Broiler chickens and early life programming: Microbiome transplant-induced cecal community dynamics and phenotypic effects

Authors: RAMIREZ, GUSTAVO - Western University Of Health Sciences; RICHARDSON, ELLA - Western University Of Health Sciences; CLARK, JORY - Western University Of Health Sciences; KISHRI, JITENDRA - Western University Of Health Sciences; DRESCHLER, YVONNE - Western University Of Health Sciences; Berrang, Mark; Meinersmann, Richard - Rick; Cox Jr, Nelson; OAKLEY, BRIAN - Western University Of Health Sciences

Submitted to: PLOS ONE
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/26/2020
Publication Date: 11/13/2020
Citation: Ramirez, G., Richardson, E., Clark, J., Kishri, J., Dreschler, Y., Berrang, M.E., Meinersmann, R.J., Cox Jr, N.A., Oakley, B. 2020. Broiler chickens and early life programming: Microbiome transplant-induced cecal community dynamics and phenotypic effects. PLoS ONE. 15(11). Article e0242108. https://doi.org/10.1371/journal.pone.0242108.
DOI: https://doi.org/10.1371/journal.pone.0242108

Interpretive Summary: In modern commercial broiler production, fertile eggs are collected and hatched in clean bio-secure cabinets away from the mother hen. This system is optimal for efficiency and control of pathogenic bacteria. However, commercially hatched chicks are not exposed to beneficial bacteria in the mother's feces and hen house environment. Published reports show that feeding complex bacterial cultures collected from the intestine of Salmonella and Campylobacter free hens to newly hatched broiler chicks establishes mature gut microflora and can prevent intestinal colonization of the growing chick with human pathogens. There is evidence that rapid maturation of gut microflora also improves broiler growth rate. In the current work we compared bacterial cultures from chicken intestinal samples to those collected from the chicken house environment. We compared the types of bacteria present in culture treatments, ability to establish a stable mature broiler chick gut microflora and the affect on broiler growth rate. We found that feeding either culture to chicks changed the gut microflora. Environmental derived cultures were less diverse than those derived from intestinal samples. Microflora of chicks treated with intestinal cultures was less stable in the weeks following initial feeding than in those treated with environmental cultures. Both types of cultures provided some protection against later intestinal colonization of treated chicks with human pathogenic bacteria. The types of bacteria in treated chick intestine were assayed and found to be different depending on type of culture applied. These data are useful to further our understanding of chicken intestinal microflora and how this important population affects chicken health, growth and possibility to carry bacteria dangerous to the eventual human consumer.

Technical Abstract: The concept of successional trajectories describes how small differences in initial community composition can magnify through time and lead to significant differences in mature communities. For many animals, the types and sources of early-life exposures to microbes have been shown to have significant and long-lasting effects on the community structure and/or function of the microbiome. In modern commercial poultry production, chicks are reared as a single age cohort and do not directly encounter adult birds. This scenario is likely to initiate a trajectory of microbial community development that is significantly different than non-industrial settings where chicks are exposed to a much broader range of environmental and fecal inocula; however, the comparative effects of these two scenarios on microbiome development and function remain largely unknown. In this work, we performed serial transfers of cecal material through multiple generations of birds to first derive a stable source of inoculum and then compared microbiome development between chicks receiving this passaged cecal material versus an environmental inoculum to test the hypothesis that the first exposure of newly hatched chicks to microbes determines early GI microbiome structure and may have longer-lasting effects on bird health and development. Cecal microbiome dynamics and bird weights were tracked for a two-week period, with half of the birds in each treatment group exposed to a pathogen challenge at 7d of age. We report that: i) a relatively stable community was derived after a single passage of transplanted cecal material, ii) this cecal inoculum significantly but ephemerally altered community structure relative to the environmental inoculum and phosphate buffer saline (PBS) controls, and iii) either microbiome transplant administered at day-of-hatch appeared to have some protective effects against pathogen challenge relative to uninoculated controls. Differentially abundant taxa were identified across treatment types and may inform future studies and identify strains associated with beneficial phenotypes.