Microbiology in the post-genomic era

Genomics has revolutionized every aspect of microbiology. Now, 13 years after the first bacterial genome was sequenced, it is important to pause and consider what has changed in microbiology research as a consequence of genomics. In this article, we review the evolving field of bacterial typing and the genomic technologies that enable comparative analysis of multiple genomes and the metagenomes of complex microbial environments, and address the implications of the genomic era for the future of microbiology.

[1]  M. Simon,et al.  Phase variation in Salmonella: genetic analysis of a recombinational switch. , 1979, Proceedings of the National Academy of Sciences of the United States of America.

[2]  J. M. Prober,et al.  A system for rapid DNA sequencing with fluorescent chain-terminating dideoxynucleotides. , 1987, Science.

[3]  D. Relman,et al.  The importance of individuals and scale: moving towards single cell microbiology. , 2007, Environmental microbiology.

[4]  Evan Powell,et al.  Comparative Genomic Analyses of Seventeen Streptococcus pneumoniae Strains: Insights into the Pneumococcal Supragenome , 2007, Journal of bacteriology.

[5]  O. White,et al.  Environmental Genome Shotgun Sequencing of the Sargasso Sea , 2004, Science.

[6]  D. Relman,et al.  An ecological and evolutionary perspective on human–microbe mutualism and disease , 2007, Nature.

[7]  Mihai Pop,et al.  Comparative Genome Sequencing for Discovery of Novel Polymorphisms in Bacillus anthracis , 2002, Science.

[8]  R. Knight,et al.  The Human Microbiome Project , 2007, Nature.

[9]  Julian Parkhill,et al.  Re-annotation and re-analysis of the Campylobacter jejuni NCTC11168 genome sequence , 2007, BMC Genomics.

[10]  Richard Moxon,et al.  Bacterial contingency loci: the role of simple sequence DNA repeats in bacterial adaptation. , 2006, Annual review of genetics.

[11]  R. Rappuoli,et al.  Genome Analysis Reveals Pili in Group B Streptococcus , 2005, Science.

[12]  F. Sanger,et al.  DNA sequencing with chain-terminating inhibitors. , 1977, Proceedings of the National Academy of Sciences of the United States of America.

[13]  M. Pop,et al.  Metagenomic Analysis of the Human Distal Gut Microbiome , 2006, Science.

[14]  Daniel Falush,et al.  A bimodal pattern of relatedness between the Salmonella Paratyphi A and Typhi genomes: convergence or divergence by homologous recombination? , 2006, Genome research.

[15]  Madabhushi Rs,et al.  Separation of 4‐color DNA sequencing extension products in noncovalently coated capillaries using low viscosity polymer solutions , 1998, Electrophoresis.

[16]  J. Joanny,et al.  Fast DNA translocation through a solid-state nanopore. , 2004, Nano letters.

[17]  R. Rappuoli Reverse vaccinology : Genomics , 2000 .

[18]  C. Buchrieser,et al.  Genomic diversity and evolution within the species Streptococcus agalactiae. , 2006, Microbes and infection.

[19]  Clive Brown,et al.  Toward the $1000 human genome , 2005 .

[20]  Edward A Graviss,et al.  Genome-wide analysis of synonymous single nucleotide polymorphisms in Mycobacterium tuberculosis complex organisms: resolution of genetic relationships among closely related microbial strains. , 2002, Genetics.

[21]  M. Achtman,et al.  Multilocus sequence typing: a portable approach to the identification of clones within populations of pathogenic microorganisms. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[22]  F. Blattner,et al.  Extensive mosaic structure revealed by the complete genome sequence of uropathogenic Escherichia coli , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[23]  Harald Huber,et al.  A new phylum of Archaea represented by a nanosized hyperthermophilic symbiont , 2002, Nature.

[24]  Guy Plunkett,et al.  Comparative Genomics of Salmonellaenterica Serovar Typhi Strains Ty2 and CT18 , 2003, Journal of bacteriology.

[25]  E. Rocha,et al.  The complete genome sequence of the murine respiratory pathogen Mycoplasma pulmonis. , 2001, Nucleic acids research.

[26]  D. Dykhuizen,et al.  Enterobacterial adhesins and the case for studying SNPs in bacteria. , 2003, Trends in microbiology.

[27]  H. Tettelin,et al.  The microbial pan-genome. , 2005, Current opinion in genetics & development.

[28]  D. Relman,et al.  Assembly of the human intestinal microbiota. , 2006, Trends in ecology & evolution.

[29]  G. Dykes,et al.  An SNP-based PCR assay to differentiate between Listeria monocytogenes lineages derived from phylogenetic analysis of the sigB gene. , 2003, Journal of microbiological methods.

[30]  D. Falush,et al.  Inference of Bacterial Microevolution Using Multilocus Sequence Data , 2007, Genetics.

