Patterns of community assembly in the developing chicken microbiome reveal rapid primary succession.

Stephanie D. Jurburg,Daniela Ceccarelli,Michael S. M. Brouwer,Alex Bossers,Jeanet van der Goot,Alfons J. M. Jansman

doi:10.1002/mbo3.821

Abstract

The fine‐scale temporal dynamics of the chicken gut microbiome are unexplored, but thought to be critical for chicken health and productivity. Here, we monitored the fecal microbiome of healthy chickens on days 1–7, 10, 14, 21, 28, and 35 after hatching, and performed 16S rRNA amplicon sequencing in order to obtain a high‐resolution census of the fecal microbiome over time. In the period studied, the fecal microbiomes of the developing chickens showed a linear‐log increase in community richness and consistent shifts in community composition. Three successional stages were detected: the first stage was dominated by vertically transmitted or rapidly colonizing taxa including Streptococcus and Escherichia/Shigella; in the second stage beginning on day 4, these taxa were displaced by rapid‐growing taxa including Lachnospiraceae and Ruminococcus‐like species variants; and in the third stage, starting on day 10, slow‐growing, specialist taxa including Candidatus Arthrobacter and Romboutsia were detected. The patterns of displacement and the previously reported ecological characteristics of many of the dominant taxa observed suggest that resource competition plays an important role in regulating successional dynamics in the developing chicken gut. We propose that the boundaries between successional stages (3–4 and 14–21 days after hatching) may be optimal times for microbiome interventions.

Highlights

The last half century has seen poultry production in the world grow more than fivefold, and this trend is expected to continue (FAO, 2016)
The proposed mechanism for this is direct or indirect competition for resources in the gastrointestinal tract (GIT) with the native microbes, resulting in a lack of available niche space (Nurmi & Rantala, 1973). This concept was developed from studies which found that broilers were most vulnerable to Salmonella infantis during the first week after hatching, and that the oral administration of a mixed bacterial culture derived from the GIT of adult chickens resulted in prevention of colonization by S. infantis in young broilers (Nurmi & Rantala, 1973; Rantala & Nurmi, 1973)
We focused on the fecal microbiome as a proxy for the GIT microbial development because of the ease of sampling for high temporal resolutions, and because we were interested in successional dynamics in the GIT rather than the exact composition of a specific section of the GIT microbiome

Summary

| INTRODUCTION

The last half century has seen poultry production in the world grow more than fivefold, and this trend is expected to continue (FAO, 2016). The proposed mechanism for this is direct or indirect competition for resources in the GIT with the native microbes, resulting in a lack of available niche space (Nurmi & Rantala, 1973) This concept was developed from studies which found that broilers were most vulnerable to Salmonella infantis during the first week after hatching, and that the oral administration of a mixed bacterial culture derived from the GIT of adult chickens resulted in prevention of colonization by S. infantis in young broilers (Nurmi & Rantala, 1973; Rantala & Nurmi, 1973). Our aims were (a) to reveal the temporal dynamics of microbial colonization of the broiler GIT, and (b) to contribute further resolution and mechanistic insight into the susceptibility of the GIT microbiome to interventions in early life, as applied to broilers

| MATERIALS AND METHODS

Findings

| DISCUSSION