Evolution of substrate specificity in a retained enzyme driven by gene loss
Abstract
The connection between gene loss and the functional adaptation of retained proteins is still poorly understood. We apply phylogenomics and metabolic modeling to detect bacterial species that are evolving by gene loss, with the finding that Actinomycetaceae genomes from human cavities are undergoing sizable reductions, including loss of L-histidine and L-tryptophan biosynthesis. We observe that the dual-substrate phosphoribosyl isomerase A or priA gene, at which these pathways converge, appears to coevolve with the occurrence oftrpandhisgenes. Characterization of a dozen PriA homologs shows that these enzymes adapt from bifunctionality in the largest genomes, to a monofunctional, yet not necessarily specialized, inefficient form in genomes undergoing reduction. These functional changes are accomplished via mutations, which result from relaxation of purifying selection, in residues structurally mapped after sequence and X-ray structural analyses. Finally, our results show how gene loss can drive the evolution of substrate specificity from retained enzymes.
- Authors:
-
[1]
- Evolution of Metabolic Diversity Laboratory, Unidad de Genómica Avanzada (Langebio), Cinvestav-IPN, Irapuato, Mexico
- Computing, Environment and Life Sciences Directorate, Argonne National Laboratory, Lemont, United States, Computation Institute, University of Chicago, Chicago
- Midwest Center for Structural Genomics, Biosciences Division, Argonne National Laboratory, Lemont, United States, Structural Biology Center, Biosciences Division, Argonne National Laboratory, Lemont, United States
- Department of Microbiology and Molecular Genetics, University of Texas Health Science Center, Houston, United States
- Midwest Center for Structural Genomics, Biosciences Division, Argonne National Laboratory, Lemont, United States
- Cinvestav-IPN, Mexico
- Midwest Center for Structural Genomics, Biosciences Division, Argonne National Laboratory, Lemont, United States, Department of Microbiology and Molecular Genetics, University of Texas Health Science Center, Houston, United States, Department of Biochemistry and Molecular Biology, University of Chicago, Chicago, United States
- Publication Date:
- Research Org.:
- Argonne National Laboratory (ANL), Argonne, IL (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES); Consejo Nacional de Ciencia y Tecnologia (CONACYT); National Science Foundation (NSF); National Institutes of Health (NIH)
- OSTI Identifier:
- 1352728
- Alternate Identifier(s):
- OSTI ID: 1352729; OSTI ID: 1393838
- Grant/Contract Number:
- AC02-06CH11357; 132376; 179290; GM094585; 1611952; DE017382
- Resource Type:
- Published Article
- Journal Name:
- eLife
- Additional Journal Information:
- Journal Name: eLife Journal Volume: 6; Journal ID: ISSN 2050-084X
- Publisher:
- eLife Sciences Publications, Ltd.
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES
Citation Formats
Juárez-Vázquez, Ana Lilia, Edirisinghe, Janaka N., Verduzco-Castro, Ernesto A., Michalska, Karolina, Wu, Chenggang, Noda-García, Lianet, Babnigg, Gyorgy, Endres, Michael, Medina-Ruíz, Sofía, Santoyo-Flores, Julián, Carrillo-Tripp, Mauricio, Ton-That, Hung, Joachimiak, Andrzej, Henry, Christopher S., and Barona-Gómez, Francisco. Evolution of substrate specificity in a retained enzyme driven by gene loss. United States: N. p., 2017.
Web. doi:10.7554/eLife.22679.
