Global phenotypic characterization of bacteria

The measure of the quality of a systems biology model is how well it can reproduce and predict the behaviors of a biological system such as a microbial cell. In recent years, these models have been built up in layers, and each layer has been growing in sophistication and accuracy in parallel with a global data set to challenge and validate the models in predicting the content or activities of genes (genomics), proteins (proteomics), metabolites (metabolomics), and ultimately cell phenotypes (phenomics). This review focuses on the latter, the phenotypes of microbial cells. The development of Phenotype MicroArrays, which attempt to give a global view of cellular phenotypes, is described. In addition to their use in fleshing out and validating systems biology models, there are many other uses of this global phenotyping technology in basic and applied microbiology research, which are also described.

[1]  Rachel L. Edwards,et al.  SpoT governs Legionella pneumophila differentiation in host macrophages , 2009, Molecular microbiology.

[2]  L. Giovannetti,et al.  Florence Conference on Phenotype Microarray Analysis of Microorganisms—The Environment, Agriculture, and Human Health 19–21 March 2008, Florence, Italy , 2008, Annals of Microbiology.

[3]  Rachel L. Edwards,et al.  Legionella pneumophila couples fatty acid flux to microbial differentiation and virulence. , 2009, Molecular microbiology.

[4]  Ian T. Paulsen,et al.  High-Throughput Phenotypic Characterization of Pseudomonas aeruginosa Membrane Transport Genes , 2008, PLoS genetics.

[5]  Carlo Viti,et al.  Important discoveries from analysing bacterial phenotypes , 2008, Molecular microbiology.

[6]  I. Paulsen,et al.  RamA Confers Multidrug Resistance in Salmonella enterica via Increased Expression of acrB, Which Is Inhibited by Chlorpromazine , 2008, Antimicrobial Agents and Chemotherapy.

[7]  M. Schmoll,et al.  Photostimulation of Hypocrea atroviridis growth occurs due to a cross-talk of carbon metabolism, blue light receptors and response to oxidative stress. , 2008, Microbiology.

[8]  M. E. Hochberg,et al.  Diversity and productivity peak at intermediate dispersal rate in evolving metacommunities , 2008, Nature.

[9]  Jason A. Papin,et al.  * Corresponding authors , 2006 .

[10]  Gail M Preston,et al.  Pseudomonas syringae pv. tomato DC3000 uses constitutive and apoplast-induced nutrient assimilation pathways to catabolize nutrients that are abundant in the tomato apoplast. , 2008, Molecular plant-microbe interactions : MPMI.

[11]  P. Rainey,et al.  Dual Involvement of CbrAB and NtrBC in the Regulation of Histidine Utilization in Pseudomonas fluorescens SBW25 , 2008, Genetics.

[12]  T. Cebula,et al.  Altered Utilization of N-Acetyl-d-Galactosamine by Escherichia coli O157:H7 from the 2006 Spinach Outbreak , 2007, Journal of bacteriology.

[13]  Judith Berman,et al.  Haplotype Mapping of a Diploid Non-Meiotic Organism Using Existing and Induced Aneuploidies , 2007, PLoS genetics.

[14]  Wayne L. Nicholson,et al.  Uncovering New Metabolic Capabilities of Bacillus subtilis Using Phenotype Profiling of Rifampin-Resistant rpoB Mutants , 2007, Journal of bacteriology.

[15]  H. Mori,et al.  The applications of systematic in-frame, single-gene knockout mutant collection of Escherichia coli K-12. , 2008, Methods in molecular biology.

[16]  Yukako Tohsato,et al.  Phenotype profiling of single gene deletion mutants of E. coli using Biolog technology. , 2008, Genome informatics. International Conference on Genome Informatics.

[17]  L. Giovannetti,et al.  Characterization of Chromate‐Resistant and ‐Reducing Bacteria by Traditional Means and by a High‐Throughput Phenomic Technique for Bioremediation Purposes , 2008, Biotechnology progress.

