Home LiteratureArticle Details
PMID: 17220307 Published · ppublish English Comparative Study Journal Article Research Support, N.I.H., Extramural

Native microbial colonization of Drosophila melanogaster and its use as a model of Enterococcus faecalis pathogenesis.

Infection and immunity ·Vol. 75 ·No. 4 ·2007-04-00 ·Pages 1565-76

Cox CR, Gilmore MS

Abstract

Enterococci are commensal organisms of the gastrointestinal (GI) tracts of a broad range of mammalian and insect hosts, but they are also leading causes of nosocomial infection. Little is known about the ecological role of enterococci in the GI tract consortia. To develop a tractable model for studying the roles of these organisms as commensals and pathogens, we characterized the Drosophila melanogaster microflora and examined the occurrence of enterococci in the gastrointestinal consortium of Drosophila. In a survey of laboratory-reared Drosophila and wild-captured flies, we found that Drosophila was naturally colonized by representatives of five bacterial phyla. Among these organisms were several species of enterococci, including Enterococcus faecalis, Enterococcus faecium, Enterococcus gallinaraum, and Enterococcus durans, as well as a previously detected but uncultured Enterococcus species. Drosophila could be cured of enterococcal carriage by antibiotic treatment and could be reassociated with laboratory strains. High-level colonization by a well-characterized strain expressing the enterococcal cytolysin was found to be detrimental to Drosophila compared to the effect of an isogenic, noncytolytic control. The anatomical distribution of enterococci in the Drosophila GI tract was determined by immunohistochemical staining of thin sections of naturally colonized and reassociated flies.