Juárez-Vázquez, Ana Lilia, Edirisinghe, Janaka N., Verduzco-Castro, Ernesto A., Michalska, Karolina, Wu, Chenggang, Noda-García, Lianet, Babnigg, Gyorgy, Endres, Michael, Medina-Ruíz, Sofía, Santoyo-Flores, Julián, Carrillo-Tripp, Mauricio, Ton-That, Hung, Joachimiak, Andrzej, Henry, Christopher S., & Barona-Gómez, Francisco. Evolution of substrate specificity in a retained enzyme driven by gene loss. United States. https://doi.org/10.7554/eLife.22679
Juárez-Vázquez, Ana Lilia, Edirisinghe, Janaka N., Verduzco-Castro, Ernesto A., Michalska, Karolina, Wu, Chenggang, Noda-García, Lianet, Babnigg, Gyorgy, Endres, Michael, Medina-Ruíz, Sofía, Santoyo-Flores, Julián, Carrillo-Tripp, Mauricio, Ton-That, Hung, Joachimiak, Andrzej, Henry, Christopher S., and Barona-Gómez, Francisco. Fri .
"Evolution of substrate specificity in a retained enzyme driven by gene loss". United States. https://doi.org/10.7554/eLife.22679.
@article{osti_1352728,
title = {Evolution of substrate specificity in a retained enzyme driven by gene loss},
author = {Juárez-Vázquez, Ana Lilia and Edirisinghe, Janaka N. and Verduzco-Castro, Ernesto A. and Michalska, Karolina and Wu, Chenggang and Noda-García, Lianet and Babnigg, Gyorgy and Endres, Michael and Medina-Ruíz, Sofía and Santoyo-Flores, Julián and Carrillo-Tripp, Mauricio and Ton-That, Hung and Joachimiak, Andrzej and Henry, Christopher S. and Barona-Gómez, Francisco},
abstractNote = {The connection between gene loss and the functional adaptation of retained proteins is still poorly understood. We apply phylogenomics and metabolic modeling to detect bacterial species that are evolving by gene loss, with the finding that Actinomycetaceae genomes from human cavities are undergoing sizable reductions, including loss of L-histidine and L-tryptophan biosynthesis. We observe that the dual-substrate phosphoribosyl isomerase A or priA gene, at which these pathways converge, appears to coevolve with the occurrence oftrpandhisgenes. Characterization of a dozen PriA homologs shows that these enzymes adapt from bifunctionality in the largest genomes, to a monofunctional, yet not necessarily specialized, inefficient form in genomes undergoing reduction. These functional changes are accomplished via mutations, which result from relaxation of purifying selection, in residues structurally mapped after sequence and X-ray structural analyses. Finally, our results show how gene loss can drive the evolution of substrate specificity from retained enzymes.},
doi = {10.7554/eLife.22679},
journal = {eLife},
number = ,
volume = 6,
place = {United States},
year = {Fri Mar 31 00:00:00 EDT 2017},
month = {Fri Mar 31 00:00:00 EDT 2017}
}
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https://doi.org/10.7554/eLife.22679
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Works referenced in this record:
Long-Term Persistence of Bi-functionality Contributes to the Robustness of Microbial Life through Exaptation
journal, January 2016
- Plach, Maximilian G.; Reisinger, Bernd; Sterner, Reinhard
- PLOS Genetics, Vol. 12, Issue 1
AutoDock4 and AutoDockTools4: Automated docking with selective receptor flexibility
journal, December 2009
- Morris, Garrett M.; Huey, Ruth; Lindstrom, William
- Journal of Computational Chemistry, Vol. 30, Issue 16
Extreme genome reduction in symbiotic bacteria
journal, November 2011
- McCutcheon, John P.; Moran, Nancy A.
- Nature Reviews Microbiology, Vol. 10, Issue 1
AutoDock Vina: Improving the speed and accuracy of docking with a new scoring function, efficient optimization, and multithreading
journal, January 2009
- Trott, Oleg; Olson, Arthur J.
- Journal of Computational Chemistry
A substrate ambiguous enzyme facilitates genome reduction in an intracellular symbiont
journal, December 2014
- Price, Daniel RG; Wilson, Alex CC
- BMC Biology, Vol. 12, Issue 1
High-throughput generation, optimization and analysis of genome-scale metabolic models
journal, August 2010
- Henry, Christopher S.; DeJongh, Matthew; Best, Aaron A.
