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Analysis of the intestinal microflora: a renaissance

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Abstract

The ability of microbial ecologists to analyse the composition of complex bacterial communities has been greatly enhanced by the application of molecular methodologies. The use of these techniques should enable an accurate record of the identity and population dynamics of the inhabitants of the intestinal tract to be obtained, and should promote an improved comprehension of the relationship between the microflora and the human host. This, in turn, will lead to a new concept of the intestinal microflora of humans.

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References

  • Amann RI, Ludwig W & Schleifer K-H (1995) Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol. Rev. 59: 143-169

    Google Scholar 

  • Aranki A & Freter R (1972) Use of anaerobic glove boxes for the cultivation of strictly anaerobic bacteria. Am. J. Clin. Nutr. 25: 1329-1334

    Google Scholar 

  • Ballongue J (1993) Bifidobacteria and probiotic action. In: Salminen S & von Wright A (Eds) Lactic Acid Bacteria (pp 357-428). Marcel Dekker, New York

    Google Scholar 

  • Barrow PA, Brooker BE, Fuller R & Newport MJ (1980) The attachment of bacteria to the gastric epithelium of the pig and its importance in the microecology of the intestine. J. Appl. Bacteriol. 48: 147-154

    Google Scholar 

  • Bassam BJ, Allen T, Flood S, Stevens J, Wyatt P & Livak KJ (1996) Nucleic acid sequence detection systems: revolutionary automation for monitoring and reporting PCR products. Australasian Biotechnol. 6: 285-294

    Google Scholar 

  • Bateup JM, Dobbinson S, McConnell MA, Munro K & Tannock GW (1998) Molecular analysis of the composition of Lactobacillus populations inhabiting the stomach and caecum of pigs. Microbial Ecology in Health and Disease 10: 95-102

    Google Scholar 

  • Berg RD (1983) Host immune response to antigens of the indigenous intestinal flora. In: Hentges DJ (Ed) Human Intestinal Micro flora in Health and Disease (pp 101-126). Academic Press, New York

    Google Scholar 

  • Biavati B, Castagnoli P, Crociani F & Trovatelli LD (1984) Species of the genus Bifidobacterium in the feces of infants. Microbiologica 7: 341-345

    Google Scholar 

  • Biavati B, Castagnoli P & Trovatelli LD (1986) Species of the genus Bifidobacterium in the feces of adults. Microbiologica 9: 39-45

    Google Scholar 

  • Bry L, Falk PG, Midtvedt T & Gordon JI (1996) A model of host-microbial interactions in an open mammalian ecosystem. Science 273: 1380-1383

    Google Scholar 

  • Caufield PW (1997) Dental caries — a transmissible and infectious disease revisited: a position paper. Pediatric Dentitstry 19: 491-498

    Google Scholar 

  • Chadwick VS & Chen W (1999) The intestinal microflora and inflammatory bowel disease. In: Tannock GW (Ed) Medical Importance of the Normal Microflora (pp 177-221). Kluwer Academic Publishers, Dordrecht, The Netherlands

    Google Scholar 

  • Croucher SC, Houston AP, Bayliss CE & Turner RJ (1983) Bacterial populations associated with different regions of the human colon wall. Appl. Environ. Microbiol. 45: 1025-1033

    Google Scholar 

  • Cummings JH & Macfarlane GT (1991) The control and consequences of bacterial fermentation in the human colon. J. Appl. Bacteriol. 70: 443-459

    Google Scholar 

  • Drasar BS & Barrow PA (1985) Intestinal Microbiology. American Society for Microbiology, Washington DC

    Google Scholar 

  • Drasar BS & Hill MJ (1974) Human Intestinal Flora. Academic Press, London

    Google Scholar 

  • Dubos R, Schaedler RW, Costello R & Hoet P (1965) Indigenous, normal, and autochthonous flora of the gastrointestinal tract. J. Exper. Med. 122: 67-76

    Google Scholar 

  • Felske A, Rheims H, Wolterink A, Stackebrandt E & Akkermans ADL (1997) Ribosome analysis reveals prominent activity of an uncultured member of the class of Actinobacteria in grassland soils. Microbiology 143: 2983-2989

    Google Scholar 

  • Ferguson WK (1967) The Renaissance. Holt, Rinehart and Winston, New York

    Google Scholar 

  • Finegold SM (1977) Anaerobic Bacteria in Human Disease. Academic Press, New York

    Google Scholar 

  • Finegold SM, Attebury R & Sutter VL (1974) Effect of diet on human fecal flora: comparison of Japanese and American diets. Am. J. Clin. Nutr. 27: 1456-1469

    Google Scholar 

  • Finegold SM, Sutter VL & Mathisen GE (1983) Normal indigenous intestinal flora. In: Hentges DJ (Ed) Human Intestinal Microflora in Health and Disease (pp 3-31). Academic Press, New York

    Google Scholar 

  • Finegold SM & Sutter VL (1978) Fecal flora in different populations, with special reference lo diet. Am. J. Clin. Nutr. 31: S116-S122

    Google Scholar 

  • Franks AH, Harmsen HJM, Raangs GC, Jansen GJ, Schut F & Welling GW (1998) Variations of bacterial populations in human feces measured by fluorescent in situ hybridization with group-specific 16S rRNA-targeted oligonucleotide probes. Appl. Environ. Microbiol. 64: 3336-3345

    Google Scholar 

  • Fuller R (1989) Probiotics in man and animals. J. Appl. Bacteriol. 66: 365-378

    Google Scholar 

  • Fuller R (1999) Probiotics for farm animals. In: Tannock GW (Ed) Probiotics: a Critical Review (pp 15-22). Horizon Scientific Press, Wymondham, UK

    Google Scholar 

  • Fuller R & Brooker BE (1974) Lactobacilli which attach lo the crop epithelium of the fowl. Am. J. Clin. Nutr. 27: 1305-1312

    Google Scholar 

  • Gastone JSH (1997) Pathogenic role of gut inflammation in the spondyloarthropathies. Current Opinion in Rheumatology 9: 302-307

    Google Scholar 

  • Goldin BR, Gorbach SL, Saxelin M, Barakat S, Gualtieri L & Salminen S (1992) Survival of Lactobacillus species (strain GG) in human gastroinlestinal tract. Digestive Diseases and Sciences 37: 121-128

    Google Scholar 

  • Goldin BR, Swenson L, Dwyer J, Sexton M & Gorabch SL1 (980) Effect of diet and Lactobacillus acidophilus supplements on human fecal bacterial enzymes. J. National Cancer Institute 64: 255-261

    Google Scholar 

  • Goodwin MA, Cooper GL, Brown J, Bickford AA, Waltman WD & Dickson TG (1991) Clinical, pathological, and epizootiological features of the long-segmented filamentous organisms (Bacteria, LSFOs) in the small intestines of chickens, turkeys, and quails. Avian Diseases 35: 872-876

    Google Scholar 

  • Gordon HA & Pesti L (1971) The gnotobiotic animal as a tool in the study of host-microbial relationships. Bacteriol. Rev. 35: 390-429

    Google Scholar 

  • Gracey M (1983) The contaminated small bowel syndrome. In: Hentges DJ (Ed) Human Intestinal Microflora in Health and Disease (pp 495-513). Academic Press, New York

    Google Scholar 

  • Gurtler V & Stanisich VA (1996) New approaches lo typing and identification of bacteria using the 16S-23S rDNA spacer region. Microbiology 142: 3-16

    Google Scholar 

  • Hill JE, Kelley LC & Langheinrich KA (1992) Visceral granulomas in chickens infected with a filamentous bacteria. Avian Diseases 36: 172-176

    Google Scholar 

  • Holdeman LV & Moore WEC (1972) Roll-lube technique for anaerobic bacteria. Am. J. Clin. Nutr. 25: 1314-1317

    Google Scholar 

  • Hungate RE (1966) The Rumen and its Microbes. Academic Press, New York

    Google Scholar 

  • Husni RN, Gordon SM, Washington JA & Longworth DL (1997) Lactobacillus bacteremia and endocarditis: review of 45 cases. Clinical Infectious Diseases 25: 1048-1055

    Google Scholar 

  • Jepson MA, Clark MA, Simmons NL & Hirst BH (1993) Actin accumulations at sites of attachment of indigenous apathogenic segmented filamentous bacteria to mouse ileal epithelial cells. Infection and Immunity 61: 4001-4004

    Google Scholar 

  • Kato I, Kobayashi S, Yokokura T & Mutai M (1981) Antitumor activity of Lactobacillus casei in mice. Gann 72: 517-523

    Google Scholar 

  • Kimura K, McCartney AL, McConnell MA & Tannock GW (1997) Analysis of fecal populations of bifidobacteria and lactobacilli and investigations of the immunological responses of their human hosts to the predominant strains. Appl. Environ. Microbiol. 63: 3394-3398

    Google Scholar 

  • Klaasen HLBM, Koopman JP, van den Brink ME, van Wezel HPN & Beynen AC (1991) Mono-association of mice with non-cultivable, intestinal, segemented, filamentous bacteria. Archives of Microbiology 156: 148-151

    Google Scholar 

  • Klaasen HLBM, Koopman JP, Poelma FGJ & Beynen AC (1992) Intestinal, segmented, filamentous bacteria. FEMS Microbiol. Rev. 88: 165-180

    Google Scholar 

  • Klaasen HLBM, van der Heijden PJ, Stok W, Poelma FGJ, Koopman JP, van den Brink ME, Bakker MH, Eling WMC & Beynen AC (1993) Apathogenic, intestinal, segmented, filamentous bacteria stimulate the mucosal immune system of mice. Infection and Immunity 61: 303-306

    Google Scholar 

  • Kolenbrander PE (1991) Coaggregation: adherence in the human oral microbial ecosystem. In: Dworkin M (Ed) Microbial Cell-Cell Interactions (pp 303-329). American Society for Microbiology, Washington DC

    Google Scholar 

  • Lehman TJ, Cremer MA, Walker SM & Dillon AM (1987) The role of humoral immunity in Lactobacillus casei cell wall induced arthritis. J. Rheumatology 14: 415-419

    Google Scholar 

  • Luckey TD (1963) Germfree Life and Gnotobiology. Academic Press, New York

    Google Scholar 

  • Macfarlane GT & Macfarlane S (1995) Human intestinal'biofilm' communities. In: Wimpenny J, Handley P, Gilbert P & Lappin-Scott H (Eds) The Life and Death of Biofilm (pp 83-87). BioLine, Cardiff

    Google Scholar 

  • McCartney AL, Wang W & Tannock GW (1996) Molecular analysis of the composition of the bifidobacterial and lactobacillus micro flora of humans. Appl. Environ. Microbiol. 62: 4608-4613

    Google Scholar 

  • Mitsuoka T (1992) The human gastrointestinal tract. In: Wood BJB (Ed) The Lactic Acid Bacteria, Volume 1, The Lactic Acid Bacteria in Health and Disease (pp 69-114). Elsevier Applied Science, London

    Google Scholar 

  • Moore WEC, Cato EP & Holdeman LV (1978) Some current concepts in intestinal bacteriology. Am. J. Clin. Nutr. 31: S33-S42

    Google Scholar 

  • Moore WEC & Holdeman LV (1974) Special problems associated with the isolation and identification of intestinal bacteria in fecal flora studies. Am. J. Clin. Nutr. 27: 1450-1455

    Google Scholar 

  • Muyzer G & Smalla K (1998) Application of denaturing gradient gel electrophoresis (DGGE) and temperature gradient gel electrophoresis (TGGE) in microbial ecology. Antonie van Leewenhoek 73: 127-141

    Google Scholar 

  • O'Sullivan DJ (1999) Methods of analysis of the intestinal microflora. In: Tannock GW (Ed) Probiotics: a Critical Review (pp 23-44). Horizon Scientific Press, Wymondham, UK

    Google Scholar 

  • Pasteur L (1885) Observations relatives a la note precedente de M. Duclaux. Academies des Sciences, Comptes Rendues (Paris) 100: 68

    Google Scholar 

  • Perdigon G & Alvarez S (1992) Probiotics and the immune state. In: Fuller R (Ed) Probiotics. The Scientific Basis (pp 146-180). Chapman and Hall, London

    Google Scholar 

  • Raskin L, Capman WC, Sharp R, Poulsen LK & Stahl DA (1997) Molecular ecology of gastrointestinal ecosystems. In: Mackie RI, White BA & Isaacson RE (Eds) Gastrointestinal Microbiology, Volume 2, Gastrointestinal Microbes and Host Interactions (pp 243-298). Chapman and Hall, New York

    Google Scholar 

  • Reilly K & Attwood GT (1998) Detection of Clostridium proteoclasticum and closely related strains in the rumen by competitive PCR. Appl. Environ. Microbiol. 64: 907-913

    Google Scholar 

  • Rettger LF, Levy MN, Weinstein L & Weiss JE (1935) Lactobacillus acidophilus and its Therapeutic Application. Yale University Press, New Haven, USA

    Google Scholar 

  • Reysenbach A-L, Giver LJ, Wickham GS & Pace NR (1992) Differential amplification of rRNA genes by polymerase chain reaction. Appl. Environ. Microbiol. 58: 3417-3418

    Google Scholar 

  • Roberton AM & Corfield AP (1999) Mucin degradation and its significance in inflammatory conditions of the gastrointestinal tract. In: Tannock GW (Ed) Medical Importance of the Normal Microflora (pp 222-261). Kluwer Academic Publishers, Dordrecht, The Netherlands

    Google Scholar 

  • Salyers AA & Whitt DD (1994) Bacterial Pathogenesis. American Society for Microbiology, Washington DC

    Google Scholar 

  • Savage DC (1977) Microbial ecology of the gastrointestinal tract. Annual Reviews of Microbiology 31: 107-133

    Google Scholar 

  • Savage DC (1983) Morphological diversity among members of the gastrointestinal microflora. International Review of Cytology 82: 305-334

    Google Scholar 

  • Savage DC, Dubos R & Schaedler RW (1968) The gastrointestinal epithelium and its autochthonous bacterial flora. J. Exper. Med. 127: 67-76

