Key Points
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This review discusses how bacterial populations have been historically defined and classified, and how these definitions have been refined with the development of molecular tools and whole-genome sequencing.
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We discuss the impact of horizontal gene transfer and how the increased awareness of this process is influencing our understanding of bacterial population structures.
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We focus on the recent development of DNA microarray technology and its use as a method for high-throughput genome-wide strain comparisons. We give details of the current achievements and limitations of this technique to assess the extent of genetic variability through a discussion of the current literature. We describe the application of this technology to characterize isolates of Helicobacter pylori, Streptococcus pneumoniae, and Salmonella enterica and S. bongori species.
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We propose how the information garnered from comparative genomic microarray analyses can provide important insight into the molecular basis of the relationships that exist between bacteria and their hosts.
Abstract
Sexual reproduction and recombination are essential for the survival of most eukaryotic populations. Until recently, the impact of these processes on the structure of bacterial populations has been largely overlooked. The advent of large-scale whole-genome sequencing and the concomitant development of molecular tools, such as microarray technology, facilitate the sensitive detection of recombination events in bacteria. These techniques are revealing that bacterial populations are comprised of isolates that show a surprisingly wide spectrum of genetic diversity at the DNA level. Our new awareness of this genetic diversity is increasing our understanding of population structures and of how these affect host–pathogen relationships.
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References
Van Belkum, A. et al. Role of genomic typing in taxonomy, evolutionary genetics, and microbial epidemiology. Clin. Microbiol. Rev. 14, 547–560 (2001).A thorough review that details current microbial nomenclature and concepts of evolutionary and population-based genetics. It reviews various molecular techniques and makes recommendations for their application in epidemiology, taxonomy and evolutionary studies.
Feil, E. J. & Spratt, B. G. Recombination and the population structures of baterial pathogens. Annu. Rev. Microbiol. 55, 561–590 (2001).This review addresses the impact of recombination on bacterial populations and gives specific focus to multilocus sequence typing.
Milkman, R. Electrophoretic variation in Escherichia coli from natural sources. Science 182, 1024–1026 (1973).
Selander, R. K. Population genetics of pathogenic bacteria. Microb. Pathog. 3, 1–7 (1987).
Beltran, P. Toward a population genetic analysis of Salmonella: genetic diversity and relationships among strains of serotypes S. choleraesuis, S. derby, S. dublin, S. enteritidis, S. heidelberg, S. infantis, S. newport, and S. typhimurium. Proc. Natl Acad. Sci. USA 85, 7753–7757 (1988).
Reeves, M. W. Clonal nature of Salmonella typhi and its genetic relatedness to other Salmonellae as shown by multilocus enzyme electrophoresis, and proposal of Salmonella bongori comb. nov. J. Clin. Microbiol. 27, 313–320 (1989).
Selander, R. K. Genetic population structure, clonal phylogeny, and pathogenicity of Salmonella paratyphi B. Infect. Immun. 58, 1891–1901 (1990).
Selander, R. K. Evolutionary genetic relationships of clones of Salmonella serovars that cause human typhoid and other enteric fevers. Infect. Immun. 58, 2262–2275 (1990).
Lefevre, J. C. DNA fingerprinting of Streptococcus pneumoniae strains by pulsed-field gel electrophoresis. J. Clin. Microbiol. 31, 2724–2728 (1993).
Li, J. et al. Recombinational basis of serovar diversity in Salmonella enterica. Proc. Natl Acad. Sci. USA 91, 2552–2556 (1994).
Spratt, B. G. Resistance to antibiotics mediated by target alterations. Science 264, 388–393 (1994).
Musser, J. M. Molecular population genetic analysis of emerged bacterial pathogens: selected insights. Emerg. Infect. Dis. 2, 1–17 (1996).
Schloter, M. et al. Ecology and evolution of bacterial microdiversity. FEMS Microbiol. Rev. 24, 647–660 (2000).