- Nature Biotechnology, Vol. 28, Issue 9
Selection of Conserved Blocks from Multiple Alignments for Their Use in Phylogenetic Analysis
journal, April 2000
- Castresana, J.
- Molecular Biology and Evolution, Vol. 17, Issue 4
Bacterial Adaptation through Loss of Function
journal, July 2013
- Hottes, Alison K.; Freddolino, Peter L.; Khare, Anupama
- PLoS Genetics, Vol. 9, Issue 7
Trimmomatic: a flexible trimmer for Illumina sequence data
journal, April 2014
- Bolger, Anthony M.; Lohse, Marc; Usadel, Bjoern
- Bioinformatics, Vol. 30, Issue 15
Allelic Exchange in Actinomyces oris with mCherry Fluorescence Counterselection
journal, July 2010
- Wu, C.; Ton-That, H.
- Applied and Environmental Microbiology, Vol. 76, Issue 17
Bisubstrate specificity in histidine/tryptophan biosynthesis isomerase from Mycobacterium tuberculosis by active site metamorphosis
journal, February 2011
- Due, Anne V.; Kuper, Jochen; Geerlof, Arie
- Proceedings of the National Academy of Sciences, Vol. 108, Issue 9
Optimization based automated curation of metabolic reconstructions
journal, January 2007
- Satish Kumar, Vinay; Dasika, Madhukar S.; Maranas, Costas D.
- BMC Bioinformatics, Vol. 8, Issue 1
Genomic analysis of a key innovation in an experimental Escherichia coli population
journal, September 2012
- Blount, Zachary D.; Barrick, Jeffrey E.; Davidson, Carla J.
- Nature, Vol. 489, Issue 7417
The effects of alternate optimal solutions in constraint-based genome-scale metabolic models
journal, October 2003
- Mahadevan, R.; Schilling, C. H.
- Metabolic Engineering, Vol. 5, Issue 4
Origins of bacterial diversity through horizontal genetic transfer and adaptation to new ecological niches
journal, September 2011
- Wiedenbeck, Jane; Cohan, Frederick M.
- FEMS Microbiology Reviews, Vol. 35, Issue 5
Evidence for genetic drift in endosymbionts (Buchnera): analyses of protein-coding genes
journal, January 1999
- Wernegreen, J. J.; Moran, N. A.
- Molecular Biology and Evolution, Vol. 16, Issue 1
In Vivo Molecular Evolution Reveals Biophysical Origins of Organismal Fitness
journal, May 2006
- Couñago, Rafael; Chen, Stephen; Shamoo, Yousif
- Molecular Cell, Vol. 22, Issue 4
Velvet: Algorithms for de novo short read assembly using de Bruijn graphs
journal, February 2008
- Zerbino, D. R.; Birney, E.
- Genome Research, Vol. 18, Issue 5
Protein Structure Prediction Using Rosetta
book, January 2004
- Rohl, Carol A.; Strauss, Charlie E. M.; Misura, Kira M. S.
- Methods in Enzymology
The RAST Server: Rapid Annotations using Subsystems Technology
journal, January 2008
- Aziz, Ramy K.; Bartels, Daniela; Best, Aaron A.
- BMC Genomics, Vol. 9, Issue 1, Article No. 75
RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies
journal, January 2014
- Stamatakis, Alexandros
- Bioinformatics, Vol. 30, Issue 9
Reconstruction and Validation of a Genome-Scale Metabolic Model for the Filamentous Fungus Neurospora crassa Using FARM
journal, July 2013
- Dreyfuss, Jonathan M.; Zucker, Jeremy D.; Hood, Heather M.
- PLoS Computational Biology, Vol. 9, Issue 7
Insights into the evolution of enzyme substrate promiscuity after the discovery of (βα)8 isomerase evolutionary intermediates from a diverse metagenome
journal, June 2015
- Noda-García, Lianet; Juárez-Vázquez, Ana L.; Ávila-Arcos, María C.