[18]  C. Knight,et al.  Integrated bioinformatic and phenotypic analysis of RpoN-dependent traits in the plant growth-promoting bacterium Pseudomonas fluorescens SBW25. , 2007, Environmental microbiology.

[19]  Marcel H Zwietering,et al.  Metabolic capacity of Bacillus cereus strains ATCC 14579 and ATCC 10987 interlinked with comparative genomics. , 2007, Environmental microbiology.

[20]  Irina S Druzhinina,et al.  Carbon Source Dependence and Photostimulation of Conidiation in Hypocrea atroviridis , 2007, Applied and Environmental Microbiology.

[21]  Amy K. Schmid,et al.  The anatomy of microbial cell state transitions in response to oxygen. , 2007, Genome research.

[22]  B. Palsson,et al.  Genome-scale Reconstruction of Metabolic Network in Bacillus subtilis Based on High-throughput Phenotyping and Gene Essentiality Data* , 2007, Journal of Biological Chemistry.

[23]  Irina S Druzhinina,et al.  Application of DNA Bar Codes for Screening of Industrially Important Fungi: the Haplotype of Trichoderma harzianum Sensu Stricto Indicates Superior Chitinase Formation , 2007, Applied and Environmental Microbiology.

[24]  T. Mascher,et al.  Regulatory Overlap and Functional Redundancy among Bacillus subtilis Extracytoplasmic Function σ Factors , 2007, Journal of bacteriology.

[25]  J. Vázquez-Boland,et al.  The PrfA virulence regulon. , 2007, Microbes and infection.

[26]  Adam M. Feist,et al.  A genome-scale metabolic reconstruction for Escherichia coli K-12 MG1655 that accounts for 1260 ORFs and thermodynamic information , 2007, Molecular systems biology.

[27]  Chung-Dar Lu,et al.  Regulation of Carbon and Nitrogen Utilization by CbrAB and NtrBC Two-Component Systems in Pseudomonas aeruginosa , 2007, Journal of bacteriology.

[28]  Pei Yee Ho,et al.  Multiple High-Throughput Analyses Monitor the Response of E. coli to Perturbations , 2007, Science.

[29]  G. Schoolnik,et al.  Genomic and Phenotypic Diversity of Coastal Vibrio cholerae Strains Is Linked to Environmental Factors , 2007, Applied and Environmental Microbiology.

[30]  Mi-Jeong Yoon,et al.  Escherichia coli enzyme IIANtr regulates the K+ transporter TrkA , 2007, Proceedings of the National Academy of Sciences.

[31]  W. Shi,et al.  β-d-Allose Inhibits Fruiting Body Formation and Sporulation in Myxococcus xanthus , 2006, Journal of bacteriology.

[32]  R. Gast,et al.  Linkage of avian and reproductive tract tropism with sequence divergence adjacent to the 5S ribosomal subunit rrfH of Salmonella enterica. , 2006, FEMS microbiology letters.

[33]  I. Paulsen,et al.  Contribution of Target Gene Mutations and Efflux to Decreased Susceptibility of Salmonella enterica Serovar Typhimurium to Fluoroquinolones and Other Antimicrobials , 2006, Antimicrobial Agents and Chemotherapy.

[34]  David J. Baumler,et al.  H-NS controls metabolism and stress tolerance in Escherichia coli O157:H7 that influence mouse passage , 2006, BMC Microbiology.

[35]  I. Glomski,et al.  Regulated translation of listeriolysin O controls virulence of Listeria monocytogenes , 2006, Molecular microbiology.

[36]  Irina S Druzhinina,et al.  A screening system for carbon sources enhancing beta-N-acetylglucosaminidase formation in Hypocrea atroviridis (Trichoderma atroviride). , 2006, Microbiology.

[37]  M. Jacques,et al.  Fhua and HgbA, outer membrane proteins of Actinobacillus pleuropneumoniae: their role as virulence determinants. , 2006, Canadian journal of microbiology.

[38]  W. Inwood,et al.  A previously undescribed pathway for pyrimidine catabolism. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[39]  M. Schmoll,et al.  Global Carbon Utilization Profiles of Wild-Type, Mutant, and Transformant Strains of Hypocrea jecorina , 2006, Applied and Environmental Microbiology.