Maynard Smith, J., Feil, E. J. & Smith, N. H. Population structure and evolutionary dynamics of pathogenic bacteria. Bioessays 22, 1115–1122 (2000).An excellent review that discusses how MLEE, MLST and advances in nucleotide sequencing technology give a quantitative estimate of the impact of recombination in bacteria and how this contributes to our understanding of bacterial species definition.
Woese, C. R. Bacterial evolution. Microbiol. Rev. 51, 221–271 (1987).
Ludwig, W. Bacterial phylogeny based on 16S and 23S rRNA sequence analysis. FEMS Microbiol. Rev. 15, 155–173 (1994).
Maiden, M. C. et al. Multilocus sequence typing: a portable approach to the identification of clones within populations of pathogenic microorganisms. Proc. Natl Acad. Sci. USA 95, 3140–3145 (1998).This paper introduces multilocus sequence typing as a method for typing microorganisms on the basis of the nucleotide sequences of a limited number of genetic loci.
Feil, E. J. Estimating the relative contributions of mutation and recombination to clonal diversification: a comparison between Neisseria meningitidis and Streptococcus pneumoniae. Res. Microbiol. 151, 465–469 (2000).
Reid, S. D. et al. Parallel evolution of virulence in pathogenic Escherichia coli. Nature 406, 64–67 (2000).
Wren, B. W. Microbial genome analysis: insights into virulence, host adaptation and evolution. Nature Rev. Genet. 1, 30–39 (2000).
Dobrindt, U. & Hacker, J. Whole genome plasticity in pathogenic bacteria. Curr. Opin. Microbiol. 4, 550–557 (2001).
Fitzgerald, J. R. & Musser, J. M. Evolutionary genomics of pathogenic bacteria. Trends Microbiol. 9, 547–553 (2001).
Graham, M. R. Toward a genome-scale understanding of group A Streptococcus pathogenesis. Curr. Opin. Microbiol. 4, 65–70 (2001).
Musser, J. M. Pneumococcal research transformed. N. Engl. J. Med. 345, 1206–1207 (2001).
Schaechter, M. Escherichia coli and Salmonella 2000: the view from here. Microbiol. Mol. Biol. Rev. 65, 119–130 (2001).
Edwards, R. A., Olsen, G. J. & Maloy, S. R. Comparative genomics of closely related Salmonellae. Trends Microbiol. 10, 94–99 (2002).
Schena, M., Shalon, D., Davis, R. W. & Brown, P. O. Quantitative monitoring of gene expression patterns with a complementary DNA microarray. Science 270, 467–470 (1995).
Cummings, C. A. & Relman, D. A. Using DNA microarrays to study host–microbe interactions. Emerg. Infect. Dis. 6, 513–525 (2000).
Diehn, M. & Relman, D. A. Comparing functional genomic datasets: lessons from DNA microarray analyses of host–pathogen interactions. Curr. Opin. Microbiol. 4, 95–101 (2001).
Lucchini, S., Thompson, A. & Hinton, J. C. Microarrays for microbiologists. Microbiology 147, 1403–1414 (2001).
Sassetti, C. M., Boyd, D. H. & Rubin, E. J. Comprehensive identification of conditionally essential genes in mycobacteria. Proc. Natl Acad. Sci. USA 98, 12712–12717 (2001).
Schoolnik, G. K. The accelerating convergence of genomics and microbiology. Genome Biol. Online 2, REPORTS4009 (2001).
Behr, M. A. et al. Comparative genomics of BCG vaccines by whole-genome DNA microarray. Science 284, 1520–1523 (1999).
Salama, N. et al. A whole-genome microarray reveals genetic diversity among Helicobacter pylori strains. Proc. Natl Acad. Sci. USA 97, 14668–14673 (2000).This study provided the first evidence of the extent of genetic diversity in bacteria using microarray analysis.
Wu, L. et al. Development and evaluation of functional gene arrays for detection of selected genes in the environment. Appl. Environ. Microbiol. 67, 5780–5790 (2001).This crucial study describes conditions for examining gene composition in natural microbial communities using microarray analysis.
