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Impact of Intestinal Microbiota on Growth and Feed Efficiency

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Impact of Intestinal Microbiota on Growth and Feed Efficiency microorganisms Review Impact of Intestinal Microbiota on Growth and Feed Efficiency in Pigs: A Review Gillian E. Gardiner 1,* , Barbara U. Metzler-Zebeli 2 and Peadar G. Lawlor 3 1 Department of Science, Waterford Institute of Technology, X91 K0EK Co. Waterford, Ireland 2 Unit Nutritional Physiology, Institute of Physiology, Pathophysiology and Biophysics, Department of Biomedical Sciences, University of Veterinary Medicine Vienna, 1210 Vienna, Austria; [email protected] 3 Teagasc, Pig Development Department, Animal and Grassland Research and Innovation Centre, Moorepark, Fermoy, P61 C996 Co. Cork, Ireland; [email protected] * Correspondence: [email protected]; Tel.: +353-51-302-626 Received: 2 October 2020; Accepted: 25 November 2020; Published: 28 November 2020 Abstract: This review summarises the evidence for a link between the porcine intestinal microbiota and growth and feed efficiency (FE), and suggests microbiota-targeted strategies to improve productivity. However, there are challenges in identifying reliable microbial predictors of host phenotype; environmental factors impact the microbe–host interplay, sequential differences along the intestine result in segment-specific FE- and growth-associated taxa/functionality, and it is often difficult to distinguish cause and effect. However, bacterial taxa involved in nutrient processing and energy harvest, and those with anti-inflammatory effects, are consistently linked with improved productivity. In particular, evidence is emerging for an association of Treponema and methanogens such as Methanobrevibacter in the small and large intestines and Lactobacillus in the large intestine with a leaner phenotype and/or improved FE. Bacterial carbohydrate and/or lipid metabolism pathways are also generally enriched in the large intestine of leaner pigs and/or those with better growth/FE. Possible microbial signalling routes linked to superior growth and FE include increased intestinal propionate production and reduced inflammatory response. In summary, the bacterial taxa and/or metabolic pathways identified here could be used as biomarkers for FE/growth in pigs, the taxa exploited as probiotics or the taxa/functionality manipulated via dietary/breeding strategies in order to improve productivity in pigs. Keywords: gut; microbiome; swine; intestine; productivity; trait; bacterial taxa; microbial metabolite signalling; mucosal immune response 1. Introduction The pig intestinal microbiota is undeniably of critical importance to its host, conferring numerous services, such as nutrient digestion, disease resistance and production of vitamins and beneficial metabolites [1]. Therefore, it is not unreasonable to suggest that the pig gut microbiome is likely to impact growth and feed efficiency (FE) in pigs. If this is the case, there is huge potential to manipulate the gut microbiome to improve pig growth and FE, which would have considerable economic and environmental benefits. This approach is also particularly timely, given current/impending restrictions on the use of in-feed antibiotics and therapeutic levels of zinc oxide, especially in Europe. Due to these economic, environmental and regulatory drivers, and also due to advances in DNA sequencing technologies, a number of studies have been published recently which investigate the link between the intestinal microbiota and growth, body composition and FE in pigs. Here, we will summarise only data from next-generation sequencing studies. However, even within these studies, it should Microorganisms 2020, 8, 1886; doi:10.3390/microorganisms8121886 www.mdpi.com/journal/microorganisms Microorganisms 2020, 8, x FOR PEER REVIEW 2 of 31 Microorganisms 2020, 8, 1886 2 of 31 these studies, it should be borne in mind that diverse methods can be employed for structural and/or functional analysis of the pig gut microbiota [2]. This review will: (1) Summarise the evidence for a belink borne between in mind the thatgut microbiome diverse methods and production can be employed traits, and for attempt structural to identify and/or functional common growth analysis- ofand the FE pig-associated gut microbiota bacterial [2 ].taxa This and review functional will: pathways (1) Summarise; (2) outline the evidence possible mechanisms for a link between by which the gutthemicrobiome gut microbiome and production might impact traits, growth and attempt and FE to; identify(3) suggest common ways growth-in which and the FE-associated knowledge bacterialaccumulated taxa andto date functional can be pathways;used to inform (2) outline strategies possible to manipulate mechanisms the bygut which microbiome the gut to microbiome improve mightgrowth impact and FE growth for commercial and FE; (3) suggestpig producers ways in; and which (4)the outline knowledge challenges accumulated associated to with date canthese be usedstrategies to inform. In order strategies to gain to manipulatean insight in theto gutthe microbiomemicrobiota composition to improve growthalong the and diverse FE for commercialsections of pigthe producers; porcine gastrointestinal and (4) outline tract challenges (GIT), readers associated are referred with these to recent strategies. reviews/studies In order to in gain this an area insight [1– into4]. the microbiota composition along the diverse sections of the porcine gastrointestinal tract (GIT), readers are referred to recent reviews/studies in this area [1–4]. 2. Evidence for a Link between the Pig Intestinal Microbiota and Pig Growth, Body Weight and 2.Body Evidence Composition for a Link between the Pig Intestinal Microbiota and Pig Growth, Body Weight and Body Composition Evidence of the link between the intestinal microