Computational Prediction of Genomic Functional Cores Specific to Different Microbes

Journal of Molecular Evolution - Tập 63 Số 6 - Trang 733-746 - 2006
Carbone, Alessandra1
1Génomique Analytique, Université Pierre et Marie Curie-Paris 6, INSERM U511, 91, Bd de I’Hôpital, Paris, France

Tóm tắt

Computational and experimental attempts tried to characterize a universial core of genes representing the minimal set of functional needs for an organism. Based on the increasing number of available complete genomes, comparative genomics has concluded that the universal core contains < 50 genes. In contrast, experiments suggest a much larger set of essential genes (certainly more than several hundreds, even under the most restrictive hypotheses) that is dependent on the biological complexity and environmental specificity of the organism. Highly biased genes, which are generally also the most expressed in translationally biased organisms, tend to be over represented in the class of genes deemed to be essential for any given bacterial species. This association is far from perfect; nevertheless, it allows us to propose a new computational method to detect, to a certain extent, ubiquitous genes, nonorthologous genes, environment-specific genes, genes involved in the stress response, and genes with no identified function but highly likely to be essential for the cell. Most of these groups of genes cannot be identified with previously attempted computational and experimental approaches. The large variety of life-styles and the unusually detectable functional signals characterizing translationally biased organisms suggest using them as reference organisms to infer essentiality in other microbial species. The case of small parasitic genomes is discussed. Data issued by the analysis are compared with previous computational and experimental studies. Results are discussed both on methodological and biological grounds.

Tài liệu tham khảo

citation_journal_title=Proc Natl Acad Sci USA; citation_title=A minimal gene set for cellular life derived by comparison of complete bacterial genomes; citation_author=AR Mushegian, EV Koonin; citation_volume=93; citation_publication_date=1996; citation_pages=10268-10273; citation_doi=10.1073/pnas.93.19.10268; citation_id=CR1

citation_journal_title=Science; citation_title=The minimal gene complement of Mycoplasma genitalium

; citation_author=CM Fraser, JD Gocayne, O White, MD Adams, RA Clayton, RD Fleischmann, CJ Bult, AR Kerlavage, G Sutton, JM Kelley, RD Fritchman; citation_volume=270; citation_publication_date=1995; citation_pages=397-403; citation_doi=10.1126/science.270.5235.397; citation_id=CR2

citation_journal_title=Science; citation_title=Whole-genome random sequencing and assembly of Haemophilus influenzae Rd

; citation_author=RD Fleischmann, MD Adams, O White, RA Clayton, EF Kirkness, AR Kerlavage, CJ Bult, JF Tomb, DA Dougherty, JM Merrick; citation_volume=269; citation_publication_date=1995; citation_pages=496-512; citation_doi=10.1126/science.7542800; citation_id=CR3

citation_journal_title=Genome Res; citation_title=Comparative genomics of the archaea (euryarchaeota): Evolution of conserved protein families, the stable core, and the variable shell; citation_author=KS Makarova, L Aravind, MY Galperin, NV Grishin, RL Tatusov, YI Wolf, EV Koonin; citation_volume=9; citation_publication_date=2003; citation_pages=608-628; citation_id=CR4

citation_journal_title=Mol Evol; citation_title=Defining the core of non-transferable prokaryotic genes: The euryarchaeal core; citation_author=CL Nesbø, Y Boucher, WF Doolittle; citation_volume=53; citation_publication_date=2001; citation_pages=340-350; citation_doi=10.1007/s002390010224; citation_id=CR5

citation_journal_title=Genome Res; citation_title=The genetic core of the universal ancestor; citation_author=JK Harris, JT Kelley, GB Spiegelman, NR Pace; citation_volume=13; citation_publication_date=2003; citation_pages=407-412; citation_doi=10.1101/gr.652803; citation_id=CR6

citation_journal_title=Nat Genet; citation_title=Universal trees based on large combined protein sequence data sets; citation_author=JR Brown, CJ Douady, MJ Italia, WE Marshall, MJ Stanhope; citation_volume=28; citation_publication_date=2001; citation_pages=281-285; citation_doi=10.1038/90129; citation_id=CR7