Cho, J. C. & Tiedje, J. M. Bacterial species determination from DNA–DNA hybridization by using genome fragments and DNA microarrays. Appl. Environ. Microbiol. 67, 3677–3682 (2001).A method based on random genome fragments and DNA microarray technology that reveals taxonomic relationships between bacterial strains.
Dorrell, N. et al. Whole genome comparison of Campylobacter jejuni human isolates using a low-cost microarray reveals extensive genetic diversity. Genome Res. 11, 1706–1715 (2001).
Bjorkholm, B. et al. Comparison of genetic divergence and fitness between two subclones of Helicobacter pylori. Infect. Immun. 69, 7832–7838 (2001).By using microarray analysis, the authors detected genetic changes between clinical isolates collected from a single patient, alluding to the potential for in vivo sub-species development.
Hurt, R. A. et al. Simultaneous recovery of RNA and DNA from soils and sediments. Appl. Environ. Microbiol. 67, 4495–4503 (2001).
Janssen, P. J., Audit, B. & Ouzounis, C. A. Strain-specific genes of Helicobacter pylori: distribution, function and dynamics. Nucleic Acids Res. 29, 4395–4404 (2001).
Israel, D. A. et al. Helicobacter pylori genetic diversity within the gastric niche of a single human host. Proc. Natl Acad. Sci. USA 98, 14625–14630 (2001).This study used microarrays to examine the extent and types of genetic change in a bacterial pathogen that occur during long-term host colonization and how these correlate with clinical outcomes of infection.
Israel, D. A. et al. Helicobacter pylori strain-specific differences in genetic content, identified by microarray, influence host inflammatory responses. J. Clin. Invest. 107, 611–620 (2001).Microarray technology was used to investigate H. pylori genetic diversity and to correlate this with disease development and severity.
Hakenbeck, R. et al. Mosaic genes and mosaic chromosomes: intra- and interspecies genomic variation of Streptococcus pneumoniae. Infect. Immun. 69, 2477–2486 (2001).These authors used an Affymetrix high-density oligonucleotide array to examine the genetic relatedness of 20 clinical S. pneumoniae isolates, 5 Streptococcus mitis isolates and 4 Streptococcus oralis isolates.
Tettelin, H. et al. Complete genome sequence of a virulent isolate of Streptococcus pneumoniae. Science 293, 498–506 (2001).
Fitzgerald, J. R. et al. Evolutionary genomics of Staphylococcus aureus: insights into the origin of methicillin-resistant strains and the toxic shock syndrome epidemic. Proc. Natl Acad. Sci. USA 98, 8821–8826 (2001).
Murray, A. E. et al. DNA/DNA hybridization to microarrays reveals gene-specific differences between closely related microbial genomes. Proc. Natl Acad. Sci. USA 98, 9853–9858 (2001).
Dziejman, M. et al. Comparative genomic analysis of Vibrio cholerae: genes that correlate with cholera endemic and pandemic disease. Proc. Natl Acad. Sci. USA 99, 1556–1561 (2002).
Smoot, J. C. et al. Genome sequence and comparative microarray analysis of serotype M18 groupA Streptococcus strains associated with acute rheumatic fever outbreaks. Proc. Natl Acad. Sci. USA 99, 4668–4673 (2002).
Wotherspoon, A. C. et al. Helicobacter pylori-associated gastritis and primary B-cell gastric lymphoma. Lancet 338, 1175–1176 (1991).
Montecucco, C. Living dangerously: how Helicobacter pylori survives in the human stomach. Nature Rev. Mol. Cell Biol. 2, 457–466 (2001).
Tummuru, M. K. et al. Cloning and expression of a high-molecular-mass major antigen of Helicobacter pylori: evidence of linkage to cytotoxin production. Infect. Immun. 61, 1799–1809 (1993).
Covacci, A. et al. Molecular characterization of the 128-kDa immunodominant antigen of Helicobacter pylori associated with cytotoxicity and duodenal ulcer. Proc. Natl Acad. Sci. USA 90, 5791–5795 (1993).
