Activity screening of environmental metagenomic libraries reveals novel carboxylesterase families

Popovic, Ana; Hai, Tran; Tchigvintsev, Anatoly; Hajighasemi, Mahbod; Nocek, Boguslaw; Khusnutdinova, Anna N.; Brown, Greg; Glinos, Julia; Flick, Robert; Skarina, Tatiana; Chernikova, Tatyana N.; Yim, Veronica; Brüls, Thomas; Paslier, Denis Le; Yakimov, Michail M.; Joachimiak, Andrzej; Ferrer, Manuel; Golyshina, Olga V.; Savchenko, Alexei; Golyshin, Peter N.; Yakunin, Alexander F.

doi:10.1038/srep44103

Title: Activity screening of environmental metagenomic libraries reveals novel carboxylesterase families

Journal Article · Wed Mar 08 00:00:00 EST 2017 · Scientific Reports

DOI:https://doi.org/10.1038/srep44103· OSTI ID:1393927

Popovic, Ana ^[1]; Hai, Tran ^[2]; Tchigvintsev, Anatoly ^[1]; Hajighasemi, Mahbod ^[1]; Nocek, Boguslaw ^[3]; Khusnutdinova, Anna N. ^[1]; Brown, Greg ^[1]; Glinos, Julia ^[1]; Flick, Robert ^[1]; Skarina, Tatiana ^[1]; Chernikova, Tatyana N. ^[2]; Yim, Veronica ^[1]; Brüls, Thomas ^[4]; Paslier, Denis Le ^[5]; Yakimov, Michail M. ^[6]; Joachimiak, Andrzej ^[3]; Ferrer, Manuel ^[7]; Golyshina, Olga V. ^[2]; Savchenko, Alexei ^[1]; Golyshin, Peter N. ^[2] more »

Univ. of Toronto, ON (Canada). Dept. of Chemical Engineering and Applied Chemistry
Bangor Univ., Gwynedd (United Kingdom). School of Biological Sciences
Argonne National Lab. (ANL), Argonne, IL (United States). Midwest Center for Structural Genomics, Structural Biology Center
Univ. of Evry Val d'Essonne (UEVE) (France). National Center of Scientific Research (CNRS)
Univ. of Evry Val d'Essonne (UEVE) (France). National Center for Scientific Research (CNRS)
Inst. for Coastal Marine Environment, Messina (Italy)
Spanish National Research Council (CSIC), Madrid (Spain). Inst. of Catalysis

Metagenomics has made accessible an enormous reserve of global biochemical diversity. In order to tap into this vast resource of novel enzymes, we have screened over one million clones from metagenome DNA libraries derived from sixteen different environments for carboxylesterase activity and identified 714 positive hits. Here, we validated the esterase activity of 80 selected genes, which belong to 17 different protein families including unknown and cyclase-like proteins. Three metagenomic enzymes exhibited lipase activity, and seven proteins showed polyester depolymerization activity against polylactic acid and polycaprolactone. Detailed biochemical characterization of four new enzymes revealed their substrate preference, whereas their catalytic residues were identified using site-directed mutagenesis. The crystal structure of the metal-ion dependent esterase MGS0169 from the amidohydrolase superfamily revealed a novel active site with a bound unknown ligand. Thus, activity-centered metagenomics has revealed diverse enzymes and novel families of microbial carboxylesterases, whose activity could not have been predicted using bioinformatics tools.

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Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER); Genome Canada; Ontario Genomics Institute; Ontario Research Fund; Natural Sciences and Engineering Research Council of Canada (NSERC); Spanish Ministerio de Economia y Competitividad (MINECO); German Federal Ministry of Education and Research (BMBF); Biotechnology and Biological Sciences Research Council (BBSRC); European Regional Development Fund (ERDF)

Grant/Contract Number:: AC02-06CH11357

OSTI ID:: 1393927

Journal Information:: Scientific Reports, Vol. 7; ISSN 2045-2322

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 48 works

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Bioprospecting Reveals Class III ω-Transaminases Converting Bulky Ketones and Environmentally Relevant Polyamines Coscolín, Cristina; Katzke, Nadine; García-Moyano, Antonio RWTH Aachen University https://doi.org/10.18154/rwth-2020-04099	text	January 2019
Application of the uridine auxotrophic host and synthetic nucleosides for a rapid selection of hydrolases from metagenomic libraries Urbelienė, Nina; Kutanovas, Simonas; Meškienė, Rita Microbial Biotechnology, Vol. 12, Issue 1 https://doi.org/10.1111/1751-7915.13316	journal	October 2018
A novel method for rapid and sensitive metagenomic activity screening Shang, Meiling; Chan, Victor J.; Wong, Dominic W. S. MethodsX, Vol. 5 https://doi.org/10.1016/j.mex.2018.06.011	journal	January 2018
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Targeted enzyme gene re-positioning: A computational approach for discovering alternative bacterial enzymes for the synthesis of plant-specific secondary metabolites Nakamura, Yuya; Hirose, Shuichi; Taniguchi, Yuko Metabolic Engineering Communications, Vol. 9 https://doi.org/10.1016/j.mec.2019.e00102	journal	December 2019
Microbial Metagenomics for Industrial and Environmental Bioprospecting: The Unknown Envoy Dhanjal, Daljeet Singh; Sharma, Deepansh Microbial Bioprospecting for Sustainable Development https://doi.org/10.1007/978-981-13-0053-0_18	book	January 2018
Enzymes from Marine Polar Regions and Their Biotechnological Applications Bruno, Stefano; Coppola, Daniela; di Prisco, Guido Marine Drugs, Vol. 17, Issue 10 https://doi.org/10.3390/md17100544	journal	September 2019
A Novel Polyester Hydrolase From the Marine Bacterium Pseudomonas aestusnigri – Structural and Functional Insights Bollinger, Alexander; Thies, Stephan; Knieps-Grünhagen, Esther Frontiers in Microbiology, Vol. 11 https://doi.org/10.3389/fmicb.2020.00114	journal	February 2020
Application of cell-free protein synthesis for faster biocatalyst development Rolf, Jascha; Rosenthal, Katrin; Lütz, Stephan Technische Universität Dortmund https://doi.org/10.17877/de290r-19948	text	January 2019
A Novel Polyester Hydrolase From the Marine Bacterium Pseudomonas aestusnigri – Structural and Functional Insights Bollinger, Alexander; Thies, Stephan; Knieps-Grünhagen, Esther Deutsches Elektronen-Synchrotron, DESY, Hamburg https://doi.org/10.3204/pubdb-2020-03228	text	January 2020
Agar plate‐based screening methods for the identification of polyester hydrolysis by Pseudomonas species Molitor, Rebecka; Bollinger, Alexander; Kubicki, Sonja Microbial Biotechnology, Vol. 13, Issue 1 https://doi.org/10.1111/1751-7915.13418	journal	January 2020
Metagenomics: novel enzymes from non-culturable microbes Berini, Francesca; Casciello, Carmine; Marcone, Giorgia Letizia FEMS Microbiology Letters, Vol. 364, Issue 21 https://doi.org/10.1093/femsle/fnx211	journal	October 2017
Decoding the ocean's microbiological secrets for marine enzyme biodiscovery Ferrer, Manuel; Méndez-García, Celia; Bargiela, Rafael FEMS Microbiology Letters, Vol. 366, Issue 1 https://doi.org/10.1093/femsle/fny285	journal	December 2018

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