citation_journal_title=Nat Rev Microbiol; citation_title=Comparative genomics, minimal gene sets and the last common ancestor; citation_author=EV Koonin; citation_volume=1; citation_publication_date=2003; citation_pages=127-136; citation_doi=10.1038/nrmicro751; citation_id=CR8

citation_journal_title=Genome Res; citation_title=Computing prokaryotic gene ubiquity: Rescuing the core from extinction; citation_author=RL Charlebois, WF Doolittle; citation_volume=14; citation_publication_date=2004; citation_pages=2469-2477; citation_doi=10.1101/gr.3024704; citation_id=CR9

citation_journal_title=FEBS Lett; citation_title=An estimation of the minimal genome size required for life; citation_author=M Itaya; citation_volume=362; citation_publication_date=1995; citation_pages=257-260; citation_doi=10.1016/0014-5793(95)00233-Y; citation_id=CR10

citation_journal_title=Proc Natl Acad Sci USA; citation_title=Essential Bacillus subtilis genes; citation_author=K Kobayashi, SD Ehrlich, A Albertini, G Amati, KK Anderson, M Arnaud, K Asai, S Ashikaga, S Aymerich, P Bessieres; citation_volume=100; citation_publication_date=2003; citation_pages=4678-4683; citation_doi=10.1073/pnas.0730515100; citation_id=CR11

citation_journal_title=Science; citation_title=Global transposon mutagenesis and a minimal Mycoplasma genome; citation_author=CA Hutchison, SN Peterson Gill, RT Cline, O White, CM Fraser, HO Smith, JC Venter; citation_volume=286; citation_publication_date=1999; citation_pages=2165-2169; citation_doi=10.1126/science.286.5447.2165; citation_id=CR12

citation_journal_title=Proc Natl Acad Sci USA; citation_title=Essential genes of a minimal bacterium; citation_author=JI Glass, N Assad-Garcia, N Alperovich, S Yooseph, MR Lewis, M Maruf, III CA Hutchison, HO Smith, JC Venter; citation_volume=103; citation_publication_date=2006; citation_pages=425-430; citation_doi=10.1073/pnas.0510013103; citation_id=CR13

citation_journal_title=Proc Natl Acad Sci USA; citation_title=A genome-scale analysis for identification of genes required for growth or survival of Haemophilus influenzae

; citation_author=BJ Akerley, EJ Rubin, VL Novick, K Amaya, N Judson, JJ Mekalanos; citation_volume=99; citation_publication_date=2002; citation_pages=966-971; citation_doi=10.1073/pnas.012602299; citation_id=CR14

citation_journal_title=J Bacteriol; citation_title=Experimental determination and system level analysis of essential genes in Escherichia coli MG 1655; citation_author=SY Gerdes, MD Scholle, JW Campbell, G Balazsi, E Ravasz, MD Daugherty, AL Somera, NC Kyrpides, I Anderson, MS Gelfand, A Bhattacharya; citation_volume=185; citation_publication_date=2003; citation_pages=5673-5684; citation_doi=10.1128/JB.185.19.5673-5684.2003; citation_id=CR15

citation_journal_title=Mol Microbiol; citation_author=null Hashimoto; citation_volume=55; citation_publication_date=2005; citation_pages=137; citation_doi=10.1111/j.1365-2958.2004.04386.x; citation_id=CR16

citation_journal_title=J Bacteriol; citation_title=Global transposon mutagenesis and essential gene analysis of Helicobacter pylori

; citation_author=NR Salama; citation_volume=186; citation_publication_date=2004; citation_pages=7926-7935; citation_doi=10.1128/JB.186.23.7926-7935.2004; citation_id=CR17

citation_journal_title=Mol Microbiol; citation_title=A genome-wide strategy for the identification of essential genes in Staphylococcus aureus

; citation_author=RA Forsyth; citation_volume=43; citation_publication_date=2002; citation_pages=1387-1400; citation_doi=10.1046/j.1365-2958.2002.02832.x; citation_id=CR19

citation_journal_title=Nucleic Acids Res; citation_title=Identification of 113 conserved essential genes using a high-throughput gene disruption system in Streptococcus pneumoniae

