This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Harmsen, H. J. M.
Right arrow Articles by Welling, G. W.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Harmsen, H. J. M.
Right arrow Articles by Welling, G. W.
Agricola
Right arrow Articles by Harmsen, H. J. M.
Right arrow Articles by Welling, G. W.

 Previous Article  |  Next Article 

Applied and Environmental Microbiology, June 2002, p. 2982-2990, Vol. 68, No. 6
0099-2240/02/$04.00+0     DOI: 10.1128/AEM.68.6.2982-2990.2002
Copyright © 2002, American Society for Microbiology. All Rights Reserved.

Extensive Set of 16S rRNA-Based Probes for Detection of Bacteria in Human Feces

Hermie J. M. Harmsen, Gerwin C. Raangs, Tao He, John E. Degener, and Gjalt W. Welling*

Department of Medical Microbiology, University of Groningen, 9700 RB Groningen, The Netherlands

Received 28 December 2001/ Accepted 3 April 2002


arrow
ABSTRACT
 
For the detection of six groups of anaerobic bacteria in human feces, we designed seven new 16S rRNA-based oligonucleotide probes. This set of probes extends the current set of probes and gives more data on the composition of the human gut flora. Probes were designed for Phascolarctobacterium and relatives (Phasco741), Veillonella (Veil223), Eubacterium hallii and relatives (Ehal1469), Lachnospira and relatives (Lach571), and Eubacterium cylindroides and relatives (Ecyl387), and two probes were designed for Ruminococcus and relatives (Rbro730 and Rfla729). The hybridization conditions for the new probes were optimized for fluorescent in situ hybridization, and the probes were validated against a set of reference organisms. The probes were applied to fecal samples of 11 volunteers to enumerate their target bacterial groups. The Phasco741 and Veil223 probes both detected average numbers below 1% of the total number of bacteria as determined with the bacterial kingdom-specific Bact338 probe. The Ecyl387 probe detected about 1.4%, the Lach571 and Ehal1469 probes detected 3.8 and 3.6%, respectively, and a combination of the Rbro730 and Rfla729 probes detected 10.3%. A set of 15 probes consisting of probes previously described and those presented here were evaluated in hybridization with the fecal samples of the same volunteers. Together, the group-specific probes detected 90% of the total bacterial cells.


arrow
INTRODUCTION
 
The human gut flora is a complex ecosystem involved in human nutrition and health (6). Encouraged by medicine and the food industry, research is currently being undertaken to stimulate that fraction of the microbiota that is beneficial for human health (9-11). For evaluation of such studies, accurate analysis of the intestinal microbiota is required. This microbiota consists mostly of anaerobic bacteria that are not easy to enumerate by conventional culturing techniques (12, 23). Therefore, for the last few years, interest in molecular analysis of human gut microbiota has been rapidly growing. Techniques such as sequence analysis of clone libraries from amplified fecal ribosomal DNA (rDNA) and denaturing or temperature-gradient gel electrophoresis (DGGE/TGGE) analysis of the amplified rDNA and rRNA have demonstrated the enormous diversity of species that thrive in the human gut (32, 36, 38). For quantitative analysis of human gut and fecal flora, 16S rRNA-based oligonucleotides were designed that were applied as either primers in PCR (27) or as probes in fluorescent in situ hybridization (FISH) (8, 13, 15). For this purpose, a large set of probes that covers around 80% of the total microbiota has already been described (8). However, detection of the remaining 20% is still a challenge. Analysis of clone libraries of 16S rDNA amplified from total fecal DNA showed the presence of sequences related to Phascolarctobacterium, Ruminococcus flavefaciens, and Eubacterium cylindroides (32). However, no group-specific probes for in situ hybridization existed to detect the bacteria corresponding to these sequences, and quantitative data about the numbers of these bacteria in feces are scarce. Veillonella can be cultured from feces of newborn children (14, 18, 19) and therefore might be present in feces from adults as well. Furthermore, the specific probe Erec482 for the Eubacterium rectale-Clostridium coccoides group detects about one-third of the total microbiota (8). This group might be too large to detect subtle variations in microbiota and therefore needs to be divided into smaller subgroups. Some probes that divide the Erec482 group have already been described, but this development needs to be continued (29). In this paper, we describe seven new group-specific probes to investigate the composition of the human gut microbiota. Together with the previously described probes with which other major groups of human gut bacteria can be detected, they form an extensive probe set for analysis of human gut microbiota (8, 13, 15). This probe set consisting of 15 probes was used to describe the composition of the fecal microbiota of 11 healthy human volunteers.


arrow
MATERIALS AND METHODS
 
Organisms and culture conditions.
All reference strains used in this study are listed in Table 1. The strains were obtained from different sources as indicated in the table: DSM is Deutsche Sammlung von Mikroorganismen und Zellkulturen (Braunschweig, Germany), ATCC is the American Type Culture Collection (Rockville, Md.), NIZO is The Netherlands Institute for Dairy Research (Ede, The Netherlands), and MMB is the Laboratory for Medical Microbiology (Groningen, The Netherlands). DSM or ATCC strains were cultivated on the media described in the respective catalogues. All other strains were cultivated in anoxic peptone-yeast extract-glucose (PYG) medium (15) under anaerobic conditions at 37°C or, in the case of facultative anaerobes, on brain heart infusion agar (Oxoid, Basingstoke, United Kingdom). All MMB strains are clinical or human fecal isolates from local and regional public health laboratories and have been identified by routine procedures.


View this table:
[in this window]
[in a new window]
  		TABLE 1. Organisms used in the FISH specificity studies and the results of the FISH specificity tests

Design and testing of oligonucleotide probes.
Oligonucleotide probes were designed with the ARB software package (24), and rRNA sequences were obtained in an aligned form from the Ribosomal Database Project (RDP) (25) supplemented with newly deposited rRNA sequences from GenBank. Fluorescein-labeled oligonucleotides against selected group-specific target sequences were synthesized commercially (Eurogentec, Seraing, Belgium) and tested for specificity against a set of reference organisms listed in Table 1. For this purpose, paraformaldehyde (PFA)-fixed cells of the reference strains were applied to slides and hybridized overnight at 50°C in hybridization buffer (0.9 M NaCl, 20 mM Tris-HCl [pH 7.2], 0.1% sodium dodecyl sulfate [wt/vol]) containing 5 ng of labeled probe µl-1 as described previously (8). If more stringent conditions were needed, formamide was added to the hybridization buffer in concentrations ranging from 0 to 60% (vol/vol). For hybridization with the Rbro730 and Rfla729 probes, cells were incubated prior to hybridization with 10 µl of 1 mg of lysozyme ml-1 in 100 mM Tris-HCl (pH 8.5) for 10 min at room temperature. Phylogenetic trees illustrating the target groups of the extensive probe set (Fig. 1) were generated with the ARB software package by applying the neighbor-joining method to a relevant selection of sequences from the database of the RDP comprising around 20,000 sequences.