- BMC Evolutionary Biology, Vol. 15, Issue 1
Phylogenomic Analysis of Natural Products Biosynthetic Gene Clusters Allows Discovery of Arseno-Organic Metabolites in Model Streptomycetes
journal, June 2016
- Cruz-Morales, Pablo; Kopp, Johannes Florian; Martínez-Guerrero, Christian
- Genome Biology and Evolution, Vol. 8, Issue 6
Molecular and Genetic Analyses of Actinomyces SPP
journal, April 1999
- Yeung, M. K.
- Critical Reviews in Oral Biology & Medicine, Vol. 10, Issue 2
HKL -3000: the integration of data reduction and structure solution – from diffraction images to an initial model in minutes
journal, July 2006
- Minor, Wladek; Cymborowski, Marcin; Otwinowski, Zbyszek
- Acta Crystallographica Section D Biological Crystallography, Vol. 62, Issue 8
Evidence for recombination between a sialidase ( nanH ) of Actinomyces naeslundii and Actinomyces oris , previously named ‘ Actinomyces naeslundii genospecies 1 and 2’
journal, November 2008
- Do, Thuy; Henssge, Uta; Gilbert, Steven C.
- FEMS Microbiology Letters, Vol. 288, Issue 2
Occurrence of a putative ancient-like isomerase involved in histidine and tryptophan biosynthesis
journal, February 2003
- Barona-Gómez, Francisco; Hodgson, David A.
- EMBO Reports, Vol. 4, Issue 3
MolProbity : all-atom structure validation for macromolecular crystallography
journal, December 2009
- Chen, Vincent B.; Arendall, W. Bryan; Headd, Jeffrey J.
- Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 1
Coot model-building tools for molecular graphics
journal, November 2004
- Emsley, Paul; Cowtan, Kevin
- Acta Crystallographica Section D Biological Crystallography, Vol. 60, Issue 12, p. 2126-2132
PHENIX: a comprehensive Python-based system for macromolecular structure solution
journal, January 2010
- Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor
- Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2, p. 213-221
MUSCLE: a multiple sequence alignment method with reduced time and space complexity
journal, August 2004
- Edgar, Robert C.
- BMC Bioinformatics, Vol. 5, Issue 1, p. 113
Actinomyces and Related Organisms in Human Infections
journal, March 2015
- Könönen, Eija; Wade, William G.
- Clinical Microbiology Reviews, Vol. 28, Issue 2
Horizontal Transfer, Not Duplication, Drives the Expansion of Protein Families in Prokaryotes
journal, January 2011
- Treangen, Todd J.; Rocha, Eduardo P. C.
- PLoS Genetics, Vol. 7, Issue 1
MrBayes 3.2: Efficient Bayesian Phylogenetic Inference and Model Choice Across a Large Model Space
journal, February 2012
- Ronquist, Fredrik; Teslenko, Maxim; van der Mark, Paul
- Systematic Biology, Vol. 61, Issue 3
Taxonomy, Physiology, and Natural Products of Actinobacteria
journal, November 2015
- Barka, Essaid Ait; Vatsa, Parul; Sanchez, Lisa
- Microbiology and Molecular Biology Reviews, Vol. 80, Issue 1
Phylogenomics and Evolutionary Dynamics of the Family Actinomycetaceae
journal, September 2014
- Zhao, Kelei; Li, Wujiao; Kang, Chunlan
- Genome Biology and Evolution, Vol. 6, Issue 10
Identification and analysis of residues contained on β → α loops of the dual-substrate (βα) 8 phosphoribosyl isomerase A specific for its phosphoribosyl anthranilate isomerase activity
journal, January 2010
- Noda-García, Lianet; Camacho-Zarco, Aldo R.; Verdel-Aranda, Karina
- Protein Science
Co-occurrence of analogous enzymes determines evolution of a novel (βα)8-isomerase sub-family after non-conserved mutations in flexible loop
journal, April 2016
- Verduzco-Castro, Ernesto A.; Michalska, Karolina; Endres, Michael
- Biochemical Journal, Vol. 473, Issue 9
Evolution of Substrate Specificity in a Recipient’s Enzyme Following Horizontal Gene Transfer
journal, June 2013
- Noda-García, Lianet; Camacho-Zarco, Aldo R.; Medina-Ruíz, Sofía
- Molecular Biology and Evolution, Vol. 30, Issue 9
PAML 4: Phylogenetic Analysis by Maximum Likelihood
journal, April 2007
- Yang, Z.