; citation_author=JA Thanassi; citation_volume=30; citation_publication_date=2002; citation_pages=3152-3162; citation_doi=10.1093/nar/gkf418; citation_id=CR20

citation_journal_title=Science; citation_title=Functional characterization of the S. cerevisiae genome by gene deletion and parallel analysis; citation_author=EA Winzeler, DD Shoemaker, A Astromoff, H Liang, K Anderson, B Andre, R Bangham, R Benito, JD Boeke, H Bussey; citation_volume=285; citation_publication_date=1999; citation_pages=901-906; citation_doi=10.1126/science.285.5429.901; citation_id=CR21

citation_journal_title=Nature; citation_title=Functional of the Saccharomyces cerevisiae genome; citation_author=G Giaever, AM Chu, L Ni, C Connelly, L Riles, S Veronneau, S Dow, A Lucau-Danila, K Anderson, B Andre; citation_volume=418; citation_publication_date=2002; citation_pages=387-391; citation_doi=10.1038/nature00935; citation_id=CR22

citation_journal_title=Nature; citation_title=Systematic functional analysis of the Caenorhabditis elegans genome using RNAi; citation_author=RS Kamath, AG Fraser, Y Dong, G Poulin, R Durbin, M Gotta, A Kanapin, N Le Bot, S Moreno, M Sohrmann; citation_volume=421; citation_publication_date=2003; citation_pages=231-237; citation_doi=10.1038/nature01278; citation_id=CR23

citation_journal_title=J Bacteriol; citation_title=DNA sequence and complementation analysis of a mutation in the rplX gene from Escherichia coli leading to loss of ribosomal protein L24; citation_author=K Nishi, ER Dabbs, J Schnier; citation_volume=163; citation_publication_date=1985; citation_pages=890-894; citation_id=CR24

citation_journal_title=J Bacteriol; citation_title=From genetic footprinting to Antimicrobial drug targets: Examples in cofactor biosynthetic pathways; citation_author=SY Gerdes, MD Scholle, M D’Souza, MV Bernal, A Baev, M Farrell, OV Kurnasov, MD Daugherty, F Mseeh, BM Polanuger; citation_volume=184; citation_publication_date=2002; citation_pages=4555-4572; citation_doi=10.1128/JB.184.16.4555-4572.2002; citation_id=CR25

citation_journal_title=Nucleic Acids Res; citation_title=Codon catalog usage and the genome hypothesis; citation_author=R Grantham, C Gautier, M Gouy, R Mercier, A Pave; citation_volume=8; citation_publication_date=1980; citation_pages=r49-r62; citation_id=CR26

citation_journal_title=Nucleic Acid Research; citation_title=The codon adaptation index - a measure of directional synonymous codon usage bias, and its potential applications; citation_author=PM Sharp, W-H Li; citation_volume=15; citation_publication_date=1987; citation_pages=1281-1295; citation_id=CR27

citation_journal_title=J Mol Evol; citation_title=Insights on the evolution of metabolic networks of unicellular translationally biased organisms from transcriptomic data and sequence analysis; citation_author=A Carbone, R Madden; citation_volume=61; citation_publication_date=2005; citation_pages=456-469; citation_doi=10.1007/s00239-004-0317-z; citation_id=CR29

citation_journal_title=Mol Biol Evol; citation_title=Codon bias signatures, organisation of microorganisms in codon space and lifestyle; citation_author=A Carbone, F Képés, A Zinovyev; citation_volume=22; citation_publication_date=2004; citation_pages=547-561; citation_doi=10.1093/molbev/msi040; citation_id=CR30

citation_journal_title=Mol Biol Evol; citation_title=How essential are nonessential genes?; citation_author=G Fang, E Rocha, A Danchin; citation_volume=22; citation_publication_date=2005; citation_pages=2147-2156; citation_doi=10.1093/molbev/msi211; citation_id=CR31

citation_journal_title=Mol Cell Biol; citation_title=Correlation between protein and mRNA abundance in yeast; citation_author=SP Gygi, Y Rochon, BR Franza, R Aebersold; citation_volume=19; citation_publication_date=1999; citation_pages=1720-1730; citation_id=CR32