View larger version (46K):
[in this window]
[in a new window]
  		FIG. 1. Phylogenetic tree based on 16S rRNA sequences illustrating the target groups of the newly described probes and the other probes of the extensive gut microbiota probe set. The tree shows the relationship between the major genera, groups, and organisms known to be present in the human gut. The species or clone sequences with their corresponding accession numbers are the target organisms that have a full match with the newly described oligonucleotide probes depicted behind the vertical bars on the right. Boxes and group names in boldface indicate that the target groups of the probes have been described previously. The sizes of the boxes reflect the number of sequences used in the tree construction, and their shape reflects the phylogenetic depth of the corresponding groups. The size bar at the bottom represents 10% sequence divergence.

Enumeration of bacteria in fecal samples by FISH.
Eleven healthy volunteers ranging from 20 to 55 years provided fresh fecal stools. Portions (0.5 g) of each stool were fixed with PFA as described previously (8). Dry weights were determined by lyophilizing a weighed portion of each homogenized fecal sample.

Fecal samples were applied to glass slides by the protocol described previously (16), except that the dilution of the PFA-fixed fecal samples was made in phosphate-buffered saline and not in 5% Tween solution. The slides were hybridized with the (newly designed) probes or stained with diamidino-2-phenylindole (DAPI) as described previously (8, 16). The fluorescent cells in the samples were counted automatically (16) with a Leica DMRXA epifluorescence microscope (Leica, Wetzlar, Germany), except when the number of cells was lower than 4 x 108 cells g-1 (wet weight): in that situation, the cells were counted visually with an Olympus BH2 epifluorescence microscope.


arrow
RESULTS
 
Design and specificity of oligonucleotide probes.
Seven specific probes were designed to extend the existing set of probes for fecal bacteria. These probes are listed together with their target organisms in Table 2. A schematic representation of the probes and their target groups is shown in Fig. 1 as a phylogenetic tree. The probe Phasco741 was for the Phascolarctobacterium group, which includes the species Phascolarctobacterium faecium, Acidaminococcus fermentans, and Succiniclasticum ruminis, members of the Clostridium cluster IX, as described before (3). The probe Veil223 was used for members of the genus Veillonella (e.g., V. dispar, V. parvula, and V. atypica). The remaining two members of the genus, V. ratti and V. criceti, have one G-T mismatch on position 9 from the 5' end of the probe and will probably hybridize with the probe under the hybridization conditions in Table 2. The probe Ehal1469 is for the Eubacterium hallii group, including E. hallii, Clostridium herbivorans, and Clostridium polysaccharolyticum, which are members of the Clostridium cluster XIVa (3). The probe Lach571 is specific for other members of cluster XIVa: the Lachnospira group, which includes the species Lachnospira multipara, Eubacterium eligens, and Lachnospira pectinoschiza. The probe Ecyl387 is specific for members of Clostridium cluster XVI, referred to here as the Eubacterium cylindroides group. The Rfla729 and the Rbro730 probes are specific for members of Clostridium cluster IV, Clostridium leptum, Clostridium sporosphaeroides, and ruminococci related to these bacteria, including Ruminococcus flavefaciens, Ruminococcus albus, and Ruminococcus bromii. Ruminococcus callidus and Eubacterium siraeum, both members of cluster IV, have only one mismatch to the Rfla729 probe. Probe design was based on 16S rRNA sequences of known bacteria and on sequences from human fecal clone libraries (32). In order to test the specificity of the newly designed probes, a selection of target and nontarget bacterial strains was hybridized in situ with the probes. This included strains with one or two mismatches in the target sequence of the 16S rRNA. The strains were hybridized and washed at 50°C. The specificity was optimized with a range of formamide concentrations in the hybridization buffer. After hybridization, the strains were screened for fluorescent signals and compared with those obtained after hybridization with bacterial probe Bact338 as a positive control and its complement non-Bact338 as the negative control. Table 1 shows the results of these hybridizations under the optimized conditions described in Table 2. All probes were specific for their target organisms, except for the Rbro730 probe and the Rfla729 probe. The Rbro730 probe also hybridized to R. albus, which has one U-G mismatch on position 13 from the 5' end of the probe. If Rbro730 is used in conjunction with the Rfla729 probe, this will not cause any problems, because the target groups overlap. The Rfla729 probe cross-reacted with R. callidus and E. siraeum, which both have one G-T mismatch on position 10 from the 5' end of the probe. Because of their close relationship with the target organisms, this cross-reaction is favorable. It would be possible to include these two species in the target group by introducing a wobble base on the mismatching position. However, this creates new single mismatches with unwanted species, and therefore this idea was rejected. The Lach571 probe has only one mismatch with many Bacteroides species. However at 60% formamide, the probe did not show fluorescence with these Bacteroides species. In addition, it was found that lowering the salt concentration from 0.9 to 0.4 M NaCl in combination with 40% formamide effected brighter signals with the target species without giving rise to fluorescence with the Bacteroides species. This was chosen as the optimal hybridization condition.


View this table:
[in this window]
[in a new window]
  		TABLE 2. Seven new probes, their target species, probe sequences, and optimal hybridization conditions for the detection of human fecal bacteria

