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Composition and Function of Chicken Gut Microbiota

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animals Review Composition and Function of Chicken Gut Microbiota Ivan Rychlik Department of Immunology, Veterinary Research Institute, 621 00 Brno, Czech Republic; [email protected]; Tel.: +420-533-331-201 Received: 8 December 2019; Accepted: 3 January 2020; Published: 8 January 2020 Simple Summary: Chickens evolved for millions of years to be hatched in a nest in contact with an adult hen. However, current commercial production of chickens is based on hatching chicks in a clean hatchery environment in the absence of adult hens. The ancestors of domestic chickens inhabited a living environment different from that used for current commercial production. Currently, the lifespan of broilers is around 5 weeks, the lifespan of egg layers is around one year while chickens can live for 15–20 years. This means that studies on chicken–microbiota interactions are of specific importance. The intestinal tract of commercially hatched chicks is gradually colonised from environmental sources only, however, if the chicks are provided experimentally with microbiota from a hen they can be colonised by adult-type microbiota from the very first days of life and become resistant to infections with pathogenic Escherichia coli, Clostridium perfringens, or Salmonella. Because of such specificities in the interactions of chickens with their gut microbiota, current knowledge in this area is critically presented in this review. Abstract: Studies analyzing the composition of gut microbiota are quite common at present, mainly due to the rapid development of DNA sequencing technologies within the last decade. This is valid also for chickens and their gut microbiota. However, chickens represent a specific model for host–microbiota interactions since contact between parents and offspring has been completely interrupted in domesticated chickens. Nearly all studies describe microbiota of chicks from hatcheries and these chickens are considered as references and controls. In reality, such chickens represent an extreme experimental group since control chicks should be, by nature, hatched in nests in contact with the parent hen. Not properly realising this fact and utilising only 16S rRNA sequencing results means that many conclusions are of questionable biological relevance. The specifics of chicken-related gut microbiota are therefore stressed in this review together with current knowledge of the biological role of selected microbiota members. These microbiota members are then evaluated for their intended use as a form of next-generation probiotics. Keywords: chicken; gut microbiota; caecum; ileum; faecal; development; Bacteroidetes; Firmicutes 1. Introduction Chickens represent one of the most widespread farm animals worldwide. Domestication of chickens started approximately 5000 years ago and since that time, chicken eggs and meat have become a common source of animal protein for humans. Before domestication, chickens, as any other species, were subjected to evolution and natural selection and the domestication of chickens introduced several changes to their natural behaviour. The ancestors of domestic chickens laid eggs in nests and warmed them by heat provided by the brooding parent. Incubated eggs were in intimate contact with the adult hen for 21 days of embryonic development and the same was true for newly hatched chicks—these were in contact with the adult hen from the very first moments of their life. The ancestors of domestic chickens also inhabited and were adapted to a living environment different from that used for current commercial production. Finally, the lifespan of meat types of chickens in commercial production is Animals 2020, 10, 103; doi:10.3390/ani10010103 www.mdpi.com/journal/animals Animals 2020, 10, x 2 of 21 life. The ancestors of domestic chickens also inhabited and were adapted to a living environment Animalsdifferent2020, 10from, 103 that used for current commercial production. Finally, the lifespan of meat types 2of of 20 chickens in commercial production is around 5 weeks while chickens reach sexual maturity around aroundweek 518 weeks of life. while The lifespan chickens of reachegg layers sexual in maturitycommercial around production week is 18 around of life. one The year lifespan while ofred egg jungle fowl can live for 15–20 years. These facts are commonly forgotten and ignored though correct layers in commercial production is around one year while red jungle fowl can live for 15–20 years. consideration of these facts has broad consequences for chicken welfare, resistance to enteric These facts are commonly forgotten and ignored though correct consideration of these facts has broad diseases and production. Serious consideration of these facts may also prevent trivial mistakes in consequences for chicken welfare, resistance to enteric diseases and production. Serious consideration experimental studies on chicken microbiota. The aim of this review was therefore to remind of these facts may also prevent trivial mistakes in experimental studies on chicken microbiota. The aim researchers of common facts related to the physiology of chicken intestinal tract which may ofinfluence this review microbiota was therefore composition to remind and researchers to summarise of common current facts knowledge related to on the the physiology composition of chicken and intestinalfunction tract of the which main may chicken influence gut microbiota microbiota members. composition and to summarise current knowledge on the composition and function of the main chicken gut microbiota members. 2. Composition of Gut Microbiota in Adult Chickens 2. Composition of Gut Microbiota in Adult Chickens Microbiota of young chickens is highly variable [1–3] and the microbiota of adult chickens, i.e., at Microbiotaleast 20 weeks of young of age, chickens has to isbe highly used for variable the definition [1–3] and of the core microbiota chicken ofgut adult microbiota chickens, [4–7]. i.e., at leastProximal 20 weeks parts of age,of the has digestive to be used tract for of theadult definition chickens of are core dominated chicken gutby microbiotaLactobacilli, [though4–7]. Proximal other partsspecies of the are digestive present as tract well of [8,9]. adult Microbiota chickens arecomp dominatedosition and by complexityLactobacilli considerably, though other increases species in are presentdistal asparts well of [ 8the,9]. intestinal Microbiota tract composition (caecum and and colon), complexity though considerablycolonic microbiota, increases due into distalphysiology parts of theof intestinal the chicken tract intestinal (caecum tract, and is colon), variable though and may colonic resemble microbiota, either ileal due or to caecal physiology microbiota of the (Figure chicken intestinal1). tract, is variable and may resemble either ileal or caecal microbiota (Figure1). FigureFigure 1. 1.Microbiota Microbiota composition composition alongalong thethe digestive tract tract of of 3 3 different different adult adult he hens.ns. Proximal Proximal parts parts of of thethe digestive digestive tract tract are are dominated dominated by byLactobacilli Lactobacilli.. Microbiota diversity diversity increases increases considerably considerably in inthe the caecum.caecum. Colonic Colonic microbiota microbiota can be a a mixture mixture of of caecal caecal and and ileal ileal microbiota, microbiota, depending depending on the on time the timeof ofsampling related related to to the the time time of ofvoiding voiding the thecaecal caecal content content into intocolon. colon. Hens Hens(a,b) were (a,b) sacrificed were sacrificed and andsampled sampled shortly shortly after after voiding voiding the caecal the caecal content content in the in colon the colonwhile whilehen (c) hen was ( csampled) was sampled a longer a time longer timeafter after voiding voiding of ofthe the caecal caecal content content into into the the colo colon,n, at atthe the time time when when the the caecal caecal microbiota microbiota was was “washed“washed out” out” and and replaced replaced with with digesta digesta originating originatin fromg from the the ileum. ileum. Data Data in thisin this figure figure originate originate from Videnskafrom Videnska et al. [8 ]et complemented al. [8] complemented with recent with recent laboratory laboratory results. results. 2.1.2.1. Crop Crop Microbiota Microbiota CropCrop microbiota microbiota of of adult adult hens hensis isdominated dominated byby Lactobacilli.. In In addition, addition, GallibacteriumGallibacterium (family(family Pasteurellaceae,Pasteurellaceae, phylum phylum Proteobacteria) Proteobacteria) isis characteristiccharacteristic of the the chicken chicken crop. crop. 2.2.2.2. Stomach Stomach Microbiota Microbiota BothBoth the the proventriculus proventriculus andand gizzard are are colonised colonised by by LactobacilliLactobacilli, likely, likely due due to their to their resistance resistance to toacidic acidic pH pH [8,9]. [8,9 ].Cyanobacteria Cyanobacteria or chloroplast or chloroplast DNA DNA can be can found be found in the instomach the stomach but it is but not itclear is not clearwhether whether this thisoriginates originates from from cyanobacteria cyanobacteria themselves themselves or whether or whether this DNA this is DNA of plant is of origin plant from origin from ingested feed, the latter hypothesis being more likely than the former. Although the stomach environment is quite hostile, it is also populated by as yet uncharacterised Proteobacteria species. Animals 2020, 10, 103 3 of 20 2.3. Small Intestine Microbiota Absolute counts
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