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Evolution of tryptophan biosynthetic pathway in microbial genomes: a comparative genetic study

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Systems and Synthetic Biology

Abstract

Biosynthetic pathway evolution needs to consider the evolution of a group of genes that code for enzymes catalysing the multiple chemical reaction steps leading to the final end product. Tryptophan biosynthetic pathway has five chemical reaction steps that are highly conserved in diverse microbial genomes, though the genes of the pathway enzymes show considerable variations in arrangements, operon structure (gene fusion and splitting) and regulation. We use a combined bioinformatic and statistical analyses approach to address the question if the pathway genes from different microbial genomes, belonging to a wide range of groups, show similar evolutionary relationships within and between them. Our analyses involved detailed study of gene organization (fusion/splitting events), base composition, relative synonymous codon usage pattern of the genes, gene expressivity, amino acid usage, etc. to assess inter- and intra-genic variations, between and within the pathway genes, in diverse group of microorganisms. We describe these genetic and genomic variations in the tryptophan pathway genes in different microorganisms to show the similarities across organisms, and compare the same genes across different organisms to find the possible variability arising possibly due to horizontal gene transfers. Such studies form the basis for moving from single gene evolution to pathway evolutionary studies that are important steps towards understanding the systems biology of intracellular pathways.

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References

  • Akashi H, Gojobori T (2002) Metabolic efficiency and amino acid composition in the proteomes of Escherichia coli and Bacillus subtilis. Proc Natl Acad Sci USA 99:3695–3700

    Article  CAS  PubMed  Google Scholar 

  • Barona-Gómez F, Hodgson DA (2003) Occurrence of a putative ancient-like isomerase involved in histidine and tryptophan biosynthesis. EMBO Rep 4(3):296–300

    Google Scholar 

  • Beiko RG, Harlow TJ, Ragan MA (2005) Highways of gene sharing in prokaryotes. Proc Natl Acad Sci USA 102:14332–14337

    Article  CAS  PubMed  Google Scholar 

  • Bentley R (1990) The shikimate pathway—a metabolic tree with many branches. Crit Rev Biochem Mol Biol 25:307–384

    Article  CAS  PubMed  Google Scholar 

  • Benzecri JP (1992) The correspondence analysis handbook. Statistics: textbooks and monographs 125. Marcel Dekker, New York

    Google Scholar 

  • Carbone A, Zinovyev A, Kepes F (2003) Codon adaptation index as a measure of dominating codon bias. Bioinformatics 19:2005–2015

    Article  CAS  PubMed  Google Scholar 

  • Carlini DB, Chen Y, Stephan W (2001) The relationship between third-codon position nucleotide content, codon bias, mRNA secondary structure and gene expression in the drosophilid alcohol dehydrogenase genes adh and adhr. Genetics 159:623–633

    CAS  PubMed  Google Scholar 

  • Chanda I, Pan A, Dutta C (2005) Proteome composition in Plasmodium falciparum: higher usage of GC-rich nonsynonymous codons in highly expressed genes. J Mol Evol 61:513–523

    Article  CAS  PubMed  Google Scholar 

  • Crawford IP (1975) Gene rearrangements in the evolution of the tryptophan synthetic pathway. Bacteriol Rev 39:87–120

    CAS  PubMed Central  PubMed  Google Scholar 

  • Crawford IP (1989) Evolution of a biosynthetic pathway: the tryptophan paradigm. Annu Rev Microbiol 43:567–600

    Article  CAS  PubMed  Google Scholar 

  • Dagan T, Martin W (2007) Ancestral genome size specify the minimum rate of lateral gene transfer during prokaryote evolution. Proc Natl Acad Sci USA 104:870–875

    Article  CAS  PubMed  Google Scholar 

  • Das S, Paul S, Chatterjee S, Dutta C (2005) Codon and amino acid usage in two major human pathogens of genus Bartonella—optimization between replicational-transcriptional selection, translational control and cost minimization. DNA Res 12:91–102

    Article  CAS  PubMed  Google Scholar 

  • Doolittle WF (2004) Microbial phylogeny and evolution: concepts and controversies. In: Sapp J (ed) Oxford Univ Press, New York, pp 119–133

  • Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32(5):1792–1797

    Article  CAS  Google Scholar 

  • Eisen JA (2000) Horizontal gene transfer among microbial genomes: new insights from complete genome analysis. Curr Opin Genet Dev 10:606–611

    Article  CAS  PubMed  Google Scholar 

  • Felsenstein J (1989) PHYLIP–phylogeny inference package (version 3.2). Cladistics 5:164–166

    Google Scholar 

  • Felsenstein J (2003) Inferring phylogenies. Sinauer Associates Inc, Massachusetts

    Google Scholar 

  • Flowers JM, Sezgin E, Kumagai S, Duvernell DD, Matzkin LM, Schmidt PS, Eanes WF (2007) Adaptive evolution of metabolic pathways in Drosophila. Mol Biol Evol 24(6):1347–1354

    Article  CAS  PubMed  Google Scholar 

  • Garcia-Vallve S, Romeu A, Palau J (2000) Horizontal gene transfer in bacterial and archaeal complete genomes. Genome Res 10:1719–1725

    Article  CAS  PubMed  Google Scholar 

  • Garcia-Vallve S, Guzman E, Montero MA, Romeu A (2003) HGT-DB: a database of putative horizontally transferred genes in prokaryotic complete genomes. Nucleic Acids Res 31:187–189

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ge F, Wang LS, Kim J (2005) The cobweb of life revealed by genome-scale estimates of horizontal gene transfer. PLoS Biol 3:e316

    Article  PubMed Central  PubMed  Google Scholar 

  • Ghosh TC, Gupta SK, Majumdar S (2000) Studies on codon usage in Entamoeba histolytica. Int J Parasitol 30(6):715–722

    Article  CAS  PubMed  Google Scholar 

  • Gogarten JP, Doolittle WF, Lawrence JG (2002) Prokaryotic evolution in light of gene transfer. Mol Biol Evol 19:2226–2238

    Article  CAS  PubMed  Google Scholar 

  • Gouy M, Gautier C (1982) Codon usage in bacteria: correlation with gene expressivity. Nucleic Acid Res 10(22):7055–7074

    Google Scholar 

  • Grantham R, Gautier C, Gouy M, Mercier R, Pave A (1980) Codon catalogue usage and genome hypothesis. Nucleic Acid Res 8:r49–r62

    CAS  PubMed  Google Scholar 

  • Grantham R, Gautier C, Gouy M, Jacobzone M, Mercier R (1981) Codon catalog usage is a genome strategy modulated for gene expressivity. Nucleic Acid Res 9(1):r43–r74

    Article  CAS  PubMed  Google Scholar 

  • Greenacre MJ (1984) Theory and applications of correspondence analysis. Academic, London

    Google Scholar 

  • Grocock RJ, Sharp PM (2002) Synonymous codon usage in Pseudomonas aeruginosa PA01. Gene 289:131–139

    Article  CAS  PubMed  Google Scholar 

  • Gupta SK, Ghosh TC (2001) Gene expressivity is the main factor in dictating the codon usage variation among the genes in Pseudomonas aeruginosa. Gene 273:63–70

    Article  CAS  PubMed  Google Scholar 

  • Hao W, Golding GB (2006) The fate of laterally transferred genes: life in the fast lane to adaptation or death. Genome Res 16:636–643

    Article  CAS  PubMed  Google Scholar 

  • Invergo BM, Montanucci L, Laayouni H, Bertranpetit J (2013) A system-level, molecular evolutionary analysis of mammalian phototransduction. BMC Evol Biol 13:52

    Google Scholar 

  • Jansen R, Bussemaker HJ, Gerstein M (2003) Revisiting the codon adaptation index from a whole-genome perspective: analyzing the relationship between gene expression and codon occurrence in yeast using a variety of models. Nucleic Acids Res 31:2242–2251

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Jardine O, Gough J, Chothia C, Teichmann SA (2002) Comparison of the small molecule metabolic enzymes of Escherichia coli and Saccharomyces cerevisiae. Genome Res 12(6):916–929

