publication . Article . Other literature type . Preprint . 2019

Molecular function limits divergent protein evolution on planetary timescales

Konaté, Mariam M; Plata, Germán; Park, Jimin; Usmanova, Dinara R; Wang, Harris; Vitkup, Dennis;
Open Access
  • Published: 18 Sep 2019 Journal: eLife, volume 8 (eissn: 2050-084X, Copyright policy)
  • Publisher: eLife Sciences Publications, Ltd
Abstract
Sequence analyses demonstrate that even after billions of years of independent evolution, protein orthologs are still diverging from each other. Although the sequence and functional evolution of proteins have been studied in detail, it is currently unknown whether the requirement to continuously maintain the same molecular function imposes an effective limit on protein divergence. Here we investigate this fundamental question using a combined computational and experimental analysis of orthologous enzymes with the same molecular function. Interestingly, our results demonstrate that the mutual divergence rates of orthologous enzymes substantially decrease after ~1...
Subjects
free text keywords: General Biochemistry, Genetics and Molecular Biology, General Immunology and Microbiology, General Neuroscience, General Medicine, Protein evolution, Biology, Molecular function, Cell biology, Evolutionary biology, Sequence homology, Homology (biology), Fitness effects, Genetics, Functional evolution, Billion years, Bioinformatics, Divergence, Research Communication, orthologous protein, evolution, E. coli
Funded by
NIH| Computational Annotation of Orphan Metabolic Activities
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 5R01GM079759-07
  • Funding stream: NATIONAL INSTITUTE OF GENERAL MEDICAL SCIENCES
,
NIH| MOLECULAR COMPOSITION OF MATURATION PROMOTING FACTOR
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 5F32GM013188-02
  • Funding stream: NATIONAL INSTITUTE OF GENERAL MEDICAL SCIENCES
72 references, page 1 of 5

Adkar, BV, Manhart, M, Bhattacharyya, S, Tian, J, Musharbash, M, Shakhnovich, EI. Optimization of lag phase shapes the evolution of a bacterial enzyme. Nature Ecology & Evolution. 2017; 1: 149 [OpenAIRE] [PubMed] [DOI]

Altschul, SF, Madden, TL, Schäffer, AA, Zhang, J, Zhang, Z, Miller, W, Lipman, DJ. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research. 1997; 25: 3389-3402 [OpenAIRE] [PubMed] [DOI]

Arnold, C, Stadler, PF. Polynomial algorithms for the maximal pairing problem: efficient phylogenetic targeting on arbitrary trees. Algorithms for Molecular Biology. 2010; 5: 25 [OpenAIRE] [PubMed] [DOI]

Bairoch, A. The ENZYME data bank in 1999. Nucleic Acids Research. 1999; 27: 310-311 [OpenAIRE] [PubMed] [DOI]

Barreto, FS, Burton, RS. Evidence for compensatory evolution of ribosomal proteins in response to rapid divergence of mitochondrial rRNA. Molecular Biology and Evolution. 2013; 30: 310-314 [OpenAIRE] [PubMed] [DOI]

Battistuzzi, FU, Feijao, A, Hedges, SB. A genomic timescale of prokaryote evolution: insights into the origin of methanogenesis, Phototrophy, and the colonization of land. BMC Evolutionary Biology. 2004; 4 [OpenAIRE] [PubMed] [DOI]

Bell, EA, Boehnke, P, Harrison, TM, Mao, WL. Potentially biogenic carbon preserved in a 4.1 billion-year-old zircon. PNAS. 2015; 112: 14518-14521 [OpenAIRE] [PubMed] [DOI]

Benkovic, SJ, Fierke, CA, Naylor, AM. Insights into enzyme function from studies on mutants of dihydrofolate reductase. Science. 1988; 239: 1105-1110 [OpenAIRE] [PubMed] [DOI]

Berman, HM, Westbrook, J, Feng, Z, Gilliland, G, Bhat, TN, Weissig, H, Shindyalov, IN, Bourne, PE. The protein data bank. Nucleic Acids Research. 2000; 28: 235-242 [OpenAIRE] [PubMed] [DOI]

Bershtein, S, Serohijos, AW, Bhattacharyya, S, Manhart, M, Choi, JM, Mu, W, Zhou, J, Shakhnovich, EI. Protein homeostasis imposes a barrier on functional integration of horizontally transferred genes in Bacteria. PLOS Genetics. 2015; 11 [OpenAIRE] [PubMed] [DOI]

Betts, HC, Puttick, MN, Clark, JW, Williams, TA, Donoghue, PCJ, Pisani, D. Integrated genomic and fossil evidence illuminates life's early evolution and eukaryote origin. Nature Ecology & Evolution. 2018; 2: 1556-1562 [OpenAIRE] [PubMed] [DOI]

Bork, P, Sander, C, Valencia, A. Convergent evolution of similar enzymatic function on different protein folds: the hexokinase, ribokinase, and galactokinase families of sugar kinases. Protein Science. 1993; 2: 31-40 [OpenAIRE] [PubMed] [DOI]

Breen, MS, Kemena, C, Vlasov, PK, Notredame, C, Kondrashov, FA. Epistasis as the primary factor in molecular evolution. Nature. 2012; 490: 535-538 [OpenAIRE] [PubMed] [DOI]

Chan, YH, Venev, SV, Zeldovich, KB, Matthews, CR. Correlation of fitness landscapes from three orthologous TIM barrels originates from sequence and structure constraints. Nature Communications. 2017; 8 [OpenAIRE] [PubMed] [DOI]