Application of the probe in enumeration of the bacterial group in human feces.
The newly designed probes were used in FISH experiments to enumerate the numbers of their target groups in fecal samples from 11 healthy volunteers. The results were listed in Table 3. The Ecyl387 probe detected 1.5 x 109 cells per g (dry weight), representing 1.8% of the total (Bact338) (range, 0.05 to 7.4%). The probes detected mostly cylindrical small rods, presumably E. cylindroides (Fig. 2A), and sometimes detected C. innocuum-like thin rods. A combination of the Rbro729 and the Rfla730 probes detected a mean number of 1.4 x 1010 cells per g (dry weight) of feces. This was 10% of the total hybridizable cell count (Bact338), which ranged from 0.6 to 28%. The probes detected brightly fluorescing cocci—presumably ruminococci—and some weakly fluorescing rods, presumably clostridia of group IV (Fig. 2B). The Veil223 probe detected 108 cells per g (dry weight). The only morphology detected was represented by small Veillonella-like cocci (Fig. 2C); on average, 0.08% of the total bacterial cells were within the range not detectable to 0.5% detectable. The Phasco741 probe detected 9.0 x 108 cells per g (dry weight), representing 0.6% of the total (Bact338) and ranging from not detectable to 2.6% detectable. The bacteria that were detected by the Phasco741 probe were all rods about 4 to 6 µm long—presumably Phascolarctobacterium or Succiniclasticum cells (Fig. 2D). The Lach571 probe also detected 5.1 x 109 cells per g (dry weight), representing 3.6% of the total (Bact338) and ranging from 1.6 to 13.6%. The morphology detected by the Lach571 probe was more diverse, ranging from large oval dividing rods (Fig. 2E) to thin rods (Fig. 2F). The Ehal1469 probe detected 5.1 x 109 cells per g (dry weight), representing 3.8% of the total (Bact338) and ranging from 0.9 to 8.2%. Their main morphology was represented by pairs of rods about 2 µm in length (Fig. 2G), although in some cases, longer rods were seen.


View this table:
[in this window]
[in a new window]
  		TABLE 3. Numbers and percentages of fecal microorganisms from 11 volunteers as determined by DAPI staining (total cells) and by hybridization with bacterial probe Bact338 (total bacteria) or newly designed probes



View larger version (76K):
[in this window]
[in a new window]
  		FIG. 2. FISH experiments with the newly designed probes on fecal samples from different volunteers. (A) Epifluorescent images of a hybridization with the Ecyl387 probe specific for the E. cylindroides group showing small fluorescent rods. (B) Hybridization with a combination of the Rbro729 and the Rfla730 probes specific for bacteria of the Ruminococcus group; the image shows one rod and different cocci. (C) Hybridization with the Veil223 probe specific for Veillonella showing small cocci. (D) Hybridization with the Phasco741 probe detecting rods of the Phascolarctobacterium group. (E and F) Two images of different fecal samples hybridized with the Lach571 probe specific for the Lachnospira group showing big oval dividing rods and one thin rod (E) or only thin rods (F). (G) Hybridization with the Ehal1469 probe showing rods of the E. hallii group. Bar, 5 µm.

Evaluation of the coverage of the extensive probe set for detecting specific bacterial groups in human feces.
A set of 15 probes were used to evaluate how much of the total microbiota was detected with these probes specific for the major bacterial groups in human feces. Furthermore, differences in counts with the various probes between individuals were analyzed. The extensive set of probes consists of the probes presented in Fig. 1 and the Bact338 probe specific for virtually all bacteria (1). Apart from the newly described seven probes, probes for other fecal bacterial groups designed and validated elsewhere were used to enumerate bacteria in the same fecal samples as described above. These were (i) Bact338 to detect the total hybridizable bacterial cells; (ii) the Erec482 probe for most members of the Clostridium group XIVa (8); (iii) Bac303 for most Bacteroides and Prevotella bacteria (26); (iv) Bif164 for the genus Bifidobacterium (23); (v) Elgc01 for Fusobacterium prausnitzii-related eubacteria (8, 36); (vi) Ato291 for the Atopobium group, with Collinsella aerofaciens as the predominant fecal species (13); (vii) Ecoli1531 for Escherichia coli and related species (28); and (viii) Lab158 for enterococci and lactobacilli (15). For this enumeration, the same 11 fecal samples described above were used. DAPI staining was used to enumerate the total amount of cells in these samples. The mean results for the 11 individuals with the 15 probes are presented in Table 4. The mean counts are given in cells per gram in both dry weight and wet weight to make the results more comparable with data from the literature.


View this table:
[in this window]
[in a new window]
  		TABLE 4. Mean numbers per gram of feces, CVs, and percentages of total microbiota from 11 volunteersa

We determined the coefficient of variation due to the enumeration assay itself (CVassay) by repeating the assay, including sample preparation, 12 times on the same stool sample. The fluorescent cells were enumerated automatically on the Leica DMRXA epifluorescence microscope. The CVassays with a 1,600x dilution of the fecal sample were 0.15 for DAPI staining and 0.09 for hybridization with Bact338. The CVassays were 0.16 for Erec482 at a 400 times dilution, 0.28 for Bif164 at a 160 times dilution, and 0.12 for Lach571 at a 40 times dilution. For the other probes, the average CVassay (0.16) of the four aforementioned FISH probes was used. The CV between individuals (CVinter) was determined by correcting the total variation (CVtotal) between the individuals for the CVassay (16). For all probes combined, the CVinter was more than two times higher than the CVassay, showing that the variation between samples can be determined by this FISH method. A high CVinter indicates a large variation between the samples of the volunteers. In general, the CVinter is high when the percentage of bacteria detected with a specific probe is low, especially those of probes that do not detect bacteria in all individual samples. The CVinter (1.07) found with the Rbro729 and Rfla730 probes was remarkably high, which indicates that there are large differences between volunteers with respect to the numbers of bacteria of this group. Summation of the percentages of the cells detected and identified with group-specific probes resulted in 56.2% for DAPI-stained cells or 90.5% for the total bacterial cells enumerated with the Bact338 probe. The Ehal1469 and Lach571 probes were excluded from this summation, since they detect a group of bacteria already covered by the Erec482 probe.


arrow
DISCUSSION
 
A set of seven new oligonucleotide probes is presented to extend the set of probes for the predominant microbiota of the human gastrointestinal tract and in particular for fecal bacteria. Five of the seven probes each detected an average of more than 1% of the total bacterial microbiota. Especially the probes for the ruminococci and related Clostridium group IV bacteria are valuable, since these probes detected 10% of the fecal bacteria, and this group of bacteria is likely to have interesting metabolic features, such as degradation of complex carbohydrates. The numbers of the ruminococcus group are within the range earlier estimated in human feces by culture techniques (7), in which a mean of 1.6 x 1010 g-1 (dry weight) was found. Also the numbers of the Eubacterium cylindroides group are within the reported ranges. The numbers of C. innocuum, E. cylindroides, and Eubacterium dolichum enumerated previously showed a large variation between the subjects with mean numbers of 4 x 108, 4 x 109, and 4 x 108 · g-1 (dry weight), respectively (7). FISH with three species-specific probes for E. cylindroides, Eubacterium biforme, and E. dolichum detected 9 x 107, 2 x 108, and 0 cells g-1 (dry weight), respectively (28). Out of 12 volunteers, 2 possessed E. cylindroides cells and 6 possessed E. biforme cells (29). Although the Veil223 and the Phasco741 probes detected a minor percentage of the total bacteria, they are interesting as well. Veillonella may play a role in microbiota development at an early age (14), and the Phascolarctobacterium group is a fairly unknown group of bacteria with interesting metabolic properties, such as succinate decarboxylation (17). The number of Veillonella cells reported here is in the same order of magnitude as that reported earlier in feces of adults in which 8 x 107 cells per g were enumerated (7). The Ehal1469 and Lach571 probes specific for subgroups within the Erec482 group detect 3.8 and 3.6% of the total fecal bacteria, respectively. When comparing fecal samples, significant changes in the target groups of these probes would be difficult to detect with Erec482, which accounts on average for 22.7% of the bacterial microbiota.