    Article  CAS  PubMed  Google Scholar 

  • Kanehisa M, Araki M, Goto S, Hattori M, Hirakawa M, Itoh M, Katayama T, Kawashima S, Okuda S, Tokimatsu T, Yamanishi Y (2007) KEGG for linking genomes to life and the environment Nucleic Acids Res 36:D480–D484

    Article  Google Scholar 

  • Karlin S, Mrazek J (1996) What drives codon choices in human genes? J Mol Biol 262:459–472

    Article  CAS  PubMed  Google Scholar 

  • Kunin V, Ouzounis CA (2003) The balance of driving forces during genome evolution in prokaryotes. Genome Res 13:1589–1594

    Article  CAS  PubMed  Google Scholar 

  • Kurland CG (2005) What tangled web: barriers to rampant horizontal gene transfer. BioEssays 27:741–747

    Article  CAS  PubMed  Google Scholar 

  • Kurland CG, Canback B, Berg OG (2003) Horizontal gene transfer: a critical view. Proc Natl Acad Sci USA 100:9658–9662

    Article  CAS  PubMed  Google Scholar 

  • Lawrence JG, Roth JR (1996) Selfish operons: horizontal transfer may drive the evolution of gene clusters. Genetics 143:1843–1860

    CAS  PubMed  Google Scholar 

  • Lynn DJ, Singer GAC, Hickey DA (2002) Synonymous codon usage is subject to selection in thermophilic bacteria; Nucleic Acids Res 30:4272–4277

    CAS  Google Scholar 

  • Merino E, Jensen RA, Yanofsky C (2008) Evolution of bacterial trp operons and their regulation. Curr Opin Microbiol 11(2):78–86

    Google Scholar 

  • Moszer I, Rocha EP, Danchin A (1999) Codon usage and lateral gene transfer in Bacilus subtilis. Curr Opin Microbiol 2:524–528

    Article  CAS  PubMed  Google Scholar 

  • Mrazek J, Karlin S (1999) Detecting alien genes in bacterial genomes. Ann NY Acad Sci 870:314–329

    Article  CAS  PubMed  Google Scholar 

  • Nakamura Y, Itoh T, Matsuda H, Gojobori T (2004) Biased biological functions of horizontally transferred genes in prokaryotic genomes. Nat Genet 36:760–766

    Article  CAS  PubMed  Google Scholar 

  • Nelson KE, Clayton RA, Gill SR, Gwinn ML, Dodson RJ, Haft DH, Hickey EK, Peterson JD, Nelson WC, Ketchum KA, McDonald L, Utterback TR, Malek JA, Linher KD, Garrett MM, Stewart AM, Cotton MD, Pratt MS, Phillips CA, Richardson D, Heidelberg J, Sutton GG, Fleischmann RD, Eisen JA, White O, Salzberg SL, Smith HO, Venter JC, Fraser CM (1999) Evidence for lateral gene transfer between Archaea and Bacteria from genome sequence of Thermotoga maritima. Nature 399:323–329

    Article  CAS  PubMed  Google Scholar 

  • Nelson-Sathi S, Dagan T, Landan G, Janssen A, Steel M, McInerney JO, Deppenmeier U, Martin WF (2012) Acquisition of 1, 000 eubacterial genes physiologically transformed a methanogen at the origin of Haloarchaea. Proc Natl Acad Sci USA 109(50):20537–20542

    Article  CAS  PubMed  Google Scholar 

  • Ochman H, Lawrence JG, Groisman EA (2000) Lateral gene transfer and the nature of bacterial innovation. Nature 405:299–304

    Article  CAS  PubMed  Google Scholar 

  • Peden JF (1999) CodonW, (http://sourceforge.net/projects/codonw/)

  • Rison SCG, Thornton JM (2002) Pathway evolution, structurally speaking. Curr Opin Struct Biol 12:374–382

    Article  CAS  PubMed  Google Scholar 

  • Seligmann H (2003) Cost minimization of amino acid usage. J Mol Evol 56:151–161

    Article  CAS  PubMed  Google Scholar 

  • Sharp PM, Li WH (1986) An evolutionary perspective on synonymous codon usage in unicellular organisms. J Mol Evol 24(1–2):28–38

