Skip to main content
  • ASM
    • Antimicrobial Agents and Chemotherapy
    • Applied and Environmental Microbiology
    • Clinical Microbiology Reviews
    • Clinical and Vaccine Immunology
    • EcoSal Plus
    • Eukaryotic Cell
    • Infection and Immunity
    • Journal of Bacteriology
    • Journal of Clinical Microbiology
    • Journal of Microbiology & Biology Education
    • Journal of Virology
    • mBio
    • Microbiology and Molecular Biology Reviews
    • Microbiology Resource Announcements
    • Microbiology Spectrum
    • Molecular and Cellular Biology
    • mSphere
    • mSystems
  • Log in
  • My alerts
  • My Cart

Main menu

  • Home
  • Articles
    • Latest Articles
    • COVID-19 Special Collection
    • Archive
  • For Authors
    • Submit a Manuscript
    • Scope
    • Editorial Policy
    • Submission, Review, & Publication Processes
    • Organization and Format
    • Errata, Author Corrections
    • Illustrations and Tables
    • Nomenclature
    • Abbreviations and Conventions
    • Ethics Resources and Policies
  • About the Journal
    • About MMBR
    • Editor in Chief
    • Editorial Board
    • For Reviewers
    • For the Media
    • For Librarians
    • For Advertisers
    • Alerts
    • RSS
    • FAQ
  • Subscribe
    • Members
    • Institutions
  • ASM
    • Antimicrobial Agents and Chemotherapy
    • Applied and Environmental Microbiology
    • Clinical Microbiology Reviews
    • Clinical and Vaccine Immunology
    • EcoSal Plus
    • Eukaryotic Cell
    • Infection and Immunity
    • Journal of Bacteriology
    • Journal of Clinical Microbiology
    • Journal of Microbiology & Biology Education
    • Journal of Virology
    • mBio
    • Microbiology and Molecular Biology Reviews
    • Microbiology Resource Announcements
    • Microbiology Spectrum
    • Molecular and Cellular Biology
    • mSphere
    • mSystems

User menu

  • Log in
  • My alerts
  • My Cart

Search

  • Advanced search
Microbiology and Molecular Biology Reviews
publisher-logosite-logo

Advanced Search

  • Home
  • Articles
    • Latest Articles
    • COVID-19 Special Collection
    • Archive
  • For Authors
    • Submit a Manuscript
    • Scope
    • Editorial Policy
    • Submission, Review, & Publication Processes
    • Organization and Format
    • Errata, Author Corrections
    • Illustrations and Tables
    • Nomenclature
    • Abbreviations and Conventions
    • Ethics Resources and Policies
  • About the Journal
    • About MMBR
    • Editor in Chief
    • Editorial Board
    • For Reviewers
    • For the Media
    • For Librarians
    • For Advertisers
    • Alerts
    • RSS
    • FAQ
  • Subscribe
    • Members
    • Institutions
ARTICLE

Short-Sequence DNA Repeats in Prokaryotic Genomes

Alex van Belkum, Stewart Scherer, Loek van Alphen, Henri Verbrugh
Alex van Belkum
Department of Medical Microbiology & Infectious Diseases, Erasmus Medical Center Rotterdam, 3015 GD Rotterdam, and
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Stewart Scherer
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Loek van Alphen
Department of Medical Microbiology, Academic Medical Center, 1105 AZ Amsterdam, The Netherlands
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Henri Verbrugh
Department of Medical Microbiology & Infectious Diseases, Erasmus Medical Center Rotterdam, 3015 GD Rotterdam, and
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
DOI: 10.1128/MMBR.62.2.275-293.1998
  • Article
  • Figures & Data
  • Info & Metrics
  • PDF
Loading

Article Figures & Data

Figures

  • Tables
  • Fig. 1.
    • Open in new tab
    • Download powerpoint
    Fig. 1.

    Schematic survey of SSRs. (A) Examples of homogeneous simple sequence motifs consisting of repeat units varying from 1 (homopolymeric tract) to 6 nucleotides in length. (B) Example of a composite, heterogeneous repeat built from three 3-nucleotide units, two 5-nucleotide units, and seven 2-nucleotide motifs. (C) Comparative analysis of four different repeats built from three 10-nucleotide units showing degeneracy among units. Identity of the nucleotide sequences B through D with the consensus given in sequence A is indicated by dashes.

  • Fig. 2.
    • Open in new tab
    • Download powerpoint
    Fig. 2.