- Molecular Biology and Evolution, Vol. 24, Issue 8
A Genomic Perspective on Protein Families
journal, October 1997
- Tatusov, R. L.
- Science, Vol. 278, Issue 5338
T-coffee: a novel method for fast and accurate multiple sequence alignment 1 1Edited by J. Thornton
journal, September 2000
- Notredame, Cédric; Higgins, Desmond G.; Heringa, Jaap
- Journal of Molecular Biology, Vol. 302, Issue 1
What is flux balance analysis?
journal, March 2010
- Orth, Jeffrey D.; Thiele, Ines; Palsson, Bernhard Ø
- Nature Biotechnology, Vol. 28, Issue 3
Phaser crystallographic software
journal, July 2007
- McCoy, Airlie J.; Grosse-Kunstleve, Ralf W.; Adams, Paul D.
- Journal of Applied Crystallography, Vol. 40, Issue 4
Evolution by gene loss
journal, April 2016
- Albalat, Ricard; Cañestro, Cristian
- Nature Reviews Genetics, Vol. 17, Issue 7
Molden: a pre- and post-processing program for molecular and electronic structures*
journal, February 2000
- Schaftenaar, G.; Noordik, J. H.
- Journal of Computer-Aided Molecular Design, Vol. 14, Issue 2, p. 123-134
RevTrans: multiple alignment of coding DNA from aligned amino acid sequences
journal, July 2003
- Wernersson, R.
- Nucleic Acids Research, Vol. 31, Issue 13
Isolation of a bacteriophage for actinomyces viscosus.
journal, January 1978
- Delisle, A. L.; Nauman, R. K.; Minah, G. E.
- Infection and Immunity, Vol. 20, Issue 1
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journal, January 2020
- Glasner, Margaret E.; Truong, Dat P.; Morse, Benjamin C.
- The FEBS Journal, Vol. 287, Issue 7
Functional Profiling and Crystal Structures of Isothiocyanate Hydrolases Found in Gut-Associated and Plant-Pathogenic Bacteria
journal, May 2018
- van den Bosch, Tijs J. M.; Tan, Kemin; Joachimiak, Andrzej
- Applied and Environmental Microbiology, Vol. 84, Issue 14
Mutations that improve efficiency of a weak-link enzyme are rare compared to adaptive mutations elsewhere in the genome
journal, December 2019
- Morgenthaler, Andrew B.; Kinney, Wallis R.; Ebmeier, Christopher C.
- eLife, Vol. 8
Evolutionary dynamics of natural product biosynthesis in bacteria
journal, January 2020
- Chevrette, Marc G.; Gutiérrez-García, Karina; Selem-Mojica, Nelly
- Natural Product Reports, Vol. 37, Issue 4
A genome scan of diversifying selection in Ophiocordyceps zombie-ant fungi suggests a role for enterotoxins in co-evolution and host specificity
journal, August 2018
- Kobmoo, Noppol; Wichadakul, Duangdao; Arnamnart, Nuntanat
- Molecular Ecology, Vol. 27, Issue 18
Chlamydia trachomatis dapF Encodes a Bifunctional Enzyme Capable of Both D-Glutamate Racemase and Diaminopimelate Epimerase Activities
journal, April 2018
- Liechti, George; Singh, Raghuveer; Rossi, Patricia L.
- mBio, Vol. 9, Issue 2