    Google Scholar 

  • Schiffrin EJ, Rochat F, Link-Amster H, Aeschlimann JM & Donnet-Hughes A (1995) Immunomodulation of human blood cells following the ingestion of lactic acid bacteria. J. Dairy Sci. 78: 491-497

    Google Scholar 

  • Severijnen AJ, van Kleef R, Hazenberg MP & van de Merwe J (1989) Cell wall fragments from major residents of the human intestinal flora induce chronic arthritis in rats. J. Rheumatology 16: 1061-1068

    Google Scholar 

  • Snel J (1997) Symbiosis between the Mouse and Segmented Filamentous Bacteria: a Gnotobiotic Study. PhD thesis, University of Nijmegen

  • Stackebrandt E & and Rainey FA (1995) Partial and complete 16S rDNA sequences, their use in generation of 16S phylogenetic trees and their implications in molecular ecological studies. In: Akkermans DL, van Elsas JD & de Bruijn FJ (Eds) Molecular Microbial Ecology Manual (pp 1-17). Kluwer Academic Publishers, Dordrecht, The Netherlands

    Google Scholar 

  • Summanen P, Baron EJ, Citron DM, Strong C, Wexler HM & Finegold SM (1993) Wadsworth Anaerobic Bacteriology Manual. Star Publishing Company, Belmont, USA

    Google Scholar 

  • Swaminathan B & Matar GM (1993) Molecular typing methods. In: Persing DH, Smith TF, Tenover FC & White TJ (Eds) Diagnostic Molecular Microbiology. Principles and Applications (pp 26-50). American Society for Microbiology, Washington DC

    Google Scholar 

  • Szentkuti L, Riedesel H, Enss M-L, Gaertner K & von Engelhardt W (1990) Pre-epithelial mucus layer in the colon of conventional and germfree rats. Histochemistry J. 22: 491-497

    Google Scholar 

  • Tagg JR, Pybus V, Phillips LV & Fiddes TM (1983) Application of inhibitor typing in a study of the transmission and retention in the human mouth of the bacterium Streptococcus salivarius. Archives of Oral Biology 28: 911-915

    Google Scholar 

  • Tannock GW (1987) Demonstration of mucosa-associated microbial populations in the colons of mice. Appl. Environ. Microbiol. 53: 1964-1968

    Google Scholar 

  • Tannock GW (1995a) Normal microflora. An introduction to microbes inhabiting the human body. Chapman and Hall, London

    Google Scholar 

  • Tannock GW (1995b) Microecology of the gastrointestinal tract in relation to lactic acid bacteria. International Dairy J. 5: 1059-1070

    Google Scholar 

  • Tannock GW (1997) Influences of the normal microbiota on the animal host. In: Mackie RI, White BA & Isaacson RE (Eds) Gastrointestinal Microbiology, Volume 2, Gastrointestinal Microbes and Host Interactions (pp 466-497). Chapman and Hall, New York

    Google Scholar 

  • Tannock GW (Ed) (1999) Medical Importance of the Normal Microflora. Kluwer Academic Publishers, Dordrecht, The Netherlands

    Google Scholar 

  • Tannock GW (Ed) (1999) Probiotics: a Critical Review. Horizon Scientific Press, Wymondham, UK

    Google Scholar 

  • Tannock GW, Crichton C, Welling GW, Koopman JP & Midtvedt T (1988) Reconstitution of the gastrointestinal microflora of lactobacillus-free mice. Appl. Environ. Microbiol. 54: 2971-2975

    Google Scholar 

  • Tannock GW, Fuller R, Smith SL & Hall MA (1990) Plasmid profiling of members of the family Enterobacteriaceae, lactobacilli, and bifidobacteria to study the transmission of bacteria from mother to infant. J. Clin. Microbiol. 28: 1225-1228

    Google Scholar 

  • Welling GW, Elfferich P, Raangs GC, Wildeboer-Veloo ACM, Jansen GJ & Degener JE (1997) 16S ribosomal RNA-targeted oligonucleotide probes for monitoring of intestinal tract bacteria. Scandanavian J. Gastroenterology 32 Supplement 222: 17-19

    Google Scholar 

  • Wilson KH & Blitchington RB (1996) Human colonic biota studied by ribosomal DNA sequence analysis. Appl. Environ. Microbiol. 62: 2273-2278

    Google Scholar 

  • Zoetendal E, Akkermans AD & De Vos WM (1998) Temperature gradient gel electrophoresis analysis of 16S rRNA from human fecal samples reveals stable and host-specific communities of active bacteria. Appl. Environ. Microbiol. 64: 3854-3859

    Google Scholar 

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Tannock, G.W. Analysis of the intestinal microflora: a renaissance. Antonie Van Leeuwenhoek 76, 265–278 (1999). https://doi.org/10.1023/A:1002038308506

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