Circadian disruption and divergent microbiota acquisition under extended photoperiod regimens in chicken

Abstract

The gut microbiota is crucial for metabolic homeostasis, immunity, growth and overall health, and it recognized that early-life microbiota acquisition is a pivotal event for later life health. Recent studies show that gut microbiota diversity and functional activity are synchronized with the host circadian rhythms in healthy individuals, and circadian disruption elicits dysbiosis in mammalian models. However, no studies have determined the associations between circadian disruption in early life, microbiota colonization, and the consequences for microbiota structure in birds. Chickens, as a major source of protein around the world, are one of the most important agricultural species, and their gut and metabolic health are significant concerns. The poultry industry routinely employs extended photoperiods (>18 hours’ light) as a management tool, and their impacts on the chicken circadian, its role in gut microbiota acquisition in early life, and consequences for later life microbiota structure remain unknown. In this study, the objectives were to a) characterize chicken circadian activity under two different light regimes (12/12 hours’ Light/Dark and 23/1 hours Light/Dark), b) characterize gut microbiota acquisition and composition in the first four weeks of life, c) determine if gut microbiota oscillate in synchrony with the host circadian, and d) to determine if fecal microbiota is representative of cecal microbiota. Expression of clock genes (clock, bmal1, and per2) were assayed, and fecal and cecal microbiota was characterized using 16s rRNA amplicon analyses from birds raised under two photoperiod treatments. Chickens raised under 12/12 LD photoperiods exhibited rhythmic clock gene activity, which was absent in birds raised under the extended (23/1 LD) photoperiod. This study is also the first to report differential microbiota acquisition under different photoperiod regimes. Gut microbiota members showed a similar oscillating pattern as the host, but this association was not as strong as found in mammals. Finally, the fecal microbiota was found to be not representative of cecal microbiota membership and structure. This is one of the first studies to demonstrate the use of photoperiods to modulate microbiota acquisition, and show its potential utility as a tool to promote the colonization of beneficial microorganisms.

Assembly of hundreds of novel bacterial genomes from the chicken caecum

“…The majority of our MAGs belonged to the orders Oscillospirales and Lachnospirales, members of the Clostridia class. The high abundance of Clostridia observed during our study correlates with several previous studies examining the chicken caecal microbiota [20,[62][63][64][65][66][67]. This is likely the product of chicks being raised in an environment where they are not exposed to a maternal microbiota as feral hens and chicks exposed to an adult hen have microbiotas which are far less dominated by Firmicutes and contain higher abundances of Bacteroidetes [68,69].…”

Assembly of hundreds of novel bacterial genomes from the chicken caecum

“…The majority of our MAGs belonged to the orders Oscillospirales and Lachnospirales , members of the Clostridia class. The high abundance of Clostridia observed during our study correlates with several previous studies examining the chicken cecal microbiota (19, 78–83). This is likely the product of chicks being raised in an environment where they are not exposed to a maternal microbiota as feral hens and chicks exposed to an adult hen have microbiotas which are far less dominated by Firmicutes and contain higher abundances of Bacteroidetes (84, 85).…”

Impact of Housing Environment on the Immune System in Chickens: A Review

“…Distinct light–dark cycles ( L : D ) enable the development of a circadian rhythm [ 97 ]. Broilers given continuous or near-continuous light develop no circadian rhythm, whereas they do under extended dark periods such as 12 L :12 D [ 98 ] or 16 L :8 D [ 99 ]. The development of a circadian rhythm is considered an important indicator of welfare in domestic animals [ 97 ], and its disruption is associated with a variety of metabolic and immune disorders [ 98 ].…”

“…Recently, it has also been demonstrated that the photoperiod affects cecal microbiota in chickens [ 98 ] and that gut microbiota influences behavior, physiology and immune system in chickens [ 173 , 174 ].…”

“…Moreover, there is an impact of the genetic background on gut microbiota composition [ 210 , 211 ] that is clearly associated with host stress response and a mediator of host health. Even though the gut microbiota of chickens has received much attention in recent years and was demonstrated to be influenced by housing environment [ 98 , 210 , 212 ], there is still a lack of information on how the microbiota interacts with the host immune system. Nevertheless, the high plasticity of the avian microbiome offers a good basis to intentionally manipulate the microbiota by nutrition or housing condition to improve intestinal barrier function and host immunity [ 213 ].…”