    Schematic representation of the mechanism of SSM during replication, which results in shortening or lengthening of SSRs. Individual repeat units are identified by arrows; bulging is the presence of non-base-pair base residues interrupting a regular 2-strand DNA helix. Bulging in the nascent strand leads to a larger number of repeat units; bulging in the template strand results in a smaller numbers of units. During replication, bulges can occur in both strands, and the effect of insertion or deletion can be neutralized by occurrence of the adverse event. The number of repeat units can decrease or increase by multiple repeats once multiple bulging in one strand has occurred.

  • Fig. 3.
    • Open in new tab
    • Download powerpoint
    Fig. 3.

    Molecular identification of SSR-type DNA. (A) Microdensitometer tracing of human leukocyte native DNA centrifuged to equilibrium in density gradients with an analytical ultracentrifuge. The satellite peaks representing repetitive DNA fractions displaying aberrant densities are indicated (I to III). (B) DNA fingerprints of human individuals generated by probing with repetitive DNA. DNA from five individuals (identified by numerals above the lanes) was digested with a restriction enzyme, the fragments were separated by electrophoresis, and after blotting, the resulting Southern blot was probed with a synthetic oligonucleotide SSR consisting of 10 units of a TTAGG motif. The autoradiograph shows that this SSR is widely dispersed throughout the human genome and clearly depicts the hypervariability in the observed banding patterns. (C) PCR amplification of SSR regions. A specific SSR was identified in the genome of H. influenzae, and primers bordering the repetitive motif were synthesized. When DNA from bacterial strains 1 to 10 was used as template, various amplicons were generated, most of them showing clear differences in length (related to the number of repeat units present). Lanes M contain 10-bp molecular size markers.

  • Fig. 4.
    • Open in new tab
    • Download powerpoint
    Fig. 4.

    Hypothetical model for the mechanism of fimbrial phase variation in H. influenzae. Transcription of the two divergently oriented genes hifA and hifB is controlled by a variable sequence of reiterated TA units (long open box) in their combined promoter region. In nine units in this SSR, the putative −10 and −35 promoter sequences for both hifA(hatched boxes) and hifB (short stippled boxes) are separated by 14 bases, which does not allow transcription of either gene. With 10 or 11 TA units, the −10 and −35 motifs are separated by 16 or 18 bases, respectively, allowing transcription of both genes, resulting in the expression of fimbriae. A spacing of 16 bases results in the highest level of fimbriation. With 12 TA units, hifAand hifB transcription can take place with alternative −35 promoter sequences (narrow boxes), which are separated by 16 bases from the corresponding −10 sequences. Solid boxes represent the +1 transcriptional start point. Reprinted from reference199 with permission of the publisher.

  • Fig. 5.
    • Open in new tab
    • Download powerpoint
    Fig. 5.

    Schematic models of MSCRAMMs from S. aureus. The MSCRAMMs shown are the ones with affinity for fibronectin (FnbpA and FnbpB), collagen (CNA), and fibrinogen (CLF, clumping factor). S, signal sequence; U or A, unique nonrepetitive sequence; δ, upstream repeat sequences; D, B, or R: repeated domains; W, cell wall-spanning domain; M, hydrophobic membrane-spanning domain; C, positively charged carboxy terminus. Reprinted from reference 139 with permission of the authors and the publisher.

  • Fig. 6.
    • Open in new tab
    • Download powerpoint
    Fig. 6.

    Epidemiology of H. influenzae infections. During an outbreak, strains 1 to 13 were isolated from different patients and compared to seven nonrelated clinical isolates (strains 14 to 20) on the basis of SSR polymorphisms. Four different SSRs were analyzed for the occurrence of length variability, and assays 3-1, 6-1, and 6-2 correctly identified the epidemic isolates as identical. The controls clearly differed in some instances. Interestingly, assay 5-2 also revealed major polymorphisms among the epidemic isolates, possibly identifying a “contingency locus” that is tailoring colonization or infection of a range of individual human hosts. Lanes M contain molecular size markers; the arrows on the right identify a 100-bp DNA fragment. Reprinted from reference 196 with permission of the American Society for Microbiology.

Tables

  • Figures
  • Table 1.