Censini, S. et al. cag, a pathogenicity island of Helicobacter pylori, encodes type I-specific and disease-associated virulence factors. Proc. Natl Acad. Sci. USA 93, 14648–14653 (1996).
Backert, S. et al. Translocation of the Helicobacter pylori CagA protein in gastric epithelial cells by a type IV secretion apparatus. Cell. Microbiol. 2, 155–164 (2000).
Odenbreit, S. et al. Translocation of Helicobacter pylori CagA into gastric epithelial cells by type IV secretion. Science 287, 1497–1500 (2000).
Segal, E. D. et al. Altered states: involvement of phosphorylated CagA in the induction of host cellular growth changes by Helicobacter pylori. Proc. Natl Acad. Sci. USA 96, 14559–14564 (1999).
Stein, M., Rappuoli, R. & Covacci, A. Tyrosine phosphorylation of the Helicobacter pylori CagA antigen after cag-driven host cell translocation. Proc. Natl Acad. Sci. USA 97, 1263–1268 (2000).
Akopyanz, N. et al. PCR-based RFLP analysis of DNA sequence diversity in the gastric pathogen Helicobacter pylori. Nucleic Acids Res. 20, 6221–6225 (1992).
Akopyanz, N. et al. DNA diversity among clinical isolates of Helicobacter pylori detected by PCR-based RAPD fingerprinting. Nucleic Acids Res. 20, 5137–5142 (1992).
Alm, R. A. et al. Genomic-sequence comparison of two unrelated isolates of the human gastric pathogen Helicobacter pylori. Nature 397, 176–180 (1999).
Alm, R. A. & Trust, T. J. Analysis of the genetic diversity of Helicobacter pylori: the tale of two genomes. J. Mol. Med. 77, 834–846 (1999).
Tomb, J. F. et al. The complete genome sequence of the gastric pathogen Helicobacter pylori. Nature 388, 539–547 (1997).
Pellegrini, M. et al. Assigning protein functions by comparative genome analysis: protein phylogenetic profiles. Proc. Natl Acad. Sci. USA 96, 4285–4288 (1999).
Gerhard, M. et al. Clinical relevance of the Helicobacter pylori gene for blood-group antigen-binding adhesin. Proc. Natl Acad. Sci. USA 96, 12778–12783 (1999).
Ilver, D. et al. Helicobacter pylori adhesin binding fucosylated histo-blood group antigens revealed by retagging. Science 279, 373–377 (1998).
Parsonnet, J. et al. Helicobacter pylori infection and the risk of gastric carcinoma. N. Engl. J. Med. 325, 1127–1131 (1991).
Sharma, S. A. et al. Interleukin-8 response of gastric epithelial cell lines to Helicobacter pylori stimulation in vitro. Infect. Immun. 63, 1681–1687 (1995).
Tummuru, M. K., Sharma, S. A. & Blaser, M. J. Helicobacter pylori picB, a homologue of the Bordetella pertussis toxin secretion protein, is required for induction of IL-8 in gastric epithelial cells. Mol. Microbiol. 18, 867–876 (1995).
Hoskins, J. et al. Genome of the bacterium Streptococcus pneumoniae strain R6. J. Bacteriol. 183, 5709–5717 (2001).
Hall, L. M. et al. Genetic relatedness within and between serotypes of Streptococcus pneumoniae from the United Kingdom: analysis of multilocus enzyme electrophoresis, pulsed-field gel electrophoresis, and antimicrobial resistance patterns. J. Clin. Microbiol. 34, 853–859 (1996).
Spratt, B. G. & Maiden, M. C. Bacterial population genetics, evolution and epidemiology. Phil. Trans. R. Soc. Lond. B 354, 701–710 (1999).
Gray, B. M. et al. Serotypes of Streptococcus pneumoniae causing disease. J. Infect. Dis. 140, 979–983 (1979).