Chang, A, Schomburg, I, Placzek, S, Jeske, L, Ulbrich, M, Xiao, M, Sensen, CW, Schomburg, D. BRENDA in 2015: exciting developments in its 25th year of existence. Nucleic Acids Research. 2015; 43: D439-D446 [OpenAIRE] [PubMed] [DOI]

72 references, page 1 of 5
Abstract
Sequence analyses demonstrate that even after billions of years of independent evolution, protein orthologs are still diverging from each other. Although the sequence and functional evolution of proteins have been studied in detail, it is currently unknown whether the requirement to continuously maintain the same molecular function imposes an effective limit on protein divergence. Here we investigate this fundamental question using a combined computational and experimental analysis of orthologous enzymes with the same molecular function. Interestingly, our results demonstrate that the mutual divergence rates of orthologous enzymes substantially decrease after ~1...
Subjects
free text keywords: General Biochemistry, Genetics and Molecular Biology, General Immunology and Microbiology, General Neuroscience, General Medicine, Protein evolution, Biology, Molecular function, Cell biology, Evolutionary biology, Sequence homology, Homology (biology), Fitness effects, Genetics, Functional evolution, Billion years, Bioinformatics, Divergence, Research Communication, orthologous protein, evolution, E. coli
Funded by
NIH| Computational Annotation of Orphan Metabolic Activities
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 5R01GM079759-07
  • Funding stream: NATIONAL INSTITUTE OF GENERAL MEDICAL SCIENCES
,
NIH| MOLECULAR COMPOSITION OF MATURATION PROMOTING FACTOR
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 5F32GM013188-02
  • Funding stream: NATIONAL INSTITUTE OF GENERAL MEDICAL SCIENCES
72 references, page 1 of 5

Adkar, BV, Manhart, M, Bhattacharyya, S, Tian, J, Musharbash, M, Shakhnovich, EI. Optimization of lag phase shapes the evolution of a bacterial enzyme. Nature Ecology & Evolution. 2017; 1: 149 [OpenAIRE] [PubMed] [DOI]

Altschul, SF, Madden, TL, Schäffer, AA, Zhang, J, Zhang, Z, Miller, W, Lipman, DJ. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research. 1997; 25: 3389-3402 [OpenAIRE] [PubMed] [DOI]

Arnold, C, Stadler, PF. Polynomial algorithms for the maximal pairing problem: efficient phylogenetic targeting on arbitrary trees. Algorithms for Molecular Biology. 2010; 5: 25 [OpenAIRE] [PubMed] [DOI]

Bairoch, A. The ENZYME data bank in 1999. Nucleic Acids Research. 1999; 27: 310-311 [OpenAIRE] [PubMed] [DOI]

Barreto, FS, Burton, RS. Evidence for compensatory evolution of ribosomal proteins in response to rapid divergence of mitochondrial rRNA. Molecular Biology and Evolution. 2013; 30: 310-314 [OpenAIRE] [PubMed] [DOI]

Battistuzzi, FU, Feijao, A, Hedges, SB. A genomic timescale of prokaryote evolution: insights into the origin of methanogenesis, Phototrophy, and the colonization of land. BMC Evolutionary Biology. 2004; 4 [OpenAIRE] [PubMed] [DOI]

Bell, EA, Boehnke, P, Harrison, TM, Mao, WL. Potentially biogenic carbon preserved in a 4.1 billion-year-old zircon. PNAS. 2015; 112: 14518-14521 [OpenAIRE] [PubMed] [DOI]

Benkovic, SJ, Fierke, CA, Naylor, AM. Insights into enzyme function from studies on mutants of dihydrofolate reductase. Science. 1988; 239: 1105-1110 [OpenAIRE] [PubMed] [DOI]

Berman, HM, Westbrook, J, Feng, Z, Gilliland, G, Bhat, TN, Weissig, H, Shindyalov, IN, Bourne, PE. The protein data bank. Nucleic Acids Research. 2000; 28: 235-242 [OpenAIRE] [PubMed] [DOI]

Bershtein, S, Serohijos, AW, Bhattacharyya, S, Manhart, M, Choi, JM, Mu, W, Zhou, J, Shakhnovich, EI. Protein homeostasis imposes a barrier on functional integration of horizontally transferred genes in Bacteria. PLOS Genetics. 2015; 11 [OpenAIRE] [PubMed] [DOI]

Betts, HC, Puttick, MN, Clark, JW, Williams, TA, Donoghue, PCJ, Pisani, D. Integrated genomic and fossil evidence illuminates life's early evolution and eukaryote origin. Nature Ecology & Evolution. 2018; 2: 1556-1562 [OpenAIRE] [PubMed] [DOI]

Bork, P, Sander, C, Valencia, A. Convergent evolution of similar enzymatic function on different protein folds: the hexokinase, ribokinase, and galactokinase families of sugar kinases. Protein Science. 1993; 2: 31-40 [OpenAIRE] [PubMed] [DOI]

Breen, MS, Kemena, C, Vlasov, PK, Notredame, C, Kondrashov, FA. Epistasis as the primary factor in molecular evolution. Nature. 2012; 490: 535-538 [OpenAIRE] [PubMed] [DOI]

Chan, YH, Venev, SV, Zeldovich, KB, Matthews, CR. Correlation of fitness landscapes from three orthologous TIM barrels originates from sequence and structure constraints. Nature Communications. 2017; 8 [OpenAIRE] [PubMed] [DOI]

Chang, A, Schomburg, I, Placzek, S, Jeske, L, Ulbrich, M, Xiao, M, Sensen, CW, Schomburg, D. BRENDA in 2015: exciting developments in its 25th year of existence. Nucleic Acids Research. 2015; 43: D439-D446 [OpenAIRE] [PubMed] [DOI]

72 references, page 1 of 5
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