Enteric microbiome ecosystem regulation of poultry gut health
Understanding a ‘healthy gut’ requires knowledge of the functional interactions of all components of the enteric microbiome ecosystem. These interactions between these diverse physiological features underscore the extent of areas encompassed by the gut and the difficulty in correlating elements of gut health with the ability to regulate poultry performance.
Gut health of production animals, including poultry, is dependent upon the interactions within the intestinal microbiome ecosystem that is made up of a diverse population of microbes within a dynamic host environment. A healthy gut is dependent upon the homeostatic interactions within the microbiome that directly influences the ability of the animal to perform its physiological functions for growth and production and reach as close as possible to 100% of its genetic potential. However, for years, research as concentrated on the microbiota’s role in maintaining of a healthy gut. However, recent findings have demonstrated that the host exerts control over the microbiota through multiple mechanisms which enable the host to shape the ecology of the microbiome and to establish a selection for microbial traits that are beneficial to the host.
Microbiota
The microbial community in the chicken gut is a multilayered, dynamic ecosystem with a homeostatic state and a certain capacity of structural resilience, although species composition and metabolic functions can be readily altered by host and environmental-dependent events. The commensal microbiota consists of trillions of microorganisms, predominately bacteria, with greater than 500 phylotypes or approximately 1 million bacteria genes, that have a fundamental symbiotic functional association with the host and, thus; are strategic managers of host physiology involved in regulating bird health. Collectively, the microbiota can be considered a ‘functional organ’ within the gut involved in assimilation of nutrients from feed, particularly through the release of energy from dietary fibre and directing a metabolome that affects energy balance and body weight. More specifically, the gut microbiota tacitly serves as a neuroendocrine organ because of its metabolic abilities to produce and regulate multiple metabolites that reach the circulation and influence the functional activities of distal organs and systems. These multidirectional axes communicate with the distal organs using neural, endocrine, immunological and metabolic signalling. Lastly, a major function of the gut microbiota is protection against pathogen colonisation and overgrowth of indigenous pathobionts by a process called colonisation resistance. The microbiota can activate a diverse number of metabolic pathways that inhibit pathogen colonisation indirectly via activation of protective immune responses and directly by occupying nutrient niches and production of metabolic products that limit pathogen colonisation and expansion.
Host
The host is under selective pressure to maintain a beneficial microbiota population throughout the intestine. To do so, the host can impose several ecological ‘filters’ that can shape the composition of the microbiota community throughout the gut. These filters include the gut epithelial cells, the enteric immune system, and the enteric nervous system.
Epithelial cells
Epithelial cells (IECs) at mucosal sites act as a protective physical barrier filter against the external environment. In the intestine, epithelial cells selectively allow nutrient absorption while they are in constant contact with diverse external environmental stimuli, including dietary cues, climate changes, and/or commensal and pathogenic microorganisms. Therefore, the functions of IECs at these tissue sites are critical. In addition to promoting barrier functions, the IECs senses the microbial environment via pattern recognition receptors and receptors sensing metabolites. Intestinal epithelial cells stimulated by gut environmental factors (microbiota and their metabolites) interact with host immune cells and modulate gut immune cell responses.
Most IECs can be broadly characterised as absorptive, having the capacity to absorb luminal contents, or secretory, releasing cytokines, chemokines, antimicrobial peptides, and other molecules specific to their functions. The majority of the IECs are enterocytes, which control water and nutrient absorption. Highly secretory IECs, such as goblet and Paneth cells, produce mucins and antimicrobials and thereby control the composition and compartmentalisation of the gut microbiome, respectively. Other IEC subsets include enteroendocrine cells, a heterogenous cell population that secretes hormones, neuropeptides, and neurotransmitters and are known to interact with gut-innervating neurons. These IEC subsets maintain barrier homeostasis by integrating signals from the external environment as well as signals from other cell types, including immune cells and neurons that underlie the epithelial layer. Epithelial cells possess an array of pattern recognition receptors that can detect pathogen- or danger-associated molecular patterns. IECs modulate and train immune responses in response to stimuli derived from the gut microbiome, which subsequently shapes the immune system.