Gray, B. M. et al. Clinical and epidemiologic studies of pneumococcal infection in children. Pediatr. Infect. Dis. 5, 201–207 (1986).
Orange, M. & Gray, B. M. Pneumococcal serotypes causing disease in children in Alabama. Pediatr. Infect. Dis. J. 12, 244–246 (1993).
Baumler, A. J. et al. Evolution of host adaptation in Salmonella enterica. Infect. Immun. 66, 4579–4587 (1998).
Conner, C. P. et al. Differential patterns of acquired virulence genes distinguish Salmonella strains. Proc. Natl Acad. Sci. USA 95, 4641–4645 (1998).
Folkesson, A. et al. Multiple insertions of fimbrial operons correlate with the evolution of Salmonella serovars responsible for human disease. Mol. Microbiol. 33, 612–622 (1999).
Townsend, S. M. et al. Salmonella enterica serovar Typhi possesses a unique repertoire of fimbrial gene sequences. Infect. Immun. 69, 2894–2901 (2001).
Baumler, A. J., Hargis, B. M. & Tsolis, R. M. Tracing the origins of Salmonella outbreaks. Science 287, 50–52 (2000).
Kingsley, R. A. & Baumler, A. J. Host adaptation and the emergence of infectious disease: the Salmonella paradigm. Mol. Microbiol. 36, 1006–1014 (2000).
Rabsch, W. et al. Competitive exclusion of Salmonella enteritidis by Salmonella gallinarum in poultry. Emerg. Infect. Dis. 6, 443–448 (2000).
Woolhouse, M. E., Taylor, L. H. & Haydon, D. T. Population biology of multihost pathogens. Science 292, 1109–1112 (2001).
McClelland, M. et al. Complete genome sequence of Salmonella enterica serovar Typhimurium LT2. Nature 413, 852–856 (2001).
Parkhill, J. et al. Complete genome sequence of a multiple drug resistant Salmonella enterica serovar Typhi CT18. Nature 413, 848–852 (2001).
Boyd, E. F. et al. Molecular genetic relationships of the Salmonellae. Appl. Environ. Microbiol. 62, 804–808 (1996).
Smith, B. P. et al. Aromatic-dependent Salmonella typhimurium as modified live vaccines for calves. Am. J. Vet. Res. 45, 59–66 (1984).
Boyd, E. F. et al. Salmonella reference collection B (SARB): strains of 37 serovars of subspecies I. J. Gen. Microbiol. 139, 1125–1132 (1993).
Figueroa-Bossi, N. et al. Variable assortment of prophages provides a transferable repertoire of pathogenic determinants in Salmonella. Mol. Microbiol. 39, 260–271 (2001).
Woodward, M. J., McLaren, I. & Wray, C. Distribution of virulence plasmids within Salmonellae. J. Gen. Microbiol. 135, 503–511 (1989).
Tinge, S. A. & Curtiss, R. Conservation of Salmonella typhimurium virulence plasmid maintenance regions among Salmonella serovars as a basis for plasmid curing. Infect. Immun. 58, 3084–3092 (1990).
Chiu, C. H. et al. Prevalence of the virulence plasmids of nontyphoid Salmonella in the serovars isolated from humans and their association with bacteremia. Microbiol. Immunol. 43, 899–903 (1999).
Ochman, H. & Groisman, E. A. Distribution of pathogenicity islands in Salmonella spp. Infect. Immun. 64, 5410–5412 (1996).
Xu, Q. et al. Identification of type II restriction and modification systems in Helicobacter pylori reveals their substantial diversity among strains. Proc. Natl Acad. Sci. USA 97, 9671–9676 (2000).
Aras, R. A. et al. Regulation of the HpyII restriction-modification system of Helicobacter pylori by gene deletion and horizontal reconstitution. Mol. Microbiol. 42, 369–382 (2001).
Davies, J. Origins and evolution of antibiotic resistance. Microbiologia 12, 9–16 (1996).