citation_journal_title=Genome Res; citation_title=A phylogenomic approach to bacterial phylogeny: Evidence of a core of genes sharing a common history; citation_author=V Daubin, M Gouy, G Perriuere; citation_volume=12; citation_publication_date=2002; citation_pages=1080-1090; citation_doi=10.1101/gr.187002; citation_id=CR33

citation_journal_title=PLoS Biol; citation_title=From gene trees to organismal phylogeny in prokaryotes: The case of the γ-proteobacteria; citation_author=E Lerat, V Daubin, NA Moran; citation_volume=1; citation_publication_date=2003; citation_pages=E19; citation_doi=10.1371/journal.pbio.0000019; citation_id=CR34

citation_journal_title=Nucleic Acids Res; citation_title=Identification of thermophilic species by the amino-acids composition deduced from their genomes; citation_author=PD Kreil, CA Ouzounis; citation_volume=29; citation_publication_date=2001; citation_pages=1608-1615; citation_doi=10.1093/nar/29.7.1608; citation_id=CR35

citation_journal_title=Nucleic Acids Res; citation_title=Synonymous codon usage is subject to selection in thermophilic bacteria; citation_author=DJ Lynn, GA Singer, DA Hickey; citation_volume=30; citation_publication_date=2002; citation_pages=4272-4277; citation_doi=10.1093/nar/gkf546; citation_id=CR36

citation_journal_title=Gene; citation_title=Amino acid composition of genomes, lifestyles of organisms, and evolutionary trends: A global picture with correspondence analysis; citation_author=F Tekaia, E Yeramian, B Dujon; citation_volume=297; citation_publication_date=2002; citation_pages=51-60; citation_doi=10.1016/S0378-1119(02)00871-5; citation_id=CR37

citation_journal_title=Nucleic Acids Res; citation_title=Variation in the strength of selected codon usage bias among bacteria; citation_author=PM Sharp, E Bailes, RJ Grocock, JF Peden, RE Sockett; citation_volume=33; citation_publication_date=2005; citation_pages=1141-1153; citation_doi=10.1093/nar/gki242; citation_id=CR38

citation_journal_title=Nature Genetics; citation_title=A massive parallelism, randomness and genomic advances; citation_author=JC Venter, S Levy, T Stockwell, K Remington, A Halpern; citation_volume=33; citation_publication_date=2003; citation_pages=219-227; citation_doi=10.1038/ng1114; citation_id=CR39

citation_journal_title=Science; citation_title=Genomics. Tinker, tailor: Can Venter stitch together a genome from scratch?; citation_author=C Zimmer; citation_volume=299; citation_publication_date=2003; citation_pages=1006-1007; citation_doi=10.1126/science.299.5609.1006; citation_id=CR40

citation_journal_title=Nucleic Acids Res; citation_title=Over-representation of repeats in stress response genes: A strategy to increase versatility under stressful conditions?; citation_author=EP Rocha, I Matic, F Taddei; citation_volume=30; citation_publication_date=2002; citation_pages=1886-1894; citation_doi=10.1093/nar/30.9.1886; citation_id=CR42

citation_journal_title=Annu Rev Genomics Hum Genet; citation_title=How many genes can make a cell: The minimal-gene-set concept; citation_author=EV Koonin; citation_volume=1; citation_publication_date=2000; citation_pages=99-116; citation_doi=10.1146/annurev.genom.1.1.99; citation_id=CR43

citation_journal_title=Genome Res; citation_title=The genome of M. acetivorans reveals extensive metabolic and physiological diversity; citation_author=JE Galagan, C Nusbaum, A Roy, MG Endrizzi, P Macdonald, W FitzHugh, S Calvo, R Engels, S Smirnov, D Atnoor; citation_volume=12; citation_publication_date=2002; citation_pages=532-542; citation_doi=10.1101/gr.223902; citation_id=CR44

citation_journal_title=Mol Microbiol; citation_title=An integrated analysis of the genome of the hyperthermophilic archaeon Pyrococcus abyssi

; citation_author=GN Cohen, V Barbe, D Flament, M Galperin, R Heilig, O Lecompte, O Poch, D Prieur, J Querellou, R Ripp; citation_volume=47; citation_publication_date=2003; citation_pages=1495-1512; citation_doi=10.1046/j.1365-2958.2003.03381.x; citation_id=CR45

citation_journal_title=Eur J Biochem; citation_title=Enzymes of hydrogen metabolism in Pyrococcus furiosus

