Influence of Maternal Bifidobacteria on the Establishment of Bifidobacteria Colonizing the Gut in Infants

212

201

Passage through the birth canal and consequent exposure to the mother's microbiota is considered to represent the initiating event for microbial colonization of the gastrointestinal tract of the newborn. However, a precise evaluation of such suspected vertical microbiota transmission has yet to be performed. Here, we evaluated the microbiomes of four sample sets, each consisting of a mother's fecal and milk samples and the corresponding infant's fecal sample, by means of amplicon-based profiling supported by shotgun metagenomics data for two key samples. Notably, targeted genome reconstruction from microbiome data revealed vertical transmission of a Bifidobacterium breve strain and a Bifidobacterium longum subsp. longum strain from mother to infant, a notion confirmed by strain isolation and genome sequencing. Furthermore, PCR analyses targeting unique genes from these two strains highlighted their persistence in the infant gut at 6 months. Thus, this study demonstrates the existence of specific bifidobacterial strains that are common to mother and child and thus indicative of vertical transmission and that are maintained in the infant for at least relatively short time spans.H uman beings may be considered superorganisms that consist of both eukaryotic and prokaryotic cells (1). It is generally accepted, not only that the nuclear and mitochondrial genomes are transferred to the next generation, but that such transfer may also include certain members and associated genomes of the symbiotic community, whose microbial genes outnumber those of the eukaryotic host by over 100-fold (2). Passage through the birth canal, together with breastfeeding, represents a very important opportunity for transfer of symbionts from one generation to the next. Notably, this transmission is facilitated by the maternal holobiont, i.e., the organism, together with its associated microbial communities, and the mother is both actively and passively engaged in providing a symbiotic and perhaps long-lasting microbial community to her offspring. However, each individual develops a specific microbial community by adulthood, suggesting that stochastic colonization is more important than direct vertical transmission. In fact, while individual strains may be directly transmitted, the majority of the long-lasting community is probably not. In mammals, it is generally accepted that the fetus develops in an essentially sterile environment within the amnion and that bacterial colonization of the fetus is made possible as soon as the amnion breaks prior to its delivery through the birth canal (3). Bifidobacteria are among the first bacterial colonizers of the human gut and have been subject to extensive scientific scrutiny (4, 5). It has become clear that certain species of the genus Bifidobacterium, e.g., Bifidobacterium breve and Bifidobacterium bifidum, are genetically adapted to colonize the infant gut (for a review, see reference 6). Such bacteria have evolved genetic strategies that allow them to metabolize particular glycans present in human ...

mentioning

confidence: 99%

mentioning

confidence: 99%

Exploring Vertical Transmission of Bifidobacteria from Mother to Child

Milani

Mancabelli

Lugli

et al. 2015

212

201

“…Recent studies have also discussed that breast milk can be another source of intestinal microbes (20,22,28,31). Several studies employing molecular biology techniques have suggested the possibility of vertical mother-toinfant transmission of intestinal microbes (1,25,26,32) and the presence of these microorganisms in breast milk (12,21,28). However, the molecular methods used in those studies, such as real-time quantitative PCR (qPCR), while effective in identifying microorganisms at the species level, do not allow comparisons at the strain level.…”

mentioning

confidence: 99%

Transmission of Intestinal Bifidobacterium longum subsp. longum Strains from Mother to Infant, Determined by Multilocus Sequencing Typing and Amplified Fragment Length Polymorphism

Makino¹,

Kushiro

Ishikawa

et al. 2011

180

143

The gastrointestinal tracts of neonates are colonized by bacteria immediately after birth. It has been discussed that the intestinal microbiota of neonates includes strains transferred from the mothers. Although some studies have indicated possible bacterial transfer from the mother to the newborn, this is the first report confirming the transfer of bifidobacteria at the strain level. Here, we investigated the mother-to-infant transmission of Bifidobacterium longum subsp. longum by genotyping bacterial isolates from the feces of mothers before delivery and of their infants after delivery. Two hundred seven isolates from 8 pairs of mothers and infants were discriminated by multilocus sequencing typing (MLST) and amplified fragment length polymorphism (AFLP) analysis. By both methods, 11 strains of B. longum subsp. longum were found to be monophyletic for the feces of the mother and her infant. This finding confirms that these strains were transferred from the intestine of the mother to that of the infant. These strains were found in the first feces (meconium) of the infant and in the feces at days 3, 7, 30, and 90 after birth, indicating that they stably colonize the infant's intestine immediately after birth. The strains isolated from each family did not belong to clusters derived from any of the other families, suggesting that each motherinfant pair might have unique family-specific strains.