[40]  Iman Chouikha,et al.  A selC-Associated Genomic Island of the Extraintestinal Avian Pathogenic Escherichia coli Strain BEN2908 Is Involved in Carbohydrate Uptake and Virulence , 2006, Journal of bacteriology.

[41]  M. Ziman,et al.  Phenotype Microarray Profiling of Staphylococcus aureus menD and hemB Mutants with the Small-Colony-Variant Phenotype , 2006, Journal of bacteriology.

[42]  T. Cebula,et al.  Exploring Genotypic and Phenotypic Diversity of Microbes Using Microarray Approaches , 2006, Toxicology mechanisms and methods.

[43]  E. Muñoz-Elías,et al.  Carbon metabolism of intracellular bacteria , 2006, Cellular microbiology.

[44]  M. Sasser,et al.  1 1 IDENTIFICATION OF MICROORGANISMS USING FATTY ACID METHYL ESTER ( FAME ) ANALYSIS AND THE MIDI SHERLOCK ® MICROBIAL IDENTIFICATION SYSTEM , 2006 .

[45]  Mi-Jeong Yoon,et al.  Requirement of the dephospho‐form of enzyme IIANtr for derepression of Escherichia coli K‐12 ilvBN expression , 2005, Molecular microbiology.

[46]  I. Biswas,et al.  Role of HtrA in Surface Protein Expression and Biofilm Formation by Streptococcus mutans , 2005, Infection and Immunity.

[47]  S. Porwollik,et al.  Correlation of Phenotype with the Genotype of Egg-Contaminating Salmonella enterica Serovar Enteritidis , 2005, Applied and Environmental Microbiology.

[48]  J. Sauer,et al.  The phagosomal transporter A couples threonine acquisition to differentiation and replication of Legionella pneumophila in macrophages. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[49]  M. Bibb,et al.  Regulation of secondary metabolism in streptomycetes. , 2005, Current opinion in microbiology.

[50]  P. Rodríguez-Palenzuela,et al.  Role of the PhoP-PhoQ System in the Virulence of Erwinia chrysanthemi Strain 3937: Involvement in Sensitivity to Plant Antimicrobial Peptides, Survival at Acid pH, and Regulation of Pectolytic Enzymes , 2005, Journal of bacteriology.

[51]  T. V. Van Dyk,et al.  Characterization of the Escherichia coli AaeAB Efflux Pump: a Metabolic Relief Valve? , 2004, Journal of bacteriology.

[52]  L. Durso,et al.  Measurements of Fitness and Competition in Commensal Escherichia coli and E. coli O157:H7 Strains , 2004, Applied and Environmental Microbiology.

[53]  Mi-Jeong Yoon,et al.  A Novel Fermentation/Respiration Switch Protein Regulated by Enzyme IIAGlc in Escherichia coli* , 2004, Journal of Biological Chemistry.

[54]  J. W. Campbell,et al.  Gene array analysis of Yersinia enterocolitica FlhD and FlhC: regulation of enzymes affecting synthesis and degradation of carbamoylphosphate. , 2004, Microbiology.

[55]  W. Goebel,et al.  New Listeria monocytogenes prfA* mutants, transcriptional properties of PrfA* proteins and structure–function of the virulence regulator PrfA , 2004, Molecular microbiology.

[56]  Markus J. Herrgård,et al.  Integrating high-throughput and computational data elucidates bacterial networks , 2004, Nature.

[57]  T. Humphrey,et al.  Subpopulation Characteristics of Egg-Contaminating Salmonella enterica serovar Enteritidis as Defined by the Lipopolysaccharide O Chain , 2004, Applied and Environmental Microbiology.

[58]  B. Wanner,et al.  Phenotype MicroArray Analysis of Escherichia coli K-12 Mutants with Deletions of All Two-Component Systems , 2003, Journal of bacteriology.

