Monica L. Gerth, Nobuhiko Tokuriki, Colin J. Jackson. Evolution of cyclohexadienyl dehydratase from an ancestral solute-binding protein. Nature Chemical Biology 2018, 14 (6) , 542-547. https://doi.org/10.1038/s41589-018-0043-2
    43. Richard A Notebaart, Bálint Kintses, Adam M Feist, Balázs Papp. Underground metabolism: network-level perspective and biotechnological potential. Current Opinion in Biotechnology 2018, 49 , 108-114. https://doi.org/10.1016/j.copbio.2017.07.015
    44. Matilda S .Newton, Vickery L Arcus, Monica L Gerth, Wayne M Patrick. Enzyme evolution: innovation is easy, optimization is complicated. Current Opinion in Structural Biology 2018, 48 , 110-116. https://doi.org/10.1016/j.sbi.2017.11.007
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    46. Jonathan D Tyzack, Nicholas Furnham, Ian Sillitoe, Christine M Orengo, Janet M Thornton. Understanding enzyme function evolution from a computational perspective. Current Opinion in Structural Biology 2017, 47 , 131-139. https://doi.org/10.1016/j.sbi.2017.08.003
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    48. Karolina Wieszczycka, Katarzyna Staszak. Artificial metalloenzymes as catalysts in non-natural compounds synthesis. Coordination Chemistry Reviews 2017, 351 , 160-171. https://doi.org/10.1016/j.ccr.2017.06.012
    49. Xiongying Tu, John A. Latham, Valerie J. Klema, Robert L. Evans, Chao Li, Judith P. Klinman, Carrie M. Wilmot. Crystal structures reveal metal-binding plasticity at the metallo-β-lactamase active site of PqqB from Pseudomonas putida. JBIC Journal of Biological Inorganic Chemistry 2017, 22 (7) , 1089-1097. https://doi.org/10.1007/s00775-017-1486-8
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