MeSH Terms
Animals Bacteria/classification,genetics,growth & development,isolation & purification Bacterial Proteins/biosynthesis Bacteriocins/biosynthesis Colony Count, Microbial Drosophila melanogaster/microbiology Enterococcus/growth & development,isolation & purification Enterococcus faecalis/growth & development,isolation & purification,metabolism,pathogenicity Gastrointestinal Tract/microbiology Immunohistochemistry Virulence Factors/biosynthesis
Chemicals
Bacterial Proteins Bacteriocins Virulence Factors cytolysin, Enterococcus faecalis
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Cox Christopher R
The Schepens Eye Research Institute, 20 Staniford Street, Boston, MA 02114, USA.
Gilmore Michael S
References (61)
61 references, click to expand
  1. Intra- and interspecific comparisons of bacterial diversity and community structure support coevolution of gut microbiota and termite host.
    Appl Environ Microbiol. 2005 Nov;71(11):6590-9 PMID: 16269686
  2. New antibiotic substances produced by beta hemolytic streptococci.
    J Infect Dis. 1949 Jan-Feb;84(1):88-91 PMID: 18109256
  3. The Termite Gut Microflora as an Oxygen Sink: Microelectrode Determination of Oxygen and pH Gradients in Guts of Lower and Higher Termites.
    Appl Environ Microbiol. 1995 Jul;61(7):2681-7 PMID: 16535076
  4. Biotyping, serotyping and phage typing of Streptococcus faecalis isolated from dental plaque in the human mouth.
    J Med Microbiol. 1987 Feb;23(1):45-54 PMID: 3102745
  5. Genetic analysis of the pAD1 pheromone response in Streptococcus faecalis, using transposon Tn917 as an insertional mutagen.
    J Bacteriol. 1984 Jun;158(3):777-83 PMID: 6327637
  6. Phylogenetic diversity of the intestinal bacterial community in the termite Reticulitermes speratus.
    Appl Environ Microbiol. 1996 Feb;62(2):461-8 PMID: 8593049
  7. A simple model host for identifying Gram-positive virulence factors.
    Proc Natl Acad Sci U S A. 2001 Sep 11;98(19):10892-7 PMID: 11535834
  8. Prevalence of local immune response against oral infection in a Drosophila/Pseudomonas infection model.
    PLoS Pathog. 2006 Jun;2(6):e56 PMID: 16789834
  9. Comparison of bacterial communities in the alkaline gut segment among various species of higher termites.
    Extremophiles. 2005 Jun;9(3):229-38 PMID: 15856134
  10. Dual cellulose-digesting system of the wood-feeding termite, Coptotermes formosanus Shiraki.
    Insect Biochem Mol Biol. 2002 Jul;32(7):777-84 PMID: 12044494
  11. Carriage of group D streptococci in the human bowel.
    J Clin Pathol. 1978 Dec;31(12):1182-6 PMID: 107199
  12. Enterococcus faecalis plasmid pAD1 replication and maintenance.
    Dev Biol Stand. 1995;85:89-98 PMID: 8586250
  13. Role of midgut electrogenic K+ pump potential difference in regulating lumen K+ and pH in larval lepidoptera.
    J Exp Biol. 1988 Nov;140:455-63 PMID: 2849625
  14. Driving forces and pathways for H+ and K+ transport in insect midgut goblet cells.
    J Exp Biol. 1992 Nov;172:403-15 PMID: 1337097
  15. Calcium and potassium content of secretions from noncancerous and cancerous stomachs.
    Cancer Res. 1946 Feb;6:54-6 PMID: 21010871
  16. Genes that fight infection: what the Drosophila genome says about animal immunity.
    Trends Genet. 2000 Oct;16(10):442-9 PMID: 11050330
  17. Enterococcus faecalis cytolysin without effect on the intestinal growth of susceptible enterococci in mice.
    J Infect Dis. 1995 Jul;172(1):273-6 PMID: 7797930
  18. Introducing DOTUR, a computer program for defining operational taxonomic units and estimating species richness.
    Appl Environ Microbiol. 2005 Mar;71(3):1501-6 PMID: 15746353
  19. Signaling mechanisms in the antimicrobial host defense of Drosophila.
    Curr Opin Microbiol. 2000 Feb;3(1):16-22 PMID: 10679426
  20. Census of the bacterial community of the gypsy moth larval midgut by using culturing and culture-independent methods.
    Appl Environ Microbiol. 2004 Jan;70(1):293-300 PMID: 14711655
  21. A Study of the Bacteria Associated with Thirty Species of Insects.
    J Bacteriol. 1941 Dec;42(6):757-90 PMID: 16560484
  22. Drosophila melanogaster as a model host for Staphylococcus aureus infection.
    Microbiology. 2004 Jul;150(Pt 7):2347-55 PMID: 15256576
  23. Molecular analysis of jejunal, ileal, caecal and recto-sigmoidal human colonic microbiota using 16S rRNA gene libraries and terminal restriction fragment length polymorphism.
    J Med Microbiol. 2005 Nov;54(Pt 11):1093-101 PMID: 16192442
  24. The Ribosomal Database Project (RDP-II): previewing a new autoaligner that allows regular updates and the new prokaryotic taxonomy.
    Nucleic Acids Res. 2003 Jan 1;31(1):442-3 PMID: 12520046
  25. Direct analysis of genes encoding 16S rRNA from complex communities reveals many novel molecular species within the human gut.
    Appl Environ Microbiol. 1999 Nov;65(11):4799-807 PMID: 10543789
  26. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools.
    Nucleic Acids Res. 1997 Dec 15;25(24):4876-82 PMID: 9396791
  27. Microbiology. The thin line between gut commensal and pathogen.
    Science. 2003 Mar 28;299(5615):1999-2002 PMID: 12663906
  28. Tissue-specific inducible expression of antimicrobial peptide genes in Drosophila surface epithelia.
    Immunity. 2000 Nov;13(5):737-48 PMID: 11114385
  29. Identification of plant-associated enterococci.
    J Appl Microbiol. 2001 Aug;91(2):268-78 PMID: 11473591
  30. Heritable endosymbionts of Drosophila.
    Genetics. 2006 Sep;174(1):363-76 PMID: 16783009