[59]  G. Bell,et al.  Divergent evolution during an experimental adaptive radiation , 2003, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[60]  K. Forchhammer,et al.  Carbon-source-dependent nitrogen regulation in Escherichia coli is mediated through glutamine-dependent GlnB signalling. , 2003, Microbiology.

[61]  B. Bochner Innovations: New technologies to assess genotype–phenotype relationships , 2003, Nature Reviews Genetics.

[62]  J. W. Campbell,et al.  FlhD/FlhC Is a Regulator of Anaerobic Respiration and the Entner-Doudoroff Pathway through Induction of the Methyl-Accepting Chemotaxis Protein Aer , 2003, Journal of bacteriology.

[63]  G. Bell,et al.  Experimental Adaptive Radiation in Pseudomonas , 2002, The American Naturalist.

[64]  A. Eisenstark,et al.  Carbon and nitrogen substrate utilization by archival Salmonella typhimurium LT2 cells , 2002, BMC Evolutionary Biology.

[65]  B. Schierwater,et al.  Speciation and phylogeography in the cosmopolitan marine moon jelly, Aurelia sp , 2002, BMC Evolutionary Biology.

[66]  W. Goebel,et al.  Hpt, a bacterial homolog of the microsomal glucose- 6-phosphate translocase, mediates rapid intracellular proliferation in Listeria , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[67]  H. Liu,et al.  Transcriptional control of dimorphism in Candida albicans. , 2001, Current opinion in microbiology.

[68]  W. Goebel,et al.  Listeria Pathogenesis and Molecular Virulence Determinants , 2001, Clinical Microbiology Reviews.

[69]  B. Bochner,et al.  Phenotype microarrays for high-throughput phenotypic testing and assay of gene function. , 2001, Genome research.

[70]  R. Lenski,et al.  The population genetics of ecological specialization in evolving Escherichia coli populations , 2000, Nature.

[71]  B. Wanner,et al.  One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[72]  J. Miller,et al.  The consequences of growth of a mutator strain of Escherichia coli as measured by loss of function among multiple gene targets and loss of fitness. , 2000, Genetics.

[73]  F. Neidhardt,et al.  Diagnosis of cellular states of microbial organisms using proteomics , 1999, Electrophoresis.

[74]  J. Berman,et al.  Linkage of adhesion, filamentous growth, and virulence in Candida albicans to a single gene, INT1. , 1998, Science.

[75]  J. Vázquez-Boland,et al.  Glucose-1-phosphate utilization by Listeria monocytogenes is PrfA dependent and coordinately expressed with virulence factors , 1997, Journal of bacteriology.

[76]  E. Groisman,et al.  Mg2+ as an Extracellular Signal: Environmental Regulation of Salmonella Virulence , 1996, Cell.

[77]  R. Fleischmann,et al.  The Minimal Gene Complement of Mycoplasma genitalium , 1995, Science.

[78]  S. P. Fodor,et al.  Multiplexed biochemical assays with biological chips , 1993, Nature.

[79]  J. Mekalanos Environmental signals controlling expression of virulence determinants in bacteria , 1992, Journal of bacteriology.

[80]  F. Neidhardt,et al.  Gene-protein index of Escherichia coli K-12. , 1983, Microbiological reviews.

[81]  L. Lillie Proceedings of the Nineteenth Annual Meeting of the American Association of Veterinary Laboratory Diagnosticians , 1977 .

[82]  M A Savageau,et al.  Generalized indicator plate for genetic, metabolic, and taxonomic studies with microorganisms , 1977, Applied and environmental microbiology.

[83]  B. Ames,et al.  Guanosine 5'-diphosphate 3'-diphosphate (ppGpp): positive effector for histidine operon transcription and general signal for amino-acid deficiency. , 1975, Proceedings of the National Academy of Sciences of the United States of America.

[84]  P. O’Farrell High resolution two-dimensional electrophoresis of proteins. , 1975, The Journal of biological chemistry.

[85]  L. E. D. D. D. Jong Bijdrage tot de kennis van het mineralisatieproces , 1926 .