Brown, J. R. & Doolittle, W. F. Archaea and the prokaryote-to-eukaryote transition. Microbiol. Mol. Biol. Rev. 61, 456–502 (1997).
Doolittle, R. F. & Handy, J. Evolutionary anomalies among the aminoacyl-tRNA synthetases. Curr. Opin. Genet. Dev. 8, 630–636 (1998).
Doolittle, W. F. & Logsdon, J. M. Jr. Archaeal genomics: do Archaea have a mixed heritage? Curr. Biol. 8, R209–R211 (1998).
Doolittle, W. F. Phylogenetic classification and the universal tree. Science 284, 2124–2129 (1999).
Koonin, E. V. et al. Comparison of archaeal and bacterial genomes: computer analysis of protein sequences predicts novel functions and suggests a chimeric origin for the Archaea. Mol. Microbiol. 25, 619–637 (1997).
Lawrence, J. G. & Ochman, H. Molecular archaeology of the Escherichia coli genome. Proc. Natl Acad. Sci. USA 95, 9413–9417 (1998).
Nelson, K. E. et al. Evidence for lateral gene transfer between Archaea and bacteria from genome sequence of Thermotoga maritima. Nature 399, 323–329 (1999).
Ochman, H., Lawrence, J. G. & Groisman, E. A. Lateral gene transfer and the nature of bacterial innovation. Nature 405, 299–304 (2000).
Doolittle, W. F. Lateral genomics. Trends Cell Biol. 9, M5–M8 (1999).
McNulty, C. A. The discovery of Campylobacter-like organisms. Curr. Top. Microbiol. Immunol. 241, 1–9 (1999).
Marshall, B. J. & Warren, J. R. Unidentified curved bacilli in the stomach of patients with gastritis and peptic ulceration. Lancet 1, 1311–1315 (1984).
Suerbaum, S. Genetic variability within Helicobacter pylori. Ijmm Int. J. Med. Microbiol. 290, 175–181 (2000).
Kelly, D. Infectious ulcers: not hurry, worry and curry? Microbiol. Today 28, 188–189 (2001).
Musher, D. M. Infections caused by Streptococcus pneumoniae: clinical spectrum, pathogenesis, immunity, and treatment. Clin. Infect. Dis. 14, 801–807 (1992).
Hausdorff, W. P. et al. Which pneumococcal serogroups cause the most invasive disease: implications for conjugate vaccine formulation and use, part I. Clin. Infect. Dis. 30, 100–121 (2000).
McCarty, M. in Microbiology, Including Immunology and Molecular Genetics (eds Davis, B. D., Dulbecco, R., Eisen, H. N. & Ginsberg, H. S.) 607–622 (Harper & Row, Philadelphia, 1980).
Neufeld, F. Uber die agglutina der pneumokokken und uber die theorien der agglutination. Z. Hyg. Infekt-Kr 40, 54–72 (1902).
Kim, J. O. et al. Relationship between cell surface carbohydrates and intrastrain variation on opsonophagocytosis of Streptococcus pneumoniae. Infect. Immun. 67, 2327–2333 (1999).
White, P. B. Great Britain Medical Research Council Special Report: No. 103 (Her Majesty's Stationery Office, London, 1926).
Crosa, J. H. et al. Molecular relationships among the Salmonellae. J. Bacteriol. 115, 307–315 (1973).
Scherer, C. A. & Miller, S. I. in Principles of Bacterial Pathogenesis (ed. Groisman, E. A.) 266–316 (Academic, San Diego, 2001).
Anriany, Y. A. et al. Salmonella enterica serovar Typhimurium DT104 displays a rugose phenotype. Appl. Environ. Microbiol. 67, 4048–4056 (2001).
McGee, L. et al. Nomenclature of major antimicrobial-resistant clones of Streptococcus pneumoniae defined by the Pneumococcal Molecular Epidemiology Network. J. Clin. Microbiol. 39, 2565–2571 (2001).
