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Applied and Environmental Microbiology, October 2000, p. 4523-4527, Vol. 66, No. 10
Department of Medical Microbiology,
University of Groningen, 9700 RB Groningen,1
and Numico Research B.V., 6700 CA
Wageningen,2 The Netherlands
Received 2 May 2000/Accepted 1 August 2000
Two 16S rRNA-targeted probes were developed: one for the
Coriobacterium group and the other for the
Atopobium cluster (which comprises most of the
Coriobacteriaceae species, including the Coriobacterium group). The new probes were based on
sequences of three new Coriobacteriaceae strains isolated
from human feces and clinical material and sequences from databases.
Application of the probes to fecal samples showed that formula-fed
infants had higher numbers of Coriobacterium group cells in
their feces than breast-fed infants. In addition, based on the
presented results, it is hypothesized that with the increasing age of a
person, the diversity of Atopobium cluster species present
in the feces increases.
In the intestinal tract of all
animals, including humans, a complex community of microorganisms exists
that is generally believed to play an important role in health and
disease (4). Therefore, medical microbiologists and
microbial ecologists have investigated the composition of this
community, i.e., gut microflora, for many decades. Anaerobic culturing
techniques enable cultivation of many numerically important fecal
microorganisms, which can be identified by biochemical techniques
(5). However, it is only since the introduction of molecular
microbiological techniques in intestinal ecology that the full
diversity of the human gut microflora can be assessed (2, 19, 25,
28, 29). 16S rRNA-targeted oligonucleotide probes directed at
different phylogenetic levels (domain, family, genus, species) of the
bacterial kingdom and with which it is possible to identify
quantitatively a large number of different bacterial groups of the gut
ecosystem have been developed (6, 9, 15, 16, 22, 23), even
those that were hitherto nonculturable (28). One group of
anaerobic bacteria, the Coriobacteriaceae, can readily be
cultured from human feces (11). Eggerthella lenta
and Collinsella aerofaciens are the best known
representatives of this group, and C. aerofaciens is an
especially well-known member of the resident microflora (5).
However, these bacteria are underrepresented in clone libraries of the
human gut microbial community (25, 28), and so far, no
specific probe for members of the Coriobacteriaceae has been
designed. In this report, the isolation, characterization, and
phylogenetic analysis of three Coriobacteriaceae strains
from feces and clinical material are described. The 16S rRNA sequences of these isolates formed, together with literature data, the basis for
the development of new specific probes to investigate the abundance of
this group of bacteria in human feces.
Two strains were isolated from human feces of two volunteers (age of
each, 30 years). The isolation was done by plating dilution series on
anaerobic tomato juice agar (per liter, 45 g of Eugonagar [Becton
Dickinson, Cockeysville, Md.], 10 g of maltose, 5 mg of hemin,
400 ml of tomato juice [autoclaved separately]). This medium is used
to enumerate and isolate bifidobacteria from human feces, and it was
noted that on these plates, gram-positive rods that were not
bifidobacteria also grew. The plates were incubated at 37°C in
anaerobic jars with a gas mixture of 90% N2-5%
H2-5% CO2. After 3 days, small translucent
colonies were picked from the 108 dilution, grown on
peptone-yeast-glucose (PYG) medium (10), and Gram stained.
Two gram-positive isolates with an irregular rod shape (G118 and H818)
were selected for further analysis. Coincidentally, a gram-positive
bacterium with a similar irregular rod shape was isolated in the
diagnostic laboratory from a patient's blood culture. This clinical
isolate (EKSO3) was isolated from a blood culture vial by plating on
Brucella blood agar anaerobic plates as previously described
(26). The blood sample originated from a patient who
suffered from colitis probably caused by Crohn's disease and who had,
as complications, an ileus and a perforation in the colon ascendens.
The new strains were deposited at the Deutsche Sammlung von
Mikroorganismen und Zellkulturen (DSMZ) under numbers 13713 (G118),
13712 (H818), and 13714 (EKSO3).
For phylogenetic analysis, DNA of the three new strains was isolated as
previously described (3) and the 16S rRNA gene was amplified
and sequenced using universal 16S rRNA-specific primers (1).
The partial 16S rRNA sequences of G118, H818, and EKSO3 were 1,432, 1,417, and 1,442 nucleotides long, respectively. They were aligned to
reference sequences present in the Ribosomal Database Project (RDP)
(18) and EMBL database by using the ARB software
(17). A phylogenetic tree was constructed using an alignment
from Escherichia coli positions 73 to 1480 by the neighbor joining method with Jukes Cantor correction based on distance matrix
and parsimony, implemented in the ARB software. Figure 1 shows a tree of the phylogenetic
relationship between the isolates and other bacterial species. This
tree indicates that the fecal isolates G118 and H818 belong to the
species C. aerofaciens, fecal bacteria forming lactic acid
and formic acid, hydrogen, and ethanol from glucose (13).