[31]  J. Banfield,et al.  Community structure and metabolism through reconstruction of microbial genomes from the environment , 2004, Nature.

[32]  K. Konstantinidis,et al.  The bacterial species definition in the genomic era , 2006, Philosophical Transactions of the Royal Society B: Biological Sciences.

[33]  W. Doolittle,et al.  Genomics and the bacterial species problem , 2006, Genome Biology.

[34]  Claudio Donati,et al.  Protein Homology Network Families Reveal Step-Wise Diversification of Type III and Type IV Secretion Systems , 2006, PLoS Comput. Biol..

[35]  W B Whitman,et al.  Relationship of 16S rRNA sequence similarity to DNA hybridization in prokaryotes. , 2001, International journal of systematic and evolutionary microbiology.

[36]  B. Levin,et al.  Genetic diversity in relation to serotype in Escherichia coli , 1985, Infection and immunity.

[37]  N. W. Davis,et al.  Genome sequence of enterohaemorrhagic Escherichia coli O157:H7 , 2001, Nature.

[38]  S. Acinas,et al.  Fine-scale phylogenetic architecture of a complex bacterial community , 2004, Nature.

[39]  Venugopal Thiruvenkataswamy,et al.  Identification and interrogation of highly informative single nucleotide polymorphism sets defined by bacterial multilocus sequence typing databases. , 2004, Journal of medical microbiology.

[40]  M. Hattori,et al.  Genomic analysis of Bacteroides fragilis reveals extensive DNA inversions regulating cell surface adaptation. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[41]  James R. Knight,et al.  Genome sequencing in microfabricated high-density picolitre reactors , 2005, Nature.

[42]  Tanja Popovic,et al.  Sequencing of 16S rRNA Gene: A Rapid Tool for Identification of Bacillus anthracis , 2002, Emerging infectious diseases.

[43]  R. Ley,et al.  Ecological and Evolutionary Forces Shaping Microbial Diversity in the Human Intestine , 2006, Cell.

[44]  G. Dougan,et al.  The genome of Salmonella enterica serovar Typhi. , 2007, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[45]  Jonathan Crabtree,et al.  Global Phylogeny of Mycobacterium tuberculosis Based on Single Nucleotide Polymorphism (SNP) Analysis: Insights into Tuberculosis Evolution, Phylogenetic Accuracy of Other DNA Fingerprinting Systems, and Recommendations for a Minimal Standard SNP Set , 2006, Journal of bacteriology.

[46]  B. Barrell,et al.  The genome sequence of the food-borne pathogen Campylobacter jejuni reveals hypervariable sequences , 2000, Nature.

[47]  C. Buchrieser,et al.  How to become a uropathogen: Comparative genomic analysis of extraintestinal pathogenic Escherichia coli strains , 2006, Proceedings of the National Academy of Sciences.

[48]  E. Mardis,et al.  An obesity-associated gut microbiome with increased capacity for energy harvest , 2006, Nature.

[49]  D. Branton,et al.  Characterization of individual polynucleotide molecules using a membrane channel. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[50]  R. Simons,et al.  Reverse Transcriptase-Mediated Tropism Switching in Bordetella Bacteriophage , 2002, Science.

[51]  C. Dekker,et al.  Translocation of double-strand DNA through a silicon oxide nanopore. , 2005, Physical review. E, Statistical, nonlinear, and soft matter physics.

[52]  Edward M. Rubin,et al.  Metagenomics: DNA sequencing of environmental samples , 2005, Nature Reviews Genetics.

[53]  H. Ochman,et al.  Lateral gene transfer and the nature of bacterial innovation , 2000, Nature.

[54]  Justin S. Hogg,et al.  Characterization and modeling of the Haemophilus influenzae core and supragenomes based on the complete genomic sequences of Rd and 12 clinical nontypeable strains , 2007, Genome Biology.

[55]  D. Caugant,et al.  Clonal diversity of Neisseria meningitidis from a population of asymptomatic carriers , 1988, Infection and immunity.

[56]  D. Relman Genome-wide responses of a pathogenic bacterium to its host. , 2002, The Journal of clinical investigation.

[57]  S. Schuster Next-generation sequencing transforms today's biology , 2008, Nature Methods.

[58]  Ulrich Dobrindt,et al.  Genomic islands in pathogenic and environmental microorganisms , 2004, Nature Reviews Microbiology.

[59]  R. Fleischmann,et al.  Modeling Bacterial Evolution with Comparative-Genome-Based Marker Systems: Application to Mycobacterium tuberculosis Evolution and Pathogenesis , 2003, Journal of bacteriology.

[60]  Lloyd M. Smith,et al.  Fluorescence detection in automated DNA sequence analysis , 1986, Nature.

[61]  R. Rappuoli,et al.  Reverse vaccinology. , 2000, Current opinion in microbiology.

[62]  D. Relman,et al.  The meaning and impact of the human genome sequence for microbiology. , 2001, Trends in microbiology.

[63]  B. Barrell,et al.  Sequencing and analysis of the genome of the Whipple's disease bacterium Tropheryma whipplei , 2003, The Lancet.

[64]  Benjamin J. Raphael,et al.  The Sorcerer II Global Ocean Sampling Expedition: Expanding the Universe of Protein Families , 2007, PLoS biology.

[65]  S. Salzberg,et al.  Complete genome sequence of Neisseria meningitidis serogroup B strain MC58. , 2000, Science.

[66]  F. Neidhardt,et al.  Escherichia Coli and Salmonella: Typhimurium Cellular and Molecular Biology , 1987 .

[67]  E. Purdom,et al.  Diversity of the Human Intestinal Microbial Flora , 2005, Science.

[68]  Marcy Yann,et al.  ヒト口腔からの微量の培養されないTM7微生物の単一細胞遺伝分析による生物学的「不明な物体」の詳細な分析 , 2007 .

[69]  T. Popović,et al.  Sequence Diversity of Neisseria meningitidis 16S rRNA Genes and Use of 16S rRNA Gene Sequencing as a Molecular Subtyping Tool , 2002, Journal of Clinical Microbiology.

[70]  G. Macfarlane,et al.  Microbial colonization of the upper gastrointestinal tract in patients with Barrett's esophagus. , 2007, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[71]  J. Handelsman Metagenomics: Application of Genomics to Uncultured Microorganisms , 2004, Microbiology and Molecular Biology Reviews.

[72]  S. Tringe,et al.  Comparative Metagenomics of Microbial Communities , 2004, Science.

[73]  Kamlesh Jangid,et al.  Comparison of 16S rRNA gene sequences of genus Methanobrevibacter , 2004, BMC Microbiology.

[74]  C. Fraser-Liggett,et al.  Insights on biology and evolution from microbial genome sequencing. , 2005, Genome research.

[75]  Mark Achtman,et al.  Evolutionary History of Salmonella Typhi , 2006, Science.

[76]  H. Tettelin,et al.  Towards a universal group B Streptococcus vaccine using multistrain genome analysis , 2006, Expert review of vaccines.

[77]  S. Quake,et al.  Dissecting biological “dark matter” with single-cell genetic analysis of rare and uncultivated TM7 microbes from the human mouth , 2007, Proceedings of the National Academy of Sciences.

[78]  J. Venter,et al.  Identification of vaccine candidates against serogroup B meningococcus by whole-genome sequencing. , 2000, Science.

[79]  S. Quake,et al.  Sequence information can be obtained from single DNA molecules , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[80]  D. Relman,et al.  How Bacterial Communities Expand Functional Repertoires , 2006, PLoS biology.

[81]  Neil Hall,et al.  Advanced sequencing technologies and their wider impact in microbiology , 2007, Journal of Experimental Biology.

[82]  B. Barrell,et al.  Complete DNA sequence of a serogroup A strain of Neisseria meningitidis Z2491 , 2000, Nature.

[83]  T. Whittam,et al.  Methods of multilocus enzyme electrophoresis for bacterial population genetics and systematics , 1986, Applied and environmental microbiology.

[84]  Benjamin L. King,et al.  Genomic-sequence comparison of two unrelated isolates of the human gastric pathogen Helicobacter pylori , 1999, Nature.

[85]  C. T. Farley,et al.  Accurate Multiplex Polony Sequencing of an Evolved Bacterial Genome , 2008 .

[86]  Edward C. Holmes,et al.  Distribution of Surface Protein Variants among Hyperinvasive Meningococci: Implications for Vaccine Design , 2004, Infection and Immunity.

[87]  A. Halpern,et al.  The Sorcerer II Global Ocean Sampling Expedition: Northwest Atlantic through Eastern Tropical Pacific , 2007, PLoS biology.

[88]  Clive Brown,et al.  Toward the 1,000 dollars human genome. , 2005, Pharmacogenomics.

[89]  H. Tettelin,et al.  Identification of a Universal Group B Streptococcus Vaccine by Multiple Genome Screen , 2005, Science.

[90]  Martin C. J. Maiden,et al.  mlstdbNet – distributed multi-locus sequence typing (MLST) databases , 2004, BMC Bioinformatics.

[91]  Jaideep P. Sundaram,et al.  Genome analysis of multiple pathogenic isolates of Streptococcus agalactiae: implications for the microbial "pan-genome". , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[92]  Lisa C. Crossman,et al.  Extensive DNA Inversions in the B. fragilis Genome Control Variable Gene Expression , 2005, Science.

[93]  Nigel Goldenfeld,et al.  Biology's next revolution , 2007, Nature.

[94]  A. Halpern,et al.  A Sanger/pyrosequencing hybrid approach for the generation of high-quality draft assemblies of marine microbial genomes. , 2006, Proceedings of the National Academy of Sciences of the United States of America.