  31. Mapping of Streptococcus faecalis plasmids pAD1 and pAD2 and studies relating to transposition of Tn917.
    J Bacteriol. 1982 Dec;152(3):1220-30 PMID: 6292164
  32. Quantification of bacterial groups within human fecal flora by oligonucleotide probe hybridization.
    Appl Environ Microbiol. 2000 May;66(5):2263-6 PMID: 10788414
  33. Induction and regulation of antimicrobial peptides in Drosophila.
    Dev Comp Immunol. 1999 Jun-Jul;23(4-5):345-58 PMID: 10426427
  34. Profiling of bacterial flora in gastric biopsies from patients with Helicobacter pylori-associated gastritis and histologically normal control individuals by temperature gradient gel electrophoresis and 16S rDNA sequence analysis.
    J Med Microbiol. 2000 Sep;49(9):817-22 PMID: 10966230
  35. Drosophila as a model host for Pseudomonas aeruginosa infection.
    J Bacteriol. 2001 Feb;183(4):1466-71 PMID: 11157963
  36. The evolution and genetics of innate immunity.
    Nat Rev Genet. 2001 Apr;2(4):256-67 PMID: 11283698
  37. Molecular analysis of the bacterial microbiota in the human stomach.
    Proc Natl Acad Sci U S A. 2006 Jan 17;103(3):732-7 PMID: 16407106
  38. Widespread prevalence of wolbachia in laboratory stocks and the implications for Drosophila research.
    Genetics. 2005 Aug;170(4):1667-75 PMID: 15937134
  39. Identification and characterization of an Enterococcus faecalis plasmid pAD1-encoded stability determinant which produces two small RNA molecules necessary for its function.
    Plasmid. 1994 Sep;32(2):168-81 PMID: 7531349
  40. Enterococci in insects.
    Appl Microbiol. 1972 Oct;24(4):575-80 PMID: 4628796
  41. Diversity of the human intestinal microbial flora.
    Science. 2005 Jun 10;308(5728):1635-8 PMID: 15831718
  42. Multiple-drug resistant enterococci: the nature of the problem and an agenda for the future.
    Emerg Infect Dis. 1998 Apr-Jun;4(2):239-49 PMID: 9621194
  43. Drosophila host defense: differential induction of antimicrobial peptide genes after infection by various classes of microorganisms.
    Proc Natl Acad Sci U S A. 1997 Dec 23;94(26):14614-9 PMID: 9405661
  44. MODELTEST: testing the model of DNA substitution.
    Bioinformatics. 1998;14(9):817-8 PMID: 9918953
  45. Enterococcus faecalis antigens in human infections.
    Infect Immun. 1997 Oct;65(10):4207-15 PMID: 9317028
  46. Introducing SONS, a tool for operational taxonomic unit-based comparisons of microbial community memberships and structures.
    Appl Environ Microbiol. 2006 Oct;72(10):6773-9 PMID: 17021230
  47. Genetic analysis of the pAD1 hemolysin/bacteriocin determinant in Enterococcus faecalis: Tn917 insertional mutagenesis and cloning.
    J Bacteriol. 1990 Jan;172(1):155-63 PMID: 2152897
  48. Bellerophon: a program to detect chimeric sequences in multiple sequence alignments.
    Bioinformatics. 2004 Sep 22;20(14):2317-9 PMID: 15073015
  49. Nutrition of the Enterococci.
    J Bacteriol. 1944 Apr;47(4):335-42 PMID: 16560783
  50. Transfer of pheromone-inducible plasmids between Enterococcus faecalis in the Syrian hamster gastrointestinal tract.
    J Infect Dis. 1992 Nov;166(5):1188-91 PMID: 1402034
  51. The genome sequence of Drosophila melanogaster.
    Science. 2000 Mar 24;287(5461):2185-95 PMID: 10731132
  52. In situ morphology of the gut microbiota of wood-eating termites [Reticulitermes flavipes (Kollar) and Coptotermes formosanus Shiraki].
    Appl Environ Microbiol. 1977 Feb;33(2):406-26 PMID: 848959
  53. Drosophila melanogaster is a genetically tractable model host for Mycobacterium marinum.
    Infect Immun. 2003 Jun;71(6):3540-50 PMID: 12761139
  54. Immunologic Adsorbents: I. Isolation of Antibody by Means of a Cellulose-Protein Antigen.
    Proc Natl Acad Sci U S A. 1951 Sep;37(9):575-8 PMID: 16589016
  55. Pseudomonas aeruginosa relA contributes to virulence in Drosophila melanogaster.
    Infect Immun. 2004 Oct;72(10):5638-45 PMID: 15385461
  56. Aerobic and facultatively anaerobic cellulolytic bacteria from the gut of the termite Zootermopsis angusticollis.
    J Appl Microbiol. 2002;92(1):32-40 PMID: 11849325
  57. Different levels of genetic homogeneity in vancomycin-resistant and -susceptible Enterococcus faecium isolates from different human and animal sources analyzed by amplified-fragment length polymorphism.
    Antimicrob Agents Chemother. 2002 Sep;46(9):2779-83 PMID: 12183228
  58. Occurrence of enterococci in animals in a wild environment.
    Appl Microbiol. 1963 Mar;11:136-40 PMID: 13936610
  59. Direct demonstration of instabilities in oxygen concentrations within the extravascular compartment of an experimental tumor.
    Cancer Res. 2006 Feb 15;66(4):2219-23 PMID: 16489024
  60. Estimating population size for capture-recapture data when capture probabilities vary by time and individual animal.
    Biometrics. 1992 Mar;48(1):201-16 PMID: 1581485
  61. Drosophila host defense after oral infection by an entomopathogenic Pseudomonas species.
    Proc Natl Acad Sci U S A. 2005 Aug 9;102(32):11414-9 PMID: 16061818
Article Info
Journal
Infection and immunity
Abbr.
Infect Immun
ISSN
0019-9567
Published
2007-04-00
Epub
2007-00-12
Pages
1565-76
Language
English
Region
United States
NLM ID
0246127
PMCID
PMC1865669
Subset
IM
Grants
NCRR NIH HHS · 1RR 020596-01A1 · United States
NIAID NIH HHS · R21 AI054614 · United States
NIAID NIH HHS · AI 41108 · United States
NIAID NIH HHS · R01 AI041108 · United States
NIAID NIH HHS · AI 054614 · United States
NCRR NIH HHS · R21 RR020596 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com