The newly designed probes described in this study are additional to the existing set of probes, complementing it to an extensive set of 15 probes. Several other probes that can be useful for gut microbiota studies exist. For instance, a new group-specific probe was proposed for Fusobacterium prausnitzii and related species (33) that could be an alternative for the Elgc01 probe. Also the group-specific probe of the Clostridium leptum group (30) would be very useful, because it detects even more target species than the Ruminococcus group probes described here. However, this probe is used in dot blot hybridization and does not function well in FISH (results not shown). Species-specific probes have been designed for members of the genera Bacteroides (5), Bifidobacterium (37), Eubacterium (29, 31), and Ruminococcus (21, 22). Although all of these probes are useful to specifically detect these species in the gut microbiota, for total microbiota analysis, the use of probes with narrow specificity is too laborious.

With the extensive set of group-specific probes used in this study, we can detect 90.5% of the total bacterial microbiota detected with the Bact338 probe. However, of the total DAPI-stained cells, only 56.2% are detected by this extensive probe set and 60.9% are detected by the bacterial probe Bact338. This might indicate that still 38% of cells remains undetected. Several reasons why these cells are not detected come to mind. They may belong to the Archaea or the Eucarya. They may simply be dead cells. They may be not permeable or metabolically active. Finally, the target site for the single Bact338 probe used here (1) may be absent in some bacterial species (4). The specific probes detect bacteria also detected by the Bact338 probe. However, some groups of bacteria need lysozyme permeabilization for effective hybridization, such as ruminococci and lactobacilli. These bacteria are detected by the specific probes, since we use lysozyme in the protocol, but not by the Bact338 probe, in which no lysozyme treatment is used. Despite these considerations, the extensive probe set still does not cover all bacterial cells. Therefore, the need for further probe development remains.

The results obtained in this study with the probes described earlier are in agreement with data we presented previously (8), although the mean counts are now on average 1.5 times lower. The CVinter values presented here are in the same range as those determined previously (8), indicating the reliability of these values. High CVinter values indicate large differences between the volunteers. This makes these probes useful as sensitive parameters in the analysis of variations in composition of microbiota in relation to health and disease or as a result of modulation by pre- or probiotics. The probes described earlier have already been successfully applied in microbiota analysis to study the relationship between microbiota development and atopy in children (18), the relationship between microbiota and milk hypersensitivity (2), and to study the effects of prebiotics (20, 34, 35). Currently, the new probes are applied to study the gut microbiota composition in relation to age, health, and disease. This extensive probe set will make FISH a more valuable and sensitive tool to study the human gut microbiota.


arrow
ACKNOWLEDGMENTS
 
We thank A. C. M. Wildeboer-Veloo and R. H. J. Tonk for technical assistance and all of the volunteers for providing a stool sample.

This work was supported by the European Research Project Fair-CT-97-3035.


arrow
FOOTNOTES
 
* Corresponding author. Mailing address: Department of Medical Microbiology, University of Groningen, P.O. Box 30001, 9700 RB Groningen, The Netherlands. Phone: 31 50 3633510. Fax: 31 50 3633528. E-mail: g.w.welling{at}med.rug.nl. Back


