Recent work characterized the chicken reproductive tract (oviduct) microbiome composition and its similarity to the egg and chick microbiomes. However, the origin of the oviduct microbiome has not been addressed yet. Here, we characterized the microbiome composition along the oviduct (infundibulum, magnum, and shell gland) as well as in the gut (jejunum and cecum) of broiler breeders at 37 weeks of age of the Cobb industrial breed. We found that while the microbiome composition along the oviduct is similar, the three sites, jejunum, cecum, and oviduct hold distinct microbiomes. However, there was also a large overlap in the composition of the gut and oviduct microbiomes, with 55 and 53% of amplicon sequence variants (ASVs) representing 96 and 90% of the total abundance in the jejunum and cecum, respectively, shared with the magnum. Furthermore, we identified a strong correlation between the relative abundance of ASVs in the gut and their probability to be found in the oviduct. These results suggest that material from the gut travels the full length of the oviduct. This is possibly the result of chicken physiology which includes the cloaca, a cavity to which both the intestinal and reproductive tracts open into. As the cloaca is common to birds, reptiles, amphibians, most fish, and monotremes, our finding may be relevant to many vertebrates. Importantly, these results indicate that mere presence in, and ascending of the oviduct are not virulence characteristics specific to pathogens, as commonly thought, but are the result of chicken physiology and characterize all gut bacteria. Furthermore, whereas a vertical transmission route from the hen to the chick has been suggested, our work starts laying a mechanistic foundation to this route, by describing the movement of gut bacteria to the oviduct, where they may be enclosed in the developing egg. Last, as our results show that gut material travels the full length of the oviduct, fertilization in poultry occurs in the presence of at least bacterial products if not live bacteria, and therefore food additives, probiotics, and diet possibly have a much more direct effect on reproduction and egg formation than previously considered.

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In the last century broiler chicken lines have undergone an extensive breeding regime aimed primarily at growth and high meat yield. It is not known if breeding has also resulted in a change to the broiler breeder’s associated gut microbiota. Here we compared the gut microbiota of 37-week-old commercial Cobb breeding dams with dams from a broiler Legacy line which has not undergone selection since 1986. The dams from both lines were kept together in the same shed under the same management protocol from day of hatch to avoid additional confounders. We chose this age to allow significant bacterial exchange, thus avoiding exposure dependent artifacts and so that we could compare dams at the same developmental state of adulthood and peak laying performance. Significant differences in the composition of the cecum bacterial communities were found. Bacteria of the genus Akkermansia, implicated in mucin degradation and associated with host metabolic health, accounted for 4.98% ± 5.04% of the Cobb cecum community, but were mostly absent from the ceca of the Legacy line dams. Inversely, Legacy dams had higher levels of Clostridiales, Lactobacillales and Aeromonadales. These results show that breeding has resulted in a change in the gut microbiota composition, likely by changing the physiological conditions in the mucosa. It remains unclear if changes in gut microbiota composition are a part of the mechanism affecting growth or are a secondary result of other physiological changes accelerating growth. Therefore, the identification of these changes opens the door to further targeted research.

Background: Efficient vertical transmission of commensal gut microbes is important for the host in order to promote gut microbiota functions such as protection from gut pathogens, and for gut microbes considering microbial competition over limited niche space. While the role of direct contact with parents in transmission is well established, conflicting reports exist regarding transmission in commercial settings where chicks are raised separated from adults, including the utilization of the chicken egg as a transmission mechanism. This question is also relevant to other vertebrates which leave their eggs after laying. Results: We compared the fecal microbiota of poultry chicks hatched and grown separately, with the microbiota of their mothers over three rounds of egg incubation and chick growth. We found that most bacterial strains identified in the hens did not appear at all in chicks up to two weeks of age. Furthermore, most of the strains common with the hens which did appear in chicks had a low incidence among the chicks. Thus, the gut microbiota of hens does not efficiently transmit to chicks when there is no contact with adults. That been said, a few bacterial strains common with the hens were good colonizers of chicks; these included members of Lactobacillales and Enterobacteriales. Finally, we performed two interventions in an attempt to disrupt transmission. In round two, we sprayed a disinfectant on half of the eggs. In round three, we treated half of the hens with an antibiotic cocktail which decimated their cecum and fecal microbiota. Both interventions resulted in a reduction in chick colonization. Interestingly, both interventions affected strains shared with the hens as well as strains not identified in hen samples, implying many ‘environmental’ opportunistic strains reach the chicks through the egg. Conclusions: To conclude, vertical transmission in commercial poultry grown separately from hens likely exists but is not efficient, possibly resulting in impairment of microbiota function as evidenced by sensitivity of chicks to gut pathogens. These results also imply that artificial exposure to adult hen bacterial strains might result in improved microbiota functioning.

The existence of vertical transmission in chickens under commercial settings, where chicks are raised separated from adults, is unclear. To answer this question, the fecal microbiota of chicks hatched and grown separately was compared with their mothers’ microbiota. Most amplicon sequence variants (ASVs) identified in hens did not appear at all in chicks up to two weeks of age, and those that did appear had a low incidence among the chicks. Nevertheless, a few ASVs that were common with the hens were highly prevalent among the chicks, implying they were efficiently transmitted to chicks. These ASVs were culturable from the reproductive tract of hens and eggshells. Furthermore, interventions attempting to disrupt transmission resulted in a reduction of prevalence in chicks. To conclude, vertical transmission in commercial poultry grown separately from adults likely exists but is not efficient, possibly resulting in impairment of microbiota function. This implies that artificial exposure to adult bacterial strains might improve microbiota functioning.