    Google Scholar 

  • Sharp PM, Li WH (1987) The codon adaptation index—a measure of directional synonymous codon usage bias, and its potential applications. Nucleic Acids Res 15:1281–1295

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Sharp PM, Tuohy TM, Mosurski KR (1986) Codon usage in yeast: cluster analysis clearly differentiates highly and lowly expressed genes. Nucleic Acids Res 14(13):5125–5143

    Google Scholar 

  • Suzuki H, Saito R, Tomita M (2005) A problem in multivariate analysis of codon usage data and a possible solution. FEBS Lett 579:6499–6504

    Article  CAS  PubMed  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    Article  CAS  Google Scholar 

  • Watt WB, Dean AM (2000) Molecular functional studies of adaptive genetic variation in prokaryotes and eukaryotes. Annu Rev Genet 34:593–622

    Article  CAS  PubMed  Google Scholar 

  • Woese CR (2000) Interpreting the universal phylogenetic tree. Proc Natl Acad Sci USA 97:8392–8396

    Article  CAS  PubMed  Google Scholar 

  • Xie G, Forst C, Bonner C, Jensen RA (2001) Significance of two distinct types of tryptophan synthase beta chain in Bacteria, Archaea and higher plants. Genome Biol 3:0004.1–0004.13

    Article  Google Scholar 

  • Xie G, Bonner CA, Jensen RA (2002) Dynamic diversity of the tryptophan pathway in chlamydiae: reductive evolution and a novel operon for tryptophan recapture. Genome Biol 3(9):00511–005117

    Article  Google Scholar 

  • Xie G, Keyhani NO, Bonner CA, Jensen RA (2003a) Ancient origin of the tryptophan operon and the dynamics of evolutionary change. Microbiol Mol Biol Rev 67:303–342

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Xie G, Bonner CA, Brettin T, Gottardo R, Keyhani NO, Jensen RA (2003b) Lateral gene transfer and ancient paralogy of operons containing redundant copies of tryptophan-pathway genes in Xylella species and in heterocystous cyanobacteria. Genome Biol 4(R14):1–18

    Google Scholar 

  • Xie G, Bonner CA, Song J, Keyhani NO, Jensen RA (2004) Inter-genomic displacement via lateral gene transfer of bacterial trp operons in an overall context of vertical genealogy. BMC Biol 2:15. doi:10.1186/1741-7007-2-15

    Article  PubMed Central  PubMed  Google Scholar 

  • Yanofsky C (2001) Advancing our knowledge in biochemistry, genetics, and microbiology through studies on tryptophan metabolism. Annu Rev Biochem 70:1–37

    Google Scholar 

  • Yanofsky C, Platt T, Crawford IP, Nichols BP, Christie GE, Horowitz H, Van Cleemput M, Wu AM (1981) The complete nucleotide sequence of the tryptophan operon of Escherichia coli. Nucleic Acids Res 9(24):6647–6668

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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Acknowledgments

The authors thank Council for Scientific and Industrial Research, India for Senior Research Fellowship to Priya V K, and Department of Biotechnology, India for financial support to S. Sarkar. Somdatta Sinha thanks Department of Science and Technology India for the J. C. Bose Fellowship, and the Santa Fe Institute, USA for the Senior International Fellowship during early stages of the work.

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Authors and Affiliations

  1. CSIR-Centre for Cellular and Molecular Biology, Uppal Road, Hyderabad, India

    V. K. Priya & Susmita Sarkar

  2. Department of Biological Sciences, Indian Institute of Science Education and Research (IISER) Mohali, Knowledge City, Sector 81, SAS Nagar, Manauli P. O., Mohali, 140306, Punjab, India

    Somdatta Sinha

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  1. V. K. Priya
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Correspondence to Somdatta Sinha.

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Priya, V.K., Sarkar, S. & Sinha, S. Evolution of tryptophan biosynthetic pathway in microbial genomes: a comparative genetic study. Syst Synth Biol 8, 59–72 (2014). https://doi.org/10.1007/s11693-013-9127-1

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