arrow
REFERENCES
 
    1
  1. Amann, R. I., B. J. Binder, R. J. Olson, S. W. Chisholm, R. Devereux, and D. A. Stahl. 1990. Combination of 16S rRNA-targeted oligonucleotide probes with flow cytometry for analyzing mixed microbial populations. Appl. Environ. Microbiol. 56:1919-1925.[Abstract/Free Full Text]
    2. 2
  2. Apostolou, E., L. Pelto, P. V. Kirjavainen, E. Isolauri, S. J. Salminen, and G. R. Gibson. 2001. Differences in the gut bacterial flora of healthy and milk-hypersensitive adults, as measured by fluorescence in situ hybridization. FEMS Immunol. Med. Microbiol. 30:217-221.[CrossRef][Medline]
    3. 3
  3. Collins, M. D., P. A. Lawson, A. Willems, J. J. Cordoba, J. Fernandez-Garayzabal, P. Garcia, J. Cai, H. Hippe, and J. A. E. Farrow. 1994. The phylogeny of the genus Clostridium: proposal of five new genera and eleven new species combinations. Int. J. Syst. Bacteriol. 44:812-826.[Abstract/Free Full Text]
    4. 4
  4. Daims, H., A. Bruhl, R. Amann, K. H. Schleifer, and M. Wagner. 1999. The domain-specific probe EUB338 is insufficient for the detection of all bacteria: development and evaluation of a more comprehensive probe set. Syst. Appl. Microbiol. 22:434-444.[Medline]
    5. 5
  5. Doré, J., A. Sghir, G. Hannequart-Gramet, G. Corthier, and P. Pochart. 1998. Design and evaluation of a 16S rRNA-targeted oligonucleotide probe for specific detection and quantitation of human faecal Bacteroides populations. Syst. Appl. Microbiol. 21:65-71.[Medline]
    6. 6
  6. Falk, P. G., L. V. Hooper, T. Midtvedt, and J. I. Gordon. 1998. Creating and maintaining the gastrointestinal ecosystem: what we know and need to know from gnotobiology. Microbiol. Mol. Biol. Rev. 62:1157-1170.[Abstract/Free Full Text]
    7. 7
  7. Finegold, S. M., V. L. Sutter, and G. E. Mathisen. 1983. Normal indigenous intestinal flora, p. 3-31. In D. J. Hentges (ed.), Human intestinal microflora in health and disease. Academic Press, NewYork, N.Y.
    8. 8
  8. Franks, A. H., H. J. M. Harmsen, G. C. Raangs, G. J. Jansen, F. Schut, and G. W. Welling. 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.[Abstract/Free Full Text]
    9. 9
  9. Gibson, G. R., and M. B. Roberfroid. 1995. Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics. J. Nutr. 125:1401-1412.
    10. 10
  10. Goldin, B. R., S. L. Gorbach, M. Saxelin, S. Barakat, L. Gualtieri, and S. Salminen. 1992. Survival of Lactobacillus species (strain GG) in human gastrointestinal tract. Dig. Dis. Sci. 37:121-128.[CrossRef][Medline]
    11. 11
  11. Gorbach, S. L., and B. R. Goldin. 1992. Nutrition and the gastrointestinal microflora. Nutr. Rev. 50:378-381.[Medline]
    12. 12
  12. Harmsen, H. J., G. R. Gibson, P. Elfferich, G. C. Raangs, A. C. Wildeboer-Veloo, A. Argaiz, M. B. Roberfroid, and G. W. Welling. 2000. Comparison of viable cell counts and fluorescence in situ hybridization using specific rRNA-based probes for the quantification of human fecal bacteria. FEMS Microbiol. Lett. 183:125-129.[CrossRef][Medline]
    13. 13
  13. Harmsen, H. J. M., A. C. M. Wildeboer-Veloo, J. Grijpstra, J. Knol, J. E. Degener, and G. W. Welling. 2000. Development of 16S rRNA-based probes for the Coriobacterium group and the Atopobium cluster and their application for enumeration of Coriobacteriaceae in human feces from volunteers of different age groups. Appl. Environ. Microbiol. 66:4523-4527.[Abstract/Free Full Text]
    14. 14
  14. Harmsen, H. J. M., A. C. Wildeboer-Veloo, G. C. Raangs, A. A. Wagendorp, N. Klijn, J. G. Bindels, and G. W. Welling. 2000. Analysis of intestinal flora development in breast-fed and formula-fed infants by using molecular identification and detection methods. J. Pediatr. Gastroenterol. Nutr. 30:61-67.[CrossRef][Medline]
    15. 15
  15. Harmsen, H. J. M., P. Elfferich, F. Schut, and G. W. Welling. 1999. A 16S rRNA-targeted probe for detection of lactobacilli and enterococci in fecal samples by fluorescent in situ hybridization. Microb. Ecol. Health Dis. 11:3-12.
    16. 16
  16. Jansen, G. J., A. C. Wildeboer-Veloo, R. H. Tonk, A. H. Franks, and G. W. Welling. 1999. Development and validation of an automated, microscopy-based method for enumeration of groups of intestinal bacteria. J. Microbiol. Methods 37:215-221.[CrossRef][Medline]
    17. 17
  17. Janssen, P. H., and K. A. O'Farrell. 1999. Succinispira mobilis gen. nov., sp. nov., a succinate-decarboxylating anaerobic bacterium. Int. J. Syst. Bacteriol. 49:1009-1013.[Abstract/Free Full Text]
    18. 18
  18. Kalliomäki, M., P. Kirjavainen, E. Eerola, P. Kero, S. Salminen, and E. Isolauri. 2001. Distinct patterns of neonatal gut microflora in infants in whom atopy was and was not developing. J. Allergy Clin. Immunol. 107:129-134.[CrossRef][Medline]
    19. 19
  19. Kleessen, B., H. Bunke, K. Tovar, J. Noack, and G. Sawatzki. 1995. Influence of two infant formulas and human milk on the development of the faecal flora in newborn infants. Acta Paediatr. 84:1347-1356.[Medline]
    20. 20