“…Bacterial DNA from the samples was analyzed by real-time PCR to count the lactobacilli according to the method reported by Mikami et al (16). The Lactobacillus genus-specific paired primers, LactoF (5Ј-TGGAAACAGRTGCTAATACCG-3Ј) and LactoR (5Ј-GTCCATTGTGGAAGATTCCC-3Ј), used in this study have been described previously by Byun et al (5).…”

Section: Methodsmentioning

confidence: 99%

“…The composition of Lactobacillus species in the stomachs of SPF mice was examined using 11 different species-specific primers reported by Walter et al (26). The extraction of bacterial DNA from the stomach and PCR amplification were done according to a method described elsewhere (16).…”

Section: Methodsmentioning

confidence: 99%

Role of Indigenous Lactobacilli in Gastrin-Mediated Acid Production in the Mouse Stomach

Takahashi¹,

Nakano²,

Matsuoka³

et al. 2011

Self Cite

It is known that the stomach is colonized by indigenous lactobacilli in mice. The aim of this study was to examine the role of such lactobacilli in the development of the stomach. For a DNA microarray analysis, germ-free BALB/c mice were orally inoculated with 10 9 CFU lactobacilli, and their stomachs were excised after 10 days to extract RNA. As a result, lactobacillus-associated gnotobiotic mice showed dramatically decreased expression of the gastrin gene in comparison to germ-free mice. The mean of the log 2 fold change in the gastrin gene was ؊4.3. Immunohistochemistry also demonstrated the number of gastrin-positive (gastrin ؉ ) cells to be significantly lower in the lactobacillus-associated gnotobiotic mice than in the germ-free mice. However, there was no significant difference in the number of somatostatin ؉ cells in these groups of mice. Consequently, gastric acid secretion also decreased in the mice colonized by lactobacilli. In addition, an increase in the expression of the genes related to muscle system development, such as nebulin and troponin genes, was observed in lactobacillus-associated mice. Moreover, infection of germ-free mice with Helicobacter pylori also showed the down-and upregulation of gastrin and muscle genes, respectively, in the stomach. These results thus suggested that indigenous lactobacilli in the stomach significantly affect the regulation of gastrinmediated gastric acid secretion without affecting somatostatin secretion in mice, while H. pylori also exerts such an effect on the stomach.The human stomach contains only a few species of bacteria if it is free from infection with Helicobacter pylori (3). During fasting, gastric juice contains only small numbers of bacteria, approximately 10 2 to 10 3 /ml, which include Streptococcus, Lactobacillus, and Veillonella. However, these bacteria are considered nonresidents that are only in transit from the oral cavity and throat (13,19). The scarcity of such bacteria in the human stomach appears to be due to the high acidity of the luminal medium.While H. pylori is a well-known pathogenic bacterium that causes peptic ulcers and cancer in the human stomach, the bacterium has also been proposed to belong to the indigenous gastric microbiota of humans from the earliest times (2). That hypothesis is supported by the fact that H. pylori is acquired in early childhood and thereafter remains stably colonizing the stomach for decades in substantial numbers. This raises questions about the role of H. pylori as the indigenous bacteria of the stomach in the physiological development and function of the organ. However, it is difficult to clarify the answers to this question by an infection study using H. pylori, because various pathogenic factors of H. pylori, such as CagA, vacuolating toxins, and urease and its metabolites, induce chronic pathological inflammation in the gastric tissue, which obscures the physiological role of H. pylori as an indigenous bacterium.In a previous study (12), we found an indigenous microbiota that predominantly consists...