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Either your web browser doesn't support Javascript or it is currently turned off. In the latter case, please turn on Javascript support in your web browser and reload this page. Lactobacillus delbrueckii TU-1, which apparently takes intact inulin into its cells and then degrades it intracellularly, was co-cultured in vitro with L. When L. These results suggest that L. Thus, L. The growth of L. This evidence suggests that prebiotic use of inulin supported the selective growth of intracellular inulin degraders such as L. The Lactobacillus species are among the industrially important lactic acid bacteria, which are found in fermented food products and can provide many beneficial effects to their hosts as probiotic bacteria [ 1 , 2 ]. For example, strains of L.
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Funding acquisition: KA. Project administration: KA RO.
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Funding acquisition: KA. Project administration: KA RO. Supervision: KA RO. On the earlier stages of fermentation up to 9 h , trace mixtures of acetate, lactate, and succinate were detectable; on the later stages after 24 h , larger amounts of acetate accumulated along with some of propionate and butyrate. These patterns were similar to those observed in the original feces.

Thus, this system could serve as a simple model to simulate the diversity as well as the metabolism of human colonic microbiota. Supplementation of the system with several prebiotic oligosaccharides including fructo-, galacto-, isomalto-, and xylo-oligosaccharides; lactulose; and lactosucrose resulted in an increased population in genus Bifidobacterium , concomitant with significant increases in acetate production. The results suggested that this fermentation system may be useful for in vitro , pre-clinical evaluation of the effects of prebiotics prior to testing in humans.

It has long been known that food components ingested by the hosts influence their gut microbiota, both quantitatively and qualitatively [ 4 , 6 ]. Consequently, various functional food components such as prebiotics, probiotics, and biogenics have attracted interest as potential ways to manipulate the gut microbiota and to improve human health [ 7 , 8 ]. Usually, the functionality of such food components has been evaluated by human intervention trials or animal-feeding trials [ 3 , 9 ]. However, human trials often are constrained by ethical considerations [ 10 , 11 ] while animal-feeding trials often give results that are not reproducible in humans, in part because of differences in microbiota composition between those of animals and humans [ 12 , 13 ].

Therefore, it was necessary to develop a relatively simple and short-term in vitro evaluation system that simulates the human colonic microbiota not only metagenomically regarding the composition of microbiota but also metabolically. On the basis of the above considerations, many in vitro models simulating the human intestinal tract have been designed to evaluate the functionality or safety of food components [ 11 , 14 — 18 ].

Such in vitro models offer several advantages, including dynamic sampling over time and high reproducibility, without the ethical issues that can arise in clinical contexts. Previously, several dynamic, multi-compartment culture systems have been designed to replicate the mechanical characteristics of an entire and continuous gastrointestinal tract [ 10 , 19 ]; those systems usually required complex and longer-term experiments for evaluation of functional food components [ 17 ].

Selected molecular techniques, such as denaturing gradient gel electrophoresis and microarray analyses, have been used to perform phylogenetic analyses of the multi-compartment-culture intestinal models [ 17 , 20 ].

However, none of those models has been able to provide sufficient evidence to confirm that the mixture of microorganisms growing in the in vitro system truly represented the taxonomic diversity of the human microbiota [ 10 , 21 ]. Recent developments in molecular biological methods have permitted improved characterization of the gut microbial ecosystem [ 22 ].

Notably, next-generation sequencing NGS has facilitated the analysis of a large number of microorganisms in the human intestinal tract and has provided the reliable taxonomic information about the in vivo microbiota [ 1 , 23 , 24 ]. It may now be possible to analyze associations between the genes of the human intestinal microbiota and host health status.

An extensive reference catalog of microbial genes present in the human intestine has been established [ 1 ]. In addition, bioinformatics for interpretation of the biological and genetic information is in development.

However, the power of NGS has not yet to our knowledge been successfully applied to the comparison of the microbiota in vivo in individual human colon to those of in vitro model systems. Therefore aim of the present study was to construct a simple fermentation system, to provide a novel human colonic model that reliably simulated the composition of the in vivo microbiota as proved by NGS analysis.

In addition, in order to substantiate the practicality of the model, we evaluated the functionality of prebiotics, in this case by testing oligosaccharides that are known to be capable of increasing numbers of genus Bifidobacterium in the human gut [ 8 , 25 , 26 ].