  20. Kleessen, B., L. Hartmann, and M. Blaut. 2001. Oligofructose and long-chain inulin: influence on the gut microbial ecology of rats associated with a human faecal flora. Br. J. Nutr. 86:291-300.[Medline]
    21. 21
  21. Krause, D. O., R. J. Bunch, L. L. Conlan, P. M. Kennedy, W. J. Smith, R. I. Mackie, and C. S. McSweeney. 2001. Repeated ruminal dosing of Ruminococcus spp. does not result in persistence, but changes in other microbial populations occur that can be measured with quantitative 16S-rRNA-based probes. Microbiology 147:1719-1729.[Abstract/Free Full Text]
    22. 22
  22. Krause, D. O., B. P. Dalrymple, W. J. Smith, R. I. Mackie, and C. S. McSweeney. 1999. 16S rDNA sequencing of Ruminococcus albus and Ruminococcus flavefaciens: design of a signature probe and its application in adult sheep. Microbiology 145:1797-1807.[Abstract/Free Full Text]
    23. 23
  23. Langendijk, P. S., F. Schut, G. J. Jansen, G. C. Raangs, G. R. Kamphuis, M. H. F. Wilkinson, and G. W. Welling. 1995. Quantitative fluorescence in situ hybridization of Bifidobacterium spp. with genus-specific 16S rRNA-targeted probes and its application in fecal samples. Appl. Environ. Microbiol. 61:3069-3075.[Abstract]
    24. 24
  24. Ludwig, W., O. Strunk, S. Klugbauer, N. Klugbauer, M. Weizenegger, J. Neumaier, M. Bachleitner, and K. H. Schleifer. 1998. Bacterial phylogeny based on comparative sequence analysis. Electrophoresis 19:554-568.[CrossRef][Medline]
    25. 25
  25. Maidak, B. L., J. R. Cole, C. T. J. Parker, G. M. Garrity, N. Larsen, B. Li, T. G. Lilburn, M. J. McCaughey, G. J. Olsen, R. Overbeek, S. Pramanik, T. M. Schmidt, J. M. Tiedje, and C. R. Woese. 1999. A new version of the RDP (Ribosomal Database Project). Nucleic Acids Res. 27:171-173.[Abstract/Free Full Text]
    26. 26
  26. Manz, W., R. Amann, W. Ludwig, M. Vancanneyt, and K. H. Schleifer. 1996. Application of a suite of 16S rRNA-specific oligonucleotide probes designed to investigate bacteria of the phylum cytophaga-flavobacter-bacteroides in the natural environment. Microbiology 142:1097-1106.[Abstract/Free Full Text]
    27. 27
  27. Matsuki, T., K. Watanabe, R. Tanaka, M. Fukuda, and H. Oyaizu. 1999. Distribution of bifidobacterial species in human intestinal microflora examined with 16S rRNA-gene-targeted species-specific primers. Appl. Environ. Microbiol. 65:4506-4512.[Abstract/Free Full Text]
    28. 28
  28. Poulsen, L. K., T. R. Licht, C. Rang, K. A. Krogfelt, and S. Molin. 1995. Physiological state of Escherichia coli BJ4 growing in the large intestines of streptomycin-treated mice. J. Bacteriol. 177:5840-5845.[Abstract/Free Full Text]
    29. 29
  29. Schwiertz, A., G. Le Blay, and M. Blaut. 2000. Quantification of different Eubacterium spp. in human fecal samples with species-specific 16S rRNA-targeted oligonucleotide probes. Appl. Environ. Microbiol. 66:375-382.[Abstract/Free Full Text]
    30. 30
  30. Sghir, A., G. Gramet, A. Suau, V. Rochet, P. Pochart, and J. Doré. 2000. Quantification of bacterial groups within human fecal flora by oligonucleotide probe hybridization. Appl. Environ. Microbiol. 66:2263-2266.[Abstract/Free Full Text]
    31. 31
  31. Simmering, R., B. Kleessen, and M. Blaut. 1999. Quantification of the flavonoid-degrading bacterium Eubacterium ramulus in human fecal samples with a species-specific oligonucleotide hybridization probe. Appl. Environ. Microbiol. 65:3705-3709.[Abstract/Free Full Text]
    32. 32
  32. Suau, A., R. Bonnet, M. Sutren, J.-J. Godon, G. R. Gibson, M. D. Collins, and J. Doré. 1999. Direct analysis of genes encoding 16S rRNA from complex communities reveals many novel molecular species within the human gut. Appl. Environ. Microbiol. 65:4799-4807.[Abstract/Free Full Text]
    33. 33
  33. Suau, A., V. Rochet, A. Sghir, G. Gramet, S. Brewaeys, M. Sutren, L. Rigottier-Gois, and J. Doré. 2001. Fusobacterium prausnitzii and related species represent a dominant group within the human fecal flora. Syst. Appl. Microbiol. 24:139-145.[CrossRef][Medline]
    34. 34
  34. Tuohy, K. M., R. K. Finlay, A. Wynne, and G. R. Gibson. 2001. A human volunteer study on the prebiotic effects of HP-inulin: faecal bacteria enumerated using fluorescent in situ hybridisation (FISH). Anaerobe 7:113-118.
    35. 35
  35. Tuohy, K. M., S. Kolida, A. M. Lustenberger, and G. R. Gibson. 2001. The prebiotic effects of biscuits containing partially hydrolysed guar gum and fructo-oligosaccharides—a human volunteer study. Br. J. Nutr. 86:341-348.[Medline]
    36. 36
  36. Wilson, K. H., and R. B. Blitchington. 1996. Human colonic biota studied by ribosomal DNA sequence analysis. Appl. Environ. Microbiol. 62:2273-2278.[Abstract]
    37. 37
  37. Yamamoto, T., M. Morotomi, and R. Tanaka. 1992. Species-specific oligonucleotide probes for five Bifidobacterium species detected in human intestinal microflora. Appl. Environ. Microbiol. 58:4076-4079.[Abstract/Free Full Text]
    38. 38
  38. Zoetendal, E. G., A. D. L. Akkermans, and W. M. De Vos. 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.[Abstract/Free Full Text]

Applied and Environmental Microbiology, June 2002, p. 2982-2990, Vol. 68, No. 6
0099-2240/02/$04.00+0     DOI: 10.1128/AEM.68.6.2982-2990.2002
Copyright © 2002, American Society for Microbiology. All Rights Reserved.



This article has been cited by other articles:

  • Klaassens, E. S., Boesten, R. J., Haarman, M., Knol, J., Schuren, F. H., Vaughan, E. E., de Vos, W. M. (2009). Mixed-Species Genomic Microarray Analysis of Fecal Samples Reveals Differential Transcriptional Responses of Bifidobacteria in Breast- and Formula-Fed Infants. Appl. Environ. Microbiol. 75: 2668-2676 [Abstract] [Full Text]  
  • Matsuda, K., Tsuji, H., Asahara, T., Matsumoto, K., Takada, T., Nomoto, K. (2009). Establishment of an Analytical System for the Human Fecal Microbiota, Based on Reverse Transcription-Quantitative PCR Targeting of Multicopy rRNA Molecules. Appl. Environ. Microbiol. 75: 1961-1969 [Abstract] [Full Text]  
  • Zoetendal, E G, Rajilic-Stojanovic, M, de Vos, W M (2008). High-throughput diversity and functionality analysis of the gastrointestinal tract microbiota. Gut 57: 1605-1615 [Abstract] [Full Text]  
  • Walter, J. (2008). Ecological Role of Lactobacilli in the Gastrointestinal Tract: Implications for Fundamental and Biomedical Research. Appl. Environ. Microbiol. 74: 4985-4996 [Full Text]  
  • Hong, P.-Y., Wu, J.-H., Liu, W.-T. (2008). Relative Abundance of Bacteroides spp. in Stools and Wastewaters as Determined by Hierarchical Oligonucleotide Primer Extension. Appl. Environ. Microbiol. 74: 2882-2893 [Abstract] [Full Text]  
  • Belenguer, A., Duncan, S. H., Holtrop, G., Anderson, S. E., Lobley, G. E., Flint, H. J. (2007). Impact of pH on Lactate Formation and Utilization by Human Fecal Microbial Communities. Appl. Environ. Microbiol. 73: 6526-6533 [Abstract] [Full Text]  
  • Robert, C., Chassard, C., Lawson, P. A., Bernalier-Donadille, A. (2007). Bacteroides cellulosilyticus sp. nov., a cellulolytic bacterium from the human gut microbial community. Int. J. Syst. Evol. Microbiol. 57: 1516-1520 [Abstract] [Full Text]  
  • Lunn, J.C., Kuhnle, G., Mai, V., Frankenfeld, C., Shuker, D.E.G., Glen, R. C., Goodman, J.M., Pollock, J.R.A., Bingham, S.A. (2007). The effect of haem in red and processed meat on the endogenous formation of N-nitroso compounds in the upper gastrointestinal tract. Carcinogenesis 28: 685-690 [Abstract] [Full Text]  
  • Swidsinski, A, Goktas, O, Bessler, C, Loening-Baucke, V, Hale, L P, Andree, H, Weizenegger, M, Holzl, M, Scherer, H, Lochs, H (2007). Spatial organisation of microbiota in quiescent adenoiditis and tonsillitis. J. Clin. Pathol. 60: 253-260 [Abstract] [Full Text]  
  • Duncan, S. H., Belenguer, A., Holtrop, G., Johnstone, A. M., Flint, H. J., Lobley, G. E. (2007). Reduced Dietary Intake of Carbohydrates by Obese Subjects Results in Decreased Concentrations of Butyrate and Butyrate-Producing Bacteria in Feces. Appl. Environ. Microbiol. 73: 1073-1078 [Abstract] [Full Text]  
  • Matsuda, K., Tsuji, H., Asahara, T., Kado, Y., Nomoto, K. (2007). Sensitive Quantitative Detection of Commensal Bacteria by rRNA-Targeted Reverse Transcription-PCR. Appl. Environ. Microbiol. 73: 32-39 [Abstract] [Full Text]  
  • Mohan, R., Koebnick, C., Schildt, J., Schmidt, S., Mueller, M., Possner, M., Radke, M., Blaut, M. (2006). Effects of Bifidobacterium lactis Bb12 Supplementation on Intestinal Microbiota of Preterm Infants: a Double-Blind, Placebo-Controlled, Randomized Study. J. Clin. Microbiol. 44: 4025-4031 [Abstract] [Full Text]  
  • Aminov, R. I., Walker, A. W., Duncan, S. H., Harmsen, H. J. M., Welling, G. W., Flint, H. J. (2006). Molecular Diversity, Cultivation, and Improved Detection by Fluorescent In Situ Hybridization of a Dominant Group of Human Gut Bacteria Related to Roseburia spp. or Eubacterium rectale. Appl. Environ. Microbiol. 72: 6371-6376 [Abstract] [Full Text]  
  • Kuhbacher, T, Ott, S J, Helwig, U, Mimura, T, Rizzello, F, Kleessen, B, Gionchetti, P, Blaut, M, Campieri, M, Folsch, U R, Kamm, M A, Schreiber, S (2006). Bacterial and fungal microbiota in relation to probiotic therapy (VSL#3) in pouchitis. Gut 55: 833-841 [Abstract] [Full Text]  
  • Belenguer, A., Duncan, S. H., Calder, A. G., Holtrop, G., Louis, P., Lobley, G. E., Flint, H. J. (2006). Two Routes of Metabolic Cross-Feeding between Bifidobacterium adolescentis and Butyrate-Producing Anaerobes from the Human Gut.. Appl. Environ. Microbiol. 72: 3593-3599 [Abstract] [Full Text]  
  • Maukonen, J., Satokari, R., Matto, J., Soderlund, H., Mattila-Sandholm, T., Saarela, M. (2006). Prevalence and temporal stability of selected clostridial groups in irritable bowel syndrome in relation to predominant faecal bacteria.. J Med Microbiol 55: 625-633 [Abstract] [Full Text]  
  • Haarman, M., Knol, J. (2006). Quantitative Real-Time PCR Analysis of Fecal Lactobacillus Species in Infants Receiving a Prebiotic Infant Formula. Appl. Environ. Microbiol. 72: 2359-2365 [Abstract] [Full Text]  
  • Snart, J., Bibiloni, R., Grayson, T., Lay, C., Zhang, H., Allison, G. E., Laverdiere, J. K., Temelli, F., Vasanthan, T., Bell, R., Tannock, G. W. (2006). Supplementation of the diet with high-viscosity Beta-glucan results in enrichment for lactobacilli in the rat cecum.. Appl. Environ. Microbiol. 72: 1925-1931 [Abstract] [Full Text]  
  • Mueller, S., Saunier, K., Hanisch, C., Norin, E., Alm, L., Midtvedt, T., Cresci, A., Silvi, S., Orpianesi, C., Verdenelli, M. C., Clavel, T., Koebnick, C., Zunft, H.-J. F., Dore, J., Blaut, M. (2006). Differences in Fecal Microbiota in Different European Study Populations in Relation to Age, Gender, and Country: a Cross-Sectional Study. Appl. Environ. Microbiol. 72: 1027-1033 [Abstract] [Full Text]  
  • He, T., Priebe, M. G., Harmsen, H. J.M., Stellaard, F., Sun, X., Welling, G. W., Vonk, R. J. (2006). Colonic Fermentation May Play a Role in Lactose Intolerance in Humans. J. Nutr. 136: 58-63 [Abstract] [Full Text]  
  • van Tongeren, S. P., Slaets, J. P. J., Harmsen, H. J. M., Welling, G. W. (2005). Fecal Microbiota Composition and Frailty. Appl. Environ. Microbiol. 71: 6438-6442 [Abstract] [Full Text]  
  • Ben-Amor, K., Heilig, H., Smidt, H., Vaughan, E. E., Abee, T., de Vos, W. M. (2005). Genetic Diversity of Viable, Injured, and Dead Fecal Bacteria Assessed by Fluorescence-Activated Cell Sorting and 16S rRNA Gene Analysis. Appl. Environ. Microbiol. 71: 4679-4689 [Abstract] [Full Text]  
