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Title: Evolution of substrate specificity in a retained enzyme driven by gene loss

Journal Article · · eLife
DOI:https://doi.org/10.7554/eLife.22679· OSTI ID:1352728
 [1];  [2];  [1];  [3];  [4];  [1];  [5];  [5];  [1];  [6];  [6];  [4];  [7];  [2]; ORCiD logo [1]
  1. Evolution of Metabolic Diversity Laboratory, Unidad de Genómica Avanzada (Langebio), Cinvestav-IPN, Irapuato, Mexico
  2. Computing, Environment and Life Sciences Directorate, Argonne National Laboratory, Lemont, United States, Computation Institute, University of Chicago, Chicago
  3. Midwest Center for Structural Genomics, Biosciences Division, Argonne National Laboratory, Lemont, United States, Structural Biology Center, Biosciences Division, Argonne National Laboratory, Lemont, United States
  4. Department of Microbiology and Molecular Genetics, University of Texas Health Science Center, Houston, United States
  5. Midwest Center for Structural Genomics, Biosciences Division, Argonne National Laboratory, Lemont, United States
  6. Cinvestav-IPN, Mexico
  7. 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
+ Show Author Affiliations

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.

Research Organization:
Argonne National Laboratory (ANL), Argonne, IL (United States)
Sponsoring Organization:
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)
Grant/Contract Number:
AC02-06CH11357; 132376; 179290; GM094585; 1611952; DE017382
OSTI ID:
1352728
Alternate ID(s):
OSTI ID: 1352729; OSTI ID: 1393838
Journal Information:
eLife, Journal Name: eLife Vol. 6; ISSN 2050-084X
Publisher:
eLife Sciences Publications, Ltd.Copyright Statement
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 19 works
Citation information provided by
Web of Science

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Cited By (6)

How enzyme promiscuity and horizontal gene transfer contribute to metabolic innovation journal January 2020
Functional Profiling and Crystal Structures of Isothiocyanate Hydrolases Found in Gut-Associated and Plant-Pathogenic Bacteria journal May 2018
Mutations that improve efficiency of a weak-link enzyme are rare compared to adaptive mutations elsewhere in the genome journal December 2019
Evolutionary dynamics of natural product biosynthesis in bacteria journal January 2020
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
Chlamydia trachomatis dapF Encodes a Bifunctional Enzyme Capable of Both D-Glutamate Racemase and Diaminopimelate Epimerase Activities journal April 2018

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