Evolution of Substrate Specificity in A Retained Enzyme Driven by Gene Loss

Juarez-Vazquez, Ana L.; Edirisinghe, Janaka N.; Verduzco-Castro, Ernesto A.; Michalska, Karolina; Wu, Chenggang; Noda-Garcia, Lianet; Babnigg, Gyorgy; Endres, Michael; Medina-Ruiz, Sofia; Santoyo-Flores, Julian; Carrillo-Tripp, Mauricio; Ton-That, Hung; Joachimiak, Andrzej; Henry, Christopher S.; Barona-Gomez, Francisco

doi:10.7554/eLife.22679.001

Title: Evolution of Substrate Specificity in A Retained Enzyme Driven by Gene Loss

Full Record
Other Related Research

Abstract

The connection between gene loss and the functional adaptation of retained proteins is still poorly understood. Here, 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 also observe that the dual-substrate phosphoribosyl isomerase A or priA gene, at which these pathways converge, appears to coevolve with the occurrence of trp and his genes. 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. These results show how gene loss can drive the evolution of substrate specificity from retained enzymes.

Authors:

Juarez-Vazquez, Ana L. ^[1]; Edirisinghe, Janaka N. ^[2]; Verduzco-Castro, Ernesto A. ^[1]; Michalska, Karolina ^[3]; Wu, Chenggang ^[4]; Noda-Garcia, Lianet ^[1]; Babnigg, Gyorgy ^[5]; Endres, Michael ^[5]; Medina-Ruiz, Sofia ^[1]; Santoyo-Flores, Julian ^[6]; Carrillo-Tripp, Mauricio ^[6]; Ton-That, Hung ^[4]; Joachimiak, Andrzej ^[7]; Henry, Christopher S. ^[2]; Barona-Gomez, Francisco ^[1]

Center for Research and Advanced Studies of the National Polytechnic Inst., Irapuato (Mexico). Evolution of Metabolic Diversity Lab.
Argonne National Lab. (ANL), Argonne, IL (United States). Computing Environment and Life Sciences Directorate; Univ. of Chicago, IL (United States). Computation Inst.
Argonne National Lab. (ANL), Argonne, IL (United States). Midwest Center for Structural Genomics, Structural Biology Center
Univ. of Texas Health Science Center, Houston, TX (United States). Dept. of Microbiology and Molecular Genetics
Argonne National Lab. (ANL), Argonne, IL (United States). Midwest Center for Structural Genomics
Center for Research and Advanced Studies of the National Polytechnic Inst. (Mexico)
Argonne National Lab. (ANL), Argonne, IL (United States). Midwest Center for Structural Genomi; Univ. of Texas Health Science Center, Houston, TX (United States). Dept. of Microbiology and Molecular Genetics; Univ. of Chicago, IL (United States). Dept. of Biochemistry and Molecular Biology

Publication Date:: Fri Mar 31 00:00:00 EDT 2017

Research Org.:: Argonne National Lab. (ANL), Argonne, IL (United States)

Sponsoring Org.:: USDOE Office of Science (SC); National Institutes of Health (NIH); National Science Foundation (NSF)

OSTI Identifier:: 1393154

Grant/Contract Number:: AC02-06CH11357; DE017382; GM094585; 132376; 179290

Resource Type:: Accepted Manuscript

Journal Name:: eLife

Additional Journal Information:: 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; 60 APPLIED LIFE SCIENCES

Citation Formats


                    Juarez-Vazquez, Ana L., Edirisinghe, Janaka N., Verduzco-Castro, Ernesto A., Michalska, Karolina, Wu, Chenggang, Noda-Garcia, Lianet, Babnigg, Gyorgy, Endres, Michael, Medina-Ruiz, Sofia, Santoyo-Flores, Julian, Carrillo-Tripp, Mauricio, Ton-That, Hung, Joachimiak, Andrzej, Henry, Christopher S., and Barona-Gomez, Francisco. Evolution of Substrate Specificity in A Retained Enzyme Driven by Gene Loss.  United States: N. p., 2017. 
Web.  doi:10.7554/eLife.22679.001.

Copy to clipboard


                    Juarez-Vazquez, Ana L., Edirisinghe, Janaka N., Verduzco-Castro, Ernesto A., Michalska, Karolina, Wu, Chenggang, Noda-Garcia, Lianet, Babnigg, Gyorgy, Endres, Michael, Medina-Ruiz, Sofia, Santoyo-Flores, Julian, Carrillo-Tripp, Mauricio, Ton-That, Hung, Joachimiak, Andrzej, Henry, Christopher S., & Barona-Gomez, Francisco. Evolution of Substrate Specificity in A Retained Enzyme Driven by Gene Loss.  United States.  https://doi.org/10.7554/eLife.22679.001

Copy to clipboard


                    Juarez-Vazquez, Ana L., Edirisinghe, Janaka N., Verduzco-Castro, Ernesto A., Michalska, Karolina, Wu, Chenggang, Noda-Garcia, Lianet, Babnigg, Gyorgy, Endres, Michael, Medina-Ruiz, Sofia, Santoyo-Flores, Julian, Carrillo-Tripp, Mauricio, Ton-That, Hung, Joachimiak, Andrzej, Henry, Christopher S., and Barona-Gomez, Francisco. Fri .  
"Evolution of Substrate Specificity in A Retained Enzyme Driven by Gene Loss".  United States.  https://doi.org/10.7554/eLife.22679.001.  https://www.osti.gov/servlets/purl/1393154.