; citation_author=PJ Silva, EC Ban, H Wassink, HCB Haaker, FT Robb, WR Hagen; citation_volume=267; citation_publication_date=2000; citation_pages=6541-6551; citation_doi=10.1046/j.1432-1327.2000.01745.x; citation_id=CR46

citation_journal_title=J Bacteriol; citation_title=DNA microarray analysis of the hyperthermophilic archaeon Pyrococcus furiosus: Evidence for a new type of sulfur-reducing enzyme complex; citation_author=GJ Schut, J Zhou, MW Adams; citation_volume=183; citation_publication_date=2001; citation_pages=7027-7036; citation_doi=10.1128/JB.183.24.7027-7036.2001; citation_id=CR47

citation_journal_title=J Bacteriol; citation_title=Purification and characterization of the alanine aminotransferase from the hyperthermophilic Archaeon Pyrococcus furiosus and its role in alanine production; citation_author=DE Ward, SW Kengen, J Oost, WM Vos; citation_volume=182; citation_publication_date=2000; citation_pages=2559-2566; citation_doi=10.1128/JB.182.9.2559-2566.2000; citation_id=CR48

citation_journal_title=Proc Natl Acad Sci USA; citation_title=Genome sequence of Streptococcus mutans UA159, a cariogenic dental pathogen; citation_author=D Ajdić, WM McShan, RE McLaughlin, G Savic, J Chang, MB Carson, C Primeaux, R Tian, S Kenton, H Jia; citation_volume=99; citation_publication_date=2002; citation_pages=14434-14439; citation_doi=10.1073/pnas.172501299; citation_id=CR49

citation_journal_title=J Bacteriol; citation_title=Studies of the processing of the protease which initiates degradation of small, acid-soluble proteins during germination of spores of Bacillus species

; citation_author=B Illades-Aguiar, P Setlow; citation_volume=176; citation_publication_date=1994; citation_pages=2788-2795; citation_id=CR50

citation_journal_title=Proc Natl Acad Sci USA; citation_title=Extreme genome reduction in Buchnera spp.: Toward the minimal genome needed for symbiotic life; citation_author=R Gil, B Sabater-Muoz, A Latorre, FJ Silva, A Moya; citation_volume=99; citation_publication_date=2002; citation_pages=4454-4458; citation_doi=10.1073/pnas.062067299; citation_id=CR51

citation_journal_title=Nature Genet; citation_title=Genome sequence of the endocellular obligate symbiont of tsetse flies, Wigglesworthia glossinidia

; citation_author=L Akman, A Yamashita, H Watanabe, K Oshima, T Shiba, M Hattori, S Aksoy; citation_volume=32; citation_publication_date=2002; citation_pages=402-407; citation_doi=10.1038/ng986; citation_id=CR52

citation_journal_title=Proc Natl Acad Sci USA; citation_title=Reductive genome evolution in Buchnera aphidicola

; citation_author=RCHJ Ham, J Kamerbeek, C Palacios, C Rausell, F Abascal, U Bastolla, JM Fernández, L Jiménez, M Postigo, FJ Silva, J Tamames, E Viguera, A Latorre, A Valencia, F Morán, A Moya; citation_volume=100; citation_publication_date=2003; citation_pages=581-586; citation_doi=10.1073/pnas.0235981100; citation_id=CR53

citation_journal_title=Microbiol Mol Biol Rev; citation_title=Metabolic interdependence of obligate intracellular bacteria and their insect hosts; citation_author=E Zientz, T Dandekar, R Gross; citation_volume=68; citation_publication_date=2004; citation_pages=745-770; citation_doi=10.1128/MMBR.68.4.745-770.2004; citation_id=CR54

citation_journal_title=Mol Microbiol; citation_title=Comparison of archaeal and bacterial genomes: Computer analysis of protein sequences predicts novel functions and suggests a chimeric origin of the archaea; citation_author=EV Koonin, AR Mushegian, MY Galperin, DR Walker; citation_volume=25; citation_publication_date=1997; citation_pages=619-637; citation_doi=10.1046/j.1365-2958.1997.4821861.x; citation_id=CR55