Operations of the single-batch fermentation system were performed using a pH-controlled multi-channel fermenter Bio Jr. The simulator consisted of eight parallel and independent vessels. Fermentation was conducted at a mL working volume per vessel. To mimic the pH of the colon of a healthy adult, the pH was adjusted to 6.

After collection, fecal samples were immediately placed under anaerobic conditions using AnaeroPack Mitsubishi Gas Chemical Co. Each fecal sample was weighed and diluted fold with 0. The human fecal samples were handled under the supervision of Takeshi Azuma, a licensed physician, in accordance with the guidelines of Kobe University Hospital, and a written informed consent was obtained from every volunteer.

All the experimental protocols were approved by the institutional ethics review board at Kobe University. All the methods used in this study were in accordance with the approved guidelines by the Medical Ethics Committee at Kobe University. Aliquots of the fermentation cultures were sampled through the side projection of the vessel without disturbing the internal anaerobic conditions at 0, 6, 9, 12 and 24 h after the initiation of fermentation. One of the vessels was assigned as the negative control without addition of oligosaccharide. Whole genomic DNA from each inoculum or culture was prepared according to the method of Marmur [ 27 ] with minor modifications.

The mixture then was shaken vigorously for 30 s at 5. The primer sets described in S1 Table were used for measuring the partial 16S rRNA gene copy number [ 31 , 32 , 33 , 34 ].

The quantitative measurement by real-time PCR was conducted in triplicate. Standard curves for absolute quantification in the cultures were prepared using 10 2 —10 6 copies of the PCR fragments of the 16S rRNA genes. The correlation coefficients for all the standard curves exceeded 0. Metagenomic data were normalized to the sum of the total genera numbers.

Data from the negative control and the experimental samples with addition of each prebiotics were compared by the Dunnett test using the JMP software package version P-values below 0. The single-batch fermentation system was designed to simulate the human colon. Operation of the batch fermentation system was initiated by inoculation with small amounts of one of the human volunteer fecal samples, which was designated as F female, age 37, Japanese , F female, age 37, Japanese , or M54 male, age 54, Japanese.

Within 24 h after the initiation of fermentation, the glucose originally contained in the medium was consumed completely, and microbial composition was not changed between 24 h and 30 h after the initiation of fermentation S2 Table. Thus, the operational duration was set as 24 h in this study. The composition of representing human gut microbiota that developed in the single-batch fermentation system was examined in detail and compared with that of the original fecal samples.

Bacterial species are known to achieve the highest and representative cell densities among Bacteria, Archaea, and Eukarya contained in human fecal samples [ 37 ]. The total number of eubacteria was calculated to range from Bacterial 16S rRNA gene sequence analysis of the fecal samples was performed using NGS, yielding 12,, quality reads with an average of 1,, reads per sample. According to the obtained sequences, a total of 24 phyla and genera were identified. Bacterial species belonging to phyla Bacteroidetes and Firmicutes have been reported to dominate human feces [ 1 , 2 ] and NGS analysis revealed that these two phyla represented Species belonging to other phyla, Actinobacteria and Verrucomicrobia, were present in minor proportions but had been detected in the fecal samples used to inoculate the cultures.

DNA samples from the fermentation cultures were isolated at 6, 9, and 24 h after inoculation into the batch system and then subjected to bacterial 16S rRNA gene sequence analysis. After 24 h of fermentation, eubacterial copy numbers reached 4.

At the earlier stages of fermentation 6 and 9 h after inoculation , species belonging to phylum Bacteroidetes decreased in number, being replaced primarily by those of phylum Proteobacteria for cultures initiated with either F, F, or M54 inocula.

Subsequently at 24 h after the initiation of fermentation , the numbers of bacteria belonging to phylum Bacteroidetes gradually increased to replace those of Proteobacteria, achieving dominance, accounting for Proportions of species of phylum Actinobacteria were largely unchanged in the fermentation cultures, while those of phylum Verrucomicrobia drastically decreased as the fermentation proceeded. A compositional view of bacterial phyla based on the taxonomic assignment of 16S rRNA genes is shown. Bacterial composition of each sample was estimated from the results of the RDP classifier.

The microbial composition was further examined at the genus level S2 Fig. In all three cases, the majority of the species of phylum Bacteroidetes belonged to genus Bacteroides in both the original fecal samples and the single-batch fermentation cultures. In the inocula, bacteria of phylum Firmicutes consisted primarily of genus Blautia ; this prevalence was maintained only in the M54 fermentation culture, while bacteria of genera Enterococcus and Streptococcus , which had been minor in the original F and F inocula, respectively, became the majority genera of this phylum in the corresponding fermentation cultures in vitro.