Acknowledgements
We thank our colleagues G. Dougan and S. Baker from the Imperial College of Science, Technology and Medicine, London, for Salmonella strains and sharing data; A. Covacci, Chiron-Biocine, Italy; J. Gordon, Washington University, Missouri; J. Parsonette, Stanford University, California; R. Peek Jr, Vanderbilt University, Tennessee; J. Solnick, University of California at Davis, for providing H. pylori clinical isolates; L. McGee from the Pneumococcal Diseases Research Unit at the South African Institute for Medical Research, Johannesburg, for the S. pneumoniae strains; and A. Kawale and S. Censini for technical assistance, C. Kim for developing analytical tools for microarray analysis and thoughtful discussion, and S. Reid, J. R. Fitzgerald and members of the Falkow Laboratory for critical reviews of the manuscript.
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Glossary
- CONJUGATION
-
The transfer of DNA from a donor cell to a recipient cell that is mediated by direct cell–cell contact.
- TRANSFORMATION
-
The uptake of DNA by a bacterium from the surrounding environment.
- TRANSDUCTION
-
Virus- or phage-mediated introduction into a cell of a DNA fragment that is derived from a different cell.
- ARCHAEA
-
A kingdom of unicellular microorganisms, many members of which can survive extreme environmental conditions, such as temperatures >100 °C, extremely alkaline or acid environs, and highly osmotic conditions.
- RIBOTYPING
-
A technique used to determine genetic and evolutionary relationships between organisms. Oligonucleotide probes targeted to highly conserved domains of coding sequences of ribosomal RNA are amplified and the products are visualized by gel electrophoresis banding patterns are compared with known species and strains to determine organism relatedness.
- ATROPHIC GASTRITIS
-
Chronic inflammation of the stomach, accompanied by atrophy of the mucous membrane and destruction of the peptic glands.
- DUODENUM
-
The first portion of the small intestine, extending from the pylorus (the posterior end of the stomach) to the jejunum (the next portion of the small intestine).
- ADENOCARCINOMA
-
A form of malignant cancer that arises from the glandular epithelium.
- SEROVAR/SEROTYPE
-
A group of intimately related microorganisms distinguished by a common set of antigenic determinants that are expressed on the cell surface.
- CHEMOKINES
-
Small molecules that have a central role in inflammatory responses and trigger migration and activation of phagocytic cells and lymphocytes.
- CLUSTER ANALYSIS
-
A mathematical algorithm that organizes a set of items according to their similarity. For example, genes can be clustered according to their similarity in pattern of expression.
- INSERTION SEQUENCES
-
Small, mobile nucleotide sequences found in the genomes of many bacterial populations.
- ADHESIVE FIMBRIAE
-
Hair-like structures that project from the surface of some bacteria. They are involved in adhesion of bacterial cells to surfaces, and can be important in bacterial virulence.
- OTITIS MEDIA
-
Infection and inflammation of the middle ear space and ear drum.
- GRAM REACTION
-
A differential stain that separates bacteria into two groups, Gram positive and Gram negative, on the basis of the biochemical composition of their cell wall.
- DIPLOCOCCUS
-
Any of a variety of encapsulated bacteria (as the pneumococcus) that usually occur in pairs.
- CAPSULE
-
A thick gel-like material generally composed of hydrophilic polysaccharide that surrounds the cell wall of Gram-positive or Gram-negative bacteria. It can contribute to pathogenicity by inhibiting phagocytosis of the bacteria by the macrophages of the host.
- ENTEROBACTERIACEAE
-
A large family of Gram-negative bacilli that inhabit the large intestine of mammals.
- AGGLUTINATED
-
The aggregation of particulate antigen by antibodies.
- TISSUE TROPISM
-
Tissue-specific bacterial adherence and colonization due to a restricted distribution of receptor structures on certain host-cell surfaces and not on others.
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Joyce, E., Chan, K., Salama, N. et al. Redefining bacterial populations: a post-genomic reformation. Nat Rev Genet 3, 462–473 (2002). https://doi.org/10.1038/nrg820
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DOI: https://doi.org/10.1038/nrg820
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