    Perfect small-unit SSRs in the S. cerevisiae genomea

    No. of unitsNo. of SSRs of unit length:
    12345678
    3—b———1710587
    4— ———203721
    5— 341—67901
    6— 14010451500
    7— 694901100
    8— 524320100
    9— 352600000
    10756352000000
    1148337500000
    1234515610000
    1324520400000
    141325300000
    15918200000
    16676100000
    17517100000
    18284000000
    19323000000
    20243100000
    • ↵a This table summarizes the occurrence of SSRs in the S. cerevisiae chromosomes. Numbers indicate the number of SSRs being present whereby the unit length defines the size of the repeat motif (1 to 8 nucleotides, horizontal scheme) and the unit number defines the number of repeat units present. No imperfections in the repeat unit were allowed for; repeat regions that are mentioned separately in the table were sometimes physically coupled (neighboring stretches of DNA). The maximum unit number was arbitrarily chosen to be 20. In the mononucleotide SSR class, the largest individual repeat contained 42 nucleotides. Incidentally, additional 2- and 3-nucleotide SSRs were encountered (results not shown).

    • ↵b —, not searched for because of expectations of an extremely large number; the minimum detectable number as used in the computer search program equals those targets not searched for.

  • Table 2.

    Occurrence of contiguous perfect small-unit SSRs in the genome of M. genitalium and M. pneumoniae

    Unit lengthRepeat positionaUnit sequenceNo. of unitsSequence homology
    M. genitalium
     386051–86066CTT5None
     3169475–169523TAG16None
     3224534–224555TAG7Attachment protein MgPa
     3227130–227163TAG11114-kDa MgPa
     3349735–349750TCT5None
     3351452–351482TAG10None
     3425824–425857TGT11Unidentified protein
     3429308–429335TAG9None
     3429967–423015CTT16None
     5212939–212954CAAAA3None
     6384465–384489TATTAC4None
    M. pneumoniae
     260190–60210AG/ACb5/5Unidentified protein
     265147–65169CT11None
     323651–23669TAG6Adhesin P1  
     634932–34950AACCCC3Adhesin P1
     6775707–775725AACCCC3Adhesin P1 precursor
    • ↵a Repeat positions are based on nucleotide sequence information described in reference55. Nucleotide repeats consisting of monomers [poly(A), poly(C), poly(G), or poly(T) tracts] were not searched for; 2-, 4-, 7-, and 8-unit repeats were not encountered. Repeats were identified by a computer program written by Stewart Scherer, University of California Los Angeles.

    • ↵b The two sequence motifs were found to be adjacent; both motifs occurred five times and were exactly neighboring.

  • Table 3.

    Survey of eubacterial SSR-containing genes with a known function

    SpeciesRepeat motifGeneLevel of regulationGene functionReference(s)
    TranscriptionTranslation/protein
    H. influenzaeCAATlic1–lic3−+LPS biosynthesisa83, 211, 212
    GCAAyadA−+Adhesin (Yersinia homolog)83
    GACAlgtC−+Glycosyltransferase83
    TTGGNDf−+Iron binding proteins83
    AGTCND−+Restriction modification, methyltransferase83
    TTTAND−+UnknownBacillus homolog83
    TAhifA/B+−Synthesis of fimbriae199, 200
    N. meningitidisGlsi2+−LPS biosynthesis18
    CTCTTopa−+Opacity surface proteins119
    Aopa+−Opacity surface proteins119
    GporA+−OMP198
    S. aureusb 93 bpfnb−+Fibronectin binding protein139
    561 bpcna−+Collagen adhesin140
     81 bpcoa−+Coagulase65, 165
    GAAGAXXXXAAXAAXCCTXGXAAAspa−+Protein A27
    GAXTCXGAXTCXGAXAGXclf−+Clumping factor, fibrinogen receptor116, 117
    Streptococcus spp.60 bppspA−+Pneumococcal surface proteinc219
    69 bpemm−+Phagocytosis resistance M protein6
    246 bpαC−+αC protein (antibody-mediated killing)67
    E. faecalisTAGTARRrep1 and rep2+−Iteron, regulates plasmid replication and transfer72
    M. hyorhinusd 36 and 39 bpvlp−+Variant membrane lipoprotein218
    Avlp+−Variant membrane lipoprotein218
    M. bovis24 bpvspA−+Membrane surface lipoprotein107
    M. fermentansAP78−+Lipoprotein in ABC transporter complex183
    U. urealyticumGGTAAAGAACAACCAGCAMB−+Serology-specific MB antigen222
    B. anthracisCAATATCAACAAvvrA−+Microfilarial sheath protein homolog87
    L. monocytogenes66 bpprfA−+Leucine-rich internalin like protein37
    E. coliA and Celac+−β-Galactosidase52, 156
    A. marginale 87 bpmsp1α−+Major surface protein2
    • ↵a Homologues for these sequences have been described for Moraxella catharralis and the human pathogenic Neisseria species.