Copy to clipboard


                    
@article{osti_1393154,

  title        = {Evolution of Substrate Specificity in A Retained Enzyme Driven by Gene Loss},

  author       = {Juarez-Vazquez, Ana L. and Edirisinghe, Janaka N. and Verduzco-Castro, Ernesto A. and Michalska, Karolina and Wu, Chenggang and Noda-Garcia, Lianet and Babnigg, Gyorgy and Endres, Michael and Medina-Ruiz, Sofia and Santoyo-Flores, Julian and Carrillo-Tripp, Mauricio and Ton-That, Hung and Joachimiak, Andrzej and Henry, Christopher S. and Barona-Gomez, Francisco},

  abstractNote = {The connection between gene loss and the functional adaptation of retained proteins is still poorly understood. Here, 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 also observe that the dual-substrate phosphoribosyl isomerase A or priA gene, at which these pathways converge, appears to coevolve with the occurrence of trp and his genes. 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. These results show how gene loss can drive the evolution of substrate specificity from retained enzymes.},

  doi          = {10.7554/eLife.22679.001},

  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}

}

Copy to clipboard

Journal Article:

Free Publicly Available Full Text

Accepted Manuscript (DOE)

Publisher's Version of Record

https://doi.org/10.7554/eLife.22679.001

Other availability

Search WorldCat to find libraries that may hold this journal

Save / Share:

Export Metadata

Save to My Library

Similar Records in DOE PAGES and OSTI.GOV collections:

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

Journal Article Juárez-Vázquez, Ana Lilia ; Edirisinghe, Janaka N. ; Verduzco-Castro, Ernesto A. ; ... - eLife

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, inefficientmore »« less
Cited by 19
https://doi.org/10.7554/eLife.22679
Catalytically impaired TrpA subunit of tryptophan synthase from Chlamydia trachomatis is an allosteric regulator of TrpB

Journal Article Michalska, Karolina ; Wellington, Samantha ; Maltseva, Natalia ; ... - Protein Science

Abstract Intracellular growth and pathogenesis of Chlamydia species is controlled by the availability of tryptophan, yet the complete biosynthetic pathway for l‐ Trp is absent among members of the genus. Some representatives, however, preserve genes encoding tryptophan synthase, TrpAB – a bifunctional enzyme catalyzing the last two steps in l‐ Trp synthesis. TrpA (subunit α) converts indole‐3‐glycerol phosphate into indole and glyceraldehyde‐3‐phosphate (α reaction). The former compound is subsequently used by TrpB (subunit β) to produce l‐ Trp in the presence of l‐ Ser and a pyridoxal 5′‐phosphate cofactor (β reaction). Previous studies have indicated that in Chlamydia , TrpAmore »« less
https://doi.org/10.1002/pro.4143
The obligate alkalophilic soda‐lake fungus Sodiomyces alkalinus has shifted to a protein diet

Journal Article Grum‐Grzhimaylo, Alexey A. ; Falkoski, Daniel L. ; van den Heuvel, Joost ; ... - Molecular Ecology

Abstract Sodiomyces alkalinus is one of the very few alkalophilic fungi, adapted to grow optimally at high pH . It is widely distributed at the plant‐deprived edges of extremely alkaline lakes and locally abundant. We sequenced the genome of S. alkalinus and reconstructed evolution of catabolic enzymes, using a phylogenomic comparison. We found that the genome of S. alkalinus is larger, but its predicted proteome is smaller and heavily depleted of both plant‐degrading enzymes and proteinases, when compared to its closest plant‐pathogenic relatives. Interestingly, despite overall losses, S. alkalinus has retained many proteinases families and acquired bacterial cell wall‐degrading enzymes, some of themmore »« less
Cited by 14
https://doi.org/10.1111/mec.14912
Regulation of methane genes and genome expression

Technical Report Reeve, John N

At the start of this project, it was known that methanogens were Archaeabacteria (now Archaea) and were therefore predicted to have gene expression and regulatory systems different from Bacteria, but few of the molecular biology details were established. The goals were then to establish the structures and organizations of genes in methanogens, and to develop the genetic technologies needed to investigate and dissect methanogen gene expression and regulation in vivo. By cloning and sequencing, we established the gene and operon structures of all of the “methane” genes that encode the enzymes that catalyze methane biosynthesis from carbon dioxide and hydrogen.more »« less
https://doi.org/10.2172/963730

Full Text Available
Structural Insight into Allosteric Inhibition of Mycobacterium tuberculosis Tryptophan Synthase

Journal Article Michalska, Karolina ; Wellington, Samantha ; Nag, Partha P. ; ... - FASEB Journal

The rise of antibiotic‐resistant pathogens requires redirecting drug discovery effort toward new cellular targets to provide new treatment options. Such alternative, yet unexplored opportunities exist in central metabolism, where many enzymes are only conditionally essential and thus their successful exploitation requires understanding of metabolic fluxes and pathway regulations under certain environmental conditions. In Mycobacterium tuberculosis , tryptophan biosynthesis represents one such promising pathway that could be targeted. In Mtb, the multistep L‐Trp synthesis involves several enzymes: TrpEG, TrpD, TrpC and TrpAB, which is validated as conditionally essential in vivo . The whole‐cell screening of a diversity‐oriented synthetic library identified amore »« less
https://doi.org/10.1096/fasebj.31.1_supplement.765.12

Similar Records