All these interactions (dietary cues, microbes and metabolites, immune crosstalk, endocrine signals, and neuronal networks), control and regulate the execution of intestinal epithelial metabolism which shapes the gut microbiota. The metabolic processes in IECs shape the gut microbiome by creating a beneficial habitat for distinct beneficial microbe species that favour the host physiology. Specifically, in the small intestine, Paneth cell production of antimicrobial peptides shape the microbiota composition and size to reduce competition with the host for dietary nutrients. In the large intestine, IECs shape the microbiota spatial organisation and composition by using oxygen-consuming processes (oxidative phosphorylation in mitochondria). The expenditure of oxygen results in a hypoxic environment, creating an oxygen gradient from the basolateral to luminal sites. The lack of luminal oxygen protects against the introduction of facultative anaerobic pathogens into the resident microbiota and promotes the expansion of anaerobic species, which ferment fibre into SCFAs (used by the gut epithelium as an energy source).
Immune system
The immune responses that provide protection from pathogens in distal tissues is quite different from those response that affect microbial communities in the gut. At the mucosal surfaces, the immune responses affect the microbiota by selecting for beneficial attributes that encourage microbial growth and survival which results in a non-specific immune function known as colonisation resistance. For years, most of the studies have demonstrated the role of the microbiota on the training and functional tuning of the immune system by detection microbial metabolites via host cell innate immune receptors. However, emerging evidence makes a compelling case that the immune system is also an ecological ‘filter’ that has an influential effect on the composition and stability of the microbiota.
The interactive relationship between gut microbiota and the host immune system is complex and not fully understood in the chicken. The gut immune system orchestrates the localisation, diversity and homeostasis of gut microbiota, while the gut microbiota provides signals for the immune system to promote the development, differentiation and regulation of immune responses. They have co-evolved with a symbiotic relationship to maintain physiological homeostasis by the ability of the enteric immune system to establish immune tolerance towards a constantly changing number of harmless microbes while concurrently preserving immune responses against pathogenic infection. During homeostasis, the host’s immune response to the intestinal microbiota is strictly compartmentalised to the mucosal surface.
Both the innate and adaptive immune system contribute in the promoting of the growth of beneficial members of the microbial community and help to maintain a stable microbial community. The innate immune system recognises and modulates the composition of the microbiota through its ability to recognise molecular patterns and exert immunological responses through pattern recognition receptors. The adaptive immune system also plays a pivotal role in regulating microbiota composition. Specifically, B cells are a key factor in maintaining intestinal homeostasis through their secretion of IgA. T cells also contribute to homeostatic regulation by providing various B cell stimulation signals under different local microenvironments. As a result, T cells and B cells simultaneously regulate intestinal flora to maintain intestinal homeostasis. Further, the co-adaptation between gut microbial populations and their metabolites and cells of the immune system is of fundamental importance in maintaining a healthy gut. In particular, the gut microbial metabolites (SCFAs, secondary bile salts, indole) play a vital part in regulating gut immunity and modulating the immune system, both locally and systemically.
Enteric nervous system
The intestinal tract is densely innervated which cooperates with intestinal microbiota, the intestinal immune system, and endocrine systems to form a complex network that is required to maintain a stable intestinal microenvironment. The enteric nervous system (ENS) is the intrinsic nervous system of the gastrointestinal tract (GI) and regulates important GI functions, including motility, nutrient uptake, and immune response. Increasing recognition that the intestinal microbiota and ENS interact during critical periods. The ENS interacts intimately with the intestinal epithelial barrier and surrounding immune cells, which regulate homeostasis of the GI tract. Changes in the local enteric are indirectly passed from the epithelial and immune cells of the gut (via hormones and neuroactive molecules) onto cells of the ENS, where they are translated into neural impulses that signal throughout the local tissue and systemically via the central nervous system. The microbiota appear to be essential for maintaining the integrity of the enteric nervous system by regulating enteric neuronal survival and promoting neurogenesis via the release of microbial MAMPS and production of metabolites, especially SCFAs.
Perspective
Optimal gut health is of vital importance to the performance of poultry to be able to perform to their genetic potential. Understanding a ‘healthy gut’ requires knowledge of the functional interactions of both internal components of the enteric ecosystem: the host and the microbiota. The connections between these diverse physiological features of the enteric ecosystem underscore the extent of areas encompassed by the gut and the difficulty in correlating specific components of gut health with the ability to regulate poultry performance. The increase in worldwide non-AGP poultry production is challenging the industry in management, health, and animal welfare. Therefore, there has been a major focus on the development of alternatives to antibiotics that have concentrated on those directed towards the microbiota especially including pre-, pro-, and postbiotics. However since, the host is under selective pressure to ensure that the microbiota becomes and remains beneficial, there is now an increased focus on how the host can be manipulated to exert ecological control over their microbiota and the development of novel antibiotic alternatives that can be directed towards modulating immunity, barrier function, the gut-brain axis, and intestinal epithelial functional metabolism.