    • ↵b The genes described for this species all produce MSCRAMMs.

    • ↵c Homologous structures were identified in diverse streptococci and Clostridium difficile.

    • ↵d See Table 2 for the analysis of M. genitalium and M. pneumoniae on the basis of the whole genome sequences as available.

    • ↵e Homopolymeric tracts.

    • ↵f ND, not defined.

PreviousNext
Back to top
Download PDF
Citation Tools
Short-Sequence DNA Repeats in Prokaryotic Genomes
Alex van Belkum, Stewart Scherer, Loek van Alphen, Henri Verbrugh
Microbiology and Molecular Biology Reviews Jun 1998, 62 (2) 275-293; DOI: 10.1128/MMBR.62.2.275-293.1998

Citation Manager Formats

  • BibTeX
  • Bookends
  • EasyBib
  • EndNote (tagged)
  • EndNote 8 (xml)
  • Medlars
  • Mendeley
  • Papers
  • RefWorks Tagged
  • Ref Manager
  • RIS
  • Zotero
Print

Alerts
Sign In to Email Alerts with your Email Address
Email

Thank you for sharing this Microbiology and Molecular Biology Reviews article.

NOTE: We request your email address only to inform the recipient that it was you who recommended this article, and that it is not junk mail. We do not retain these email addresses.

Enter multiple addresses on separate lines or separate them with commas.
Short-Sequence DNA Repeats in Prokaryotic Genomes
(Your Name) has forwarded a page to you from Microbiology and Molecular Biology Reviews
(Your Name) thought you would be interested in this article in Microbiology and Molecular Biology Reviews.
CAPTCHA
This question is for testing whether or not you are a human visitor and to prevent automated spam submissions.
Share
Short-Sequence DNA Repeats in Prokaryotic Genomes
Alex van Belkum, Stewart Scherer, Loek van Alphen, Henri Verbrugh
Microbiology and Molecular Biology Reviews Jun 1998, 62 (2) 275-293; DOI: 10.1128/MMBR.62.2.275-293.1998
del.icio.us logo Digg logo Reddit logo Twitter logo CiteULike logo Facebook logo Google logo Mendeley logo
  • Top
  • Article
    • SUMMARY
    • MOLECULAR ANALYSIS OF SSRS
    • WHOLE GENOME SEQUENCES AS A SOURCE OF SSRS
    • STRUCTURAL FEATURES OF SSRS
    • DISPERSED REPEATS IN PROKARYOTIC DNA
    • CONTIGUOUS REPEATS IN PROKARYOTIC DNA
    • SPECIFIC SSRS IN DNA FROM VARIOUS BACTERIAL SPECIES
    • SSRS IN PATHOGENIC PROTOZOA AND LOWER EUKARYOTES
    • SSRS AND MICROBIAL EVOLUTION
    • SSRS AND MICROBIAL PATHOGENESIS
    • SSRS IN MOLECULAR EPIDEMIOLOGY
    • CONCLUDING REMARKS AND PROSPECTS
    • ACKNOWLEDGMENTS
    • REFERENCES
  • Figures & Data
  • Info & Metrics
  • PDF

KEYWORDS

DNA, Bacterial
Repetitive Sequences, Nucleic Acid

Related Articles

Cited By...

About

  • About MMBR
  • Editor in Chief
  • Editorial Board
  • For Reviewers
  • For the Media
  • For Librarians
  • For Advertisers
  • Alerts
  • RSS
  • FAQ
  • Permissions
  • Journal Announcements

Authors

  • ASM Author Center
  • Submit a Manuscript
  • Ethics
  • Contact Us

Follow #MMBRJournal

@ASMicrobiology

       

ASM Journals

ASM journals are the most prominent publications in the field, delivering up-to-date and authoritative coverage of both basic and clinical microbiology.

About ASM | Contact Us | Press Room

 

ASM is a member of

Scientific Society Publisher Alliance

 

American Society for Microbiology
1752 N St. NW
Washington, DC 20036
Phone: (202) 737-3600

Copyright © 2021 American Society for Microbiology | Privacy Policy | Website feedback

Print ISSN: 1092-2172; Online ISSN: 1098-5557