Bacteria of the phylum Proteobacteria were primarily members of the genus Escherichia , both in the inocula and during culturing, and this pattern was largely extended in the fermentation cultures.

In the fecal inocula, species of phylum Actinobacteria belonged mainly to genus Bifidobacterium , and were well maintained in the fermentation cultures. In contrast, the majority of the bacteria of phylum Verrucomicrobia in the original fecal samples belonged to genus Akkermansia , but most of these organisms were lost during the in vitro cultivation. Therefore, at the phylum level, the single-batch fermentation system maintained and simulated proportions of the majority of the bacterial species that dominated in the original fecal samples, including members of phyla Bacteroidetes and Firmicutes.

However, at the genus level, the single-batch fermentation system did not always reproduce the microbial composition of the inoculating fecal samples. The Shannon-Wiener index of the original human fecal samples 2.

Additionally, the numbers of species also exhibited changes similar to those seen by the Shannon-Wiener index as cultivation proceeded Fig 2B. That is, at earlier stages, species numbers in the fermentation systems fell compared to those observed in the fecal inocula, but numbers subsequently rose to levels almost the same as the original ones by 24 h.

On the other hand, a PCA indicated a transition in the composition of the microbiota at the species level in fermentation systems Fig 3. Compositions of the bacterial community in the single-batch fermentation cultures diverged greatly from those of the original fecal samples at earlier fermentation stages, but gradually came back to those of the respective inocula at later time points, coinciding with the tendencies observed in diversity and number of the species.

The Shannon-Wiener diversity index characterizes the diversity in a community, i. F, F, and M54 are indicated in blue, orange, and green, respectively. The numbers indicate the sampling time points. Short-chain fatty acids SCFA are metabolic products of the human gut microbiota that are absorbed by the host; these metabolites have been associated with benefits for host health [ 38 ]. Therefore, we monitored the SCFA profiles in the in vitro fermentation cultures.

In the three fecal samples obtained from human volunteers, SCFAs consisted mainly of acetate, propionate, and butyrate Fig 4A. The single-batch fermentation system showed a constant increase in acetate, propionate, and butyrate throughout the operational duration Fig 4B. At 24 h after the initiation of fermentation, acetate became the predominant SCFA, followed by propionate and butyrate, almost consistent with the pattern in the original human fecal samples Fig 4A.

Through the first 9 h after the initiation of fermentation, production of lactate and succinate was observed, along with subsequent lactate consumption in F, F, and M54 and succinate consumption in F and F cultures Fig 4B.

Caproate was detected only at very low levels throughout the operation. Values of the ratios are shown as the percentage of the sum of acetate, propionate, and butyrate concentrations. We evaluated the effect on bacteria of genus Bifidobacterium of adding each of these prebiotic oligosaccharides to the single-batch fermentation system. For these experiments, inocula were obtained from six human volunteers F female, age 37; F female, age 23; M male, age 38; F female, age 35; M male, age 24; M male, age At 24 h after the initiation of fermentation, the numbers of total eubacteria and those belonging to genus Bifidobacterium were estimated by quantitative PCR analysis.

In majority of the cases 33 of 42 total trials , eubacterial copy numbers were not significantly changed compared to the control system by the addition of prebiotic oligosaccharides to the medium Fig 5. However, in 35 cases out of 42 total trials, addition of the prebiotic oligosaccharides yielded a significant increase compared to unsupplemented control cultures in the ratios of bacteria belonging to genus Bifidobacterium as a fraction of total eubacteria Fig 5.

Among the prebiotics, the sole exception was raffinose: in cultures from 4 of 6 human subjects including F37, F35, M24, and M43 inocula , its addition did not increase the proportion of bacteria of genus Bifidobacterium. In addition, raffinose did not increased acetate production at 24 h after the initiation of fermentation, in contrast to significant elevation in acetate production observed with other the prebiotic oligosaccharides Table 1. On the other hand, increases or decreases in the production of propionate and butyrate were not found in cultures that incorporated any of the prebiotic oligosaccharides.

Error bars show standard deviation for mean of triplicates. Changes are presented as the ratio of concentration in the experimental system normalized to that in the control system without added prebiotics. In this study, the total number of eubacteria in the inoculating fecal samples was calculated to range



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