  • O'May, G. A., Reynolds, N., Macfarlane, G. T. (2005). Effect of pH on an In Vitro Model of Gastric Microbiota in Enteral Nutrition Patients. Appl. Environ. Microbiol. 71: 4777-4783 [Abstract] [Full Text]  
  • Mennink-Kersten, M. A. S. H., Ruegebrink, D., Klont, R. R., Warris, A., Gavini, F., Op den Camp, H. J. M., Verweij, P. E. (2005). Bifidobacterial Lipoglycan as a New Cause for False-Positive Platelia Aspergillus Enzyme-Linked Immunosorbent Assay Reactivity. J. Clin. Microbiol. 43: 3925-3931 [Abstract] [Full Text]  
  • Walker, A. W., Duncan, S. H., McWilliam Leitch, E. C., Child, M. W., Flint, H. J. (2005). pH and Peptide Supply Can Radically Alter Bacterial Populations and Short-Chain Fatty Acid Ratios within Microbial Communities from the Human Colon. Appl. Environ. Microbiol. 71: 3692-3700 [Abstract] [Full Text]  
  • Lay, C., Rigottier-Gois, L., Holmstrom, K., Rajilic, M., Vaughan, E. E., de Vos, W. M., Collins, M. D., Thiel, R., Namsolleck, P., Blaut, M., Dore, J. (2005). Colonic Microbiota Signatures across Five Northern European Countries. Appl. Environ. Microbiol. 71: 4153-4155 [Abstract] [Full Text]  
  • Swidsinski, A., Weber, J., Loening-Baucke, V., Hale, L. P., Lochs, H. (2005). Spatial Organization and Composition of the Mucosal Flora in Patients with Inflammatory Bowel Disease. J. Clin. Microbiol. 43: 3380-3389 [Abstract] [Full Text]  
  • Haarman, M., Knol, J. (2005). Quantitative Real-Time PCR Assays To Identify and Quantify Fecal Bifidobacterium Species in Infants Receiving a Prebiotic Infant Formula. Appl. Environ. Microbiol. 71: 2318-2324 [Abstract] [Full Text]  
  • Swidsinski, A, Schlien, P, Pernthaler, A, Gottschalk, U, Barlehner, E, Decker, G, Swidsinski, S, Strassburg, J, Loening-Baucke, V, Hoffmann, U, Seehofer, D, Hale, L P, Lochs, H (2005). Bacterial biofilm within diseased pancreatic and biliary tracts. Gut 54: 388-395 [Abstract] [Full Text]  
  • Matsuki, T., Watanabe, K., Fujimoto, J., Takada, T., Tanaka, R. (2004). Use of 16S rRNA Gene-Targeted Group-Specific Primers for Real-Time PCR Analysis of Predominant Bacteria in Human Feces. Appl. Environ. Microbiol. 70: 7220-7228 [Abstract] [Full Text]  
  • Duncan, S. H., Louis, P., Flint, H. J. (2004). Lactate-Utilizing Bacteria, Isolated from Human Feces, That Produce Butyrate as a Major Fermentation Product. Appl. Environ. Microbiol. 70: 5810-5817 [Abstract] [Full Text]  
  • Brummel, T., Ching, A., Seroude, L., Simon, A. F., Benzer, S. (2004). Drosophila lifespan enhancement by exogenous bacteria. Proc. Natl. Acad. Sci. USA 101: 12974-12979 [Abstract] [Full Text]  
  • Konstantinov, S. R., Awati, A., Smidt, H., Williams, B. A., Akkermans, A. D. L., de Vos, W. M. (2004). Specific Response of a Novel and Abundant Lactobacillus amylovorus-Like Phylotype to Dietary Prebiotics in the Guts of Weaning Piglets. Appl. Environ. Microbiol. 70: 3821-3830 [Abstract] [Full Text]  
  • Gueimonde, M., Tolkko, S., Korpimaki, T., Salminen, S. (2004). New Real-Time Quantitative PCR Procedure for Quantification of Bifidobacteria in Human Fecal Samples. Appl. Environ. Microbiol. 70: 4165-4169 [Abstract] [Full Text]  
  • Tannock, G. W., Munro, K., Bibiloni, R., Simon, M. A., Hargreaves, P., Gopal, P., Harmsen, H., Welling, G. (2004). Impact of Consumption of Oligosaccharide-Containing Biscuits on the Fecal Microbiota of Humans. Appl. Environ. Microbiol. 70: 2129-2136 [Abstract] [Full Text]  
  • Rawls, J. F., Samuel, B. S., Gordon, J. I. (2004). From The Cover: Gnotobiotic zebrafish reveal evolutionarily conserved responses to the gut microbiota. Proc. Natl. Acad. Sci. USA 101: 4596-4601 [Abstract] [Full Text]  
  • Simpson, P. J., Ross, R. P., Fitzgerald, G. F., Stanton, C. (2004). Bifidobacterium psychraerophilum sp. nov. and Aeriscardovia aeriphila gen. nov., sp. nov., isolated from a porcine caecum. Int. J. Syst. Evol. Microbiol. 54: 401-406 [Abstract] [Full Text]  
  • Zoetendal, E. G., Collier, C. T., Koike, S., Mackie, R. I., Gaskins, H. R. (2004). Molecular Ecological Analysis of the Gastrointestinal Microbiota: A Review. J. Nutr. 134: 465-472 [Abstract] [Full Text]  
  • Mai, V., Katki, H. A., Harmsen, H., Gallaher, D., Schatzkin, A., Baer, D. J., Clevidence, B. (2004). Effects of a Controlled Diet and Black Tea Drinking on the Fecal Microflora Composition and the Fecal Bile Acid Profile of Human Volunteers in a Double-Blinded Randomized Feeding Study. J. Nutr. 134: 473-478 [Abstract] [Full Text]  
  • Matsuki, T., Watanabe, K., Fujimoto, J., Kado, Y., Takada, T., Matsumoto, K., Tanaka, R. (2004). Quantitative PCR with 16S rRNA-Gene-Targeted Species-Specific Primers for Analysis of Human Intestinal Bifidobacteria. Appl. Environ. Microbiol. 70: 167-173 [Abstract] [Full Text]  
  • Hopkins, M. J., Englyst, H. N., Macfarlane, S., Furrie, E., Macfarlane, G. T., McBain, A. J. (2003). Degradation of Cross-Linked and Non-Cross-Linked Arabinoxylans by the Intestinal Microbiota in Children. Appl. Environ. Microbiol. 69: 6354-6360 [Abstract] [Full Text]  
  • Breitbart, M., Hewson, I., Felts, B., Mahaffy, J. M., Nulton, J., Salamon, P., Rohwer, F. (2003). Metagenomic Analyses of an Uncultured Viral Community from Human Feces. J. Bacteriol. 185: 6220-6223 [Abstract] [Full Text]  
  • Xu, J., Gordon, J. I. (2003). Inaugural Article: Honor thy symbionts. Proc. Natl. Acad. Sci. USA 100: 10452-10459 [Abstract] [Full Text]  
  • Hold, G. L., Schwiertz, A., Aminov, R. I., Blaut, M., Flint, H. J. (2003). Oligonucleotide Probes That Detect Quantitatively Significant Groups of Butyrate-Producing Bacteria in Human Feces. Appl. Environ. Microbiol. 69: 4320-4324 [Abstract] [Full Text]  
  • Duncan, S. H., Scott, K. P., Ramsay, A. G., Harmsen, H. J. M., Welling, G. W., Stewart, C. S., Flint, H. J. (2003). Effects of Alternative Dietary Substrates on Competition between Human Colonic Bacteria in an Anaerobic Fermentor System. Appl. Environ. Microbiol. 69: 1136-1142 [Abstract] [Full Text]  

This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Harmsen, H. J. M.
Right arrow Articles by Welling, G. W.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Harmsen, H. J. M.
Right arrow Articles by Welling, G. W.
Agricola
Right arrow Articles by Harmsen, H. J. M.
Right arrow Articles by Welling, G. W.

Copyright © 2009 by the American Society for Microbiology.   For an alternate route to Journals.ASM.org, visit: http://intl-journals.asm.org | More Info»