C. aerofaciens was recently renamed from Eubacterium
aerofaciens after the finding that this bacterium is not related
to Eubacterium sp. sensu stricto or clostridia but to the
Coriobacteriaceae (13). The two new strains and
the two C. aerofaciens strains described before have 99%
sequence similarity among each other and have 93% sequence similarity
with strain EKSO3 (Fig. 1). The closest relative of these five strains is Coriobacterium glomerans, a bacterium isolated from the
intestinal tract of the red soldier bug (7), with 92%
sequence similarity. These species belong to the family of
Coriobacteriaceae of the Actinobacteria
subdivision of gram-positive bacteria (21), to which
E. lenta (formerly known as Eubacterium lentum)
and the genera Slackia and Atopobium belong
(14, 24, 27). The group of bacteria of the family
Coriobacteriaceae without the genera Slackia and
Denitrobacterium will be indicated in this paper as the
Atopobium cluster (18).
0099-2240/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.
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
ABSTRACT
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FIG. 1.
Tree based on 16S rRNA sequences showing the
phylogenetic relationship of the newly isolated strains G118, H818, and
EKSO3 with the genus Collinsella and Coriobacterium
glomerans, the family of Coriobacteriaceae, and three
distant bacteria as an outgroup. Accession numbers of the used
sequences are after the species names. *, sequence is available from
the Ribosomal Database Project. (A), specificity of the ATO291 probe;
(CA), the strain hybridizes with both ATO291 and COR653 probes. Numbers
next to the branch nodes indicate bootstrap values (%); only values
more than 90% are shown. Bar, 10% sequence divergence.
Standard tests according to Holdeman et al. (10) were
performed to see what phenotypic characteristics the new strains had and to what extent they differed from those of C. aerofaciens. Gas chromatography of the short-chain fatty acids
produced after growth in PYG medium showed that all strains produced as
main product H2, acetic acid, lactic acid, and ethanol. The
addition of 0.5% Tween 80 increased the maximum growth rate of
C. aerofaciens, G118, and H818 on PYG medium 1.1, 1.4, and
1.3 times, respectively. EKSO3 showed almost no growth on PYG medium,
but the addition of 0.5% Tween 80 resulted in a growth rate (µ) of
0.468 h
1, which was similar to the growth rate of the
other three strains. Therefore, 0.5% Tween 80 was included in the PY
medium for testing of carbohydrate utilization of all strains. The
carbohydrates from which acid was produced are listed in Table
1. Based on the fermentation pattern of
five sugars, the strains could be classified into groups as suggested
by Kageyama et al. (13). The clinical isolate EKSO3 belonged
to group I subgroup C, a subgroup for which so far only one isolate is
described. The C. aerofaciens strains all belonged to group
III since they utilized sucrose but not cellobiose. However, all three
had different fermentation patterns so they should be classified into
different subgroups, although only one subgroup has been defined so far
(13).
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Two specific 16S rRNA-targeted oligonucleotide probes were designed using the ARB software (17) to detect bacteria of the Atopobium group in fecal samples. The first probe, S-*-Cor-0653-a-A-18 (COR653) (5'-CCCTCCC(A/C)TACCGGACCC), is specific for the genera Coriobacterium and Collinsella, here referred to as the Coriobacterium group. The second probe, S-*-Ato-0291-a-A-17 (ATO291) (5'-GGTCGGTCTCTCAACCC), is specific for the Atopobium cluster, which includes the Coriobacterium group. The specificity of the probes as indicated (Fig. 1) was confirmed by testing against a panel of reference strains. This panel consisted of the four strains described in Table 1, C. glomerans, Atopobium minutum, Atopobium parvulum, E. lenta, Slackia exigua, and a panel of 45 obligate anaerobes that were used before as reference strains (6). The probes were used for detection of Coriobacteriaceae organisms in fecal samples of volunteers from different age groups. Fecal samples were prepared and 4',6'-diamidino-2-phenylindole (DAPI) stained as previously described (6) except for the fecal samples from babies which were prepared as mentioned previously (8). Fluorescent in situ hybridizations (FISH) using the COR653, ATO291, and BIF164 probes were performed on the fecal samples at 50°C without addition of formamide, and the fluorescing cells were counted automatically (12), except for the fecal samples of babies, of which the fluorescing cells were counted as previously described (8).
Table 2 shows the number of bacteria
belonging to the Atopobium cluster and, in particular, the
Collinsella group relative to the number of total bacteria
in fecal samples of people belonging to different age groups. For
comparison, the number of bifidobacteria is also shown. In a previous
study with newborn infants, it was already shown that 12 days after
birth, feces of breast-fed babies contained mainly bifidobacteria,
while feces of formula-fed babies contained a more diverse microflora
(8). These data also suggested that a bacterial group
remained undetected in the fecal samples of formula-fed babies.
Therefore, the samples from this previous study were evaluated again in
the present study, and a striking difference between the formula-fed
and breast-fed babies was found. In breast-fed babies, only one out of
six babies contained a small amount of Coriobacterium group
cells, while in formula-fed babies, four out of six babies had large
numbers of Coriobacterium group cells in their feces,
reaching up to 39% of the total bacterial population. In these babies,
all Atopobium probe-positive bacteria also hybridized with
the probe for the Coriobacterium group, identifying them as
such. This was checked by combining the two probes with different
labels in one assay. Figure 2 shows a
phase-contrast image and a fluorescent image of feces from a
formula-fed baby after hybridization with the two probes. The
sample contained about 35% Coriobacterium group
cells, no bifidobacteria, about 40% Bacteroides, and 5%
E. coli. All positive cells show a yellowish fluorescence of
both the green COR653 and the red ATO291 probes. In contrast to these
baby feces samples, in fecal samples of older children and adults, not
all Atopobium group bacteria hybridized to the
Coriobacterium group probe. Figure
3 shows an example of a hybridization
with feces of a young volunteer (10 years old) using the two probes and
also a DAPI counterstaining which intercalates with DNA, thus staining
all DNA-containing cells. The yellowish-white bacteria hybridized with
both probes and were DAPI stained and are therefore
Coriobacterium group bacteria. The remaining red bacteria
are other members of the Atopobium group. This shows that
there are also non-Coriobacterium group cells that are
either true atopobia or related to E. lenta, another
gram-positive rod known to be present in fecal samples (20).
Our results, however, indicate that in the feces of newborn babies,
only bacteria of the Coriobacterium group are present and no
Eggerthella or Atopobium bacteria are present,
while in older children or adults, Eggerthella or
Atopobium can also be found. In elderly people, the
variation in the number of fecal atopobia between individuals was
larger than in children, and relatively more atopobia were detected
that did not hybridize to the probe for the Coriobacterium
group than in children. The numbers of atopobia in feces of adults (25 to 55 years old) were lower than in the former two groups. Currently, it is being investigated whether these age effects are related to diet,
for instance, milk and carbohydrate consumption.
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It is well known from culture-based studies previously described (5, 11) and confirmed with our FISH methodology that Coriobacteriaceae (formerly referred to as E. lentum and E. aerofaciens) form an interesting group of numerically important bacteria in the human intestinal tract. However, this group is often overlooked in other studies in which fecal samples are analyzed using molecular tools (6, 16, 28, 29) and has been mentioned only once so far (25). Surprisingly, they seem to be underrepresented in 16S rRNA clones libraries of total fecal DNA (28, 29). According to Suau et al., this could be due to the PCR conditions used or the high G + C content of the DNA of these bacteria, prohibiting the amplification of coriobacterial rDNA (25). In this study, we also report the isolation of a strain belonging to the Coriobacterium group from a blood culture of a patient suffering from colitis, therefore indicating its potential clinical importance. Based on the phenotypical characteristics, this strain is closely related only to a single isolate of C. aerofaciens grouped as I C according to Kageyama et al. (13). However, based on 16S rRNA analysis, this strain is not closely related to C. aerofaciens as defined previously but seems to belong to a separate genus. This is supported by phenotypic characteristics, such as the fact that strain EKSO3 grew very poorly on PYG medium without Tween 80, unlike the other strains. It would be interesting to analyze the 16S rRNA genes of strains of the different groups according to Kageyama et al. to gather more data for a further taxonomic differentiation of these groups of Collinsella-like strains. C. aerofaciens strains were also isolated from patients with colon cancer, ulcerative colitis, and Crohn's disease (13). It is tempting to suggest a relation between the Coriobacterium group and these diseases. However, many individuals tested had Coriobacterium group cells in their feces, and the beneficial or potentially pathogenic traits of these bacteria still need to be elucidated. The newly designed specific probes may help to investigate the possible involvement of Coriobacteriaceae in gastrointestinal diseases, e.g., bowel cancer pathogenesis, for instance, by studying their attachment to colon tissue by using FISH. The results indicate that bacteria of the Coriobacterium group play a role in the early development of the newborn infant's gut microflora. The molecular tools allow more focused study on the relation of the new strains to the newborn's predominant intestinal bacteria, i.e., Bifidobacterium spp. The data also suggest that with the increasing age of a human, the diversity of Atopobium cluster species present in the feces increases. This phenomenon and especially the role of E. lenta as a major representative of the non-Coriobacterium group needs to be further investigated.
The recent reclassification of C. aerofaciens (13) and our new specific probes give new attention to this group of fecal bacteria. This may help to elucidate their role in food conversion and their interaction with pre- and probiotic food additives and may affect future molecular research on interactions between lactic-acid-producing bacteria in the intestinal tract.
Nucleotide sequence accession numbers. The sequences of the new isolates were deposited in the EMBL database under accession no. AJ245919 (G118), AJ245920 (H818), and AJ245921 (EKSO3).
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ACKNOWLEDGMENTS |
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We thank G. L. Jellema, G. C. Raangs, C. Slootmaker-van der Meulen, R. H. J. Tonk, and E. Poelwijk for their technical assistance.
This work was supported by grant 901-14-167 to G.W.W. from the Netherlands Organization for Scientific Research (NWO) and the European Research Project Fair-CT-97-3035.
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FOOTNOTES |
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* 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.
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Applied and Environmental Microbiology, October 2000, p. 4523-4527, Vol. 66, No. 10
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Copyright © 2000, American Society for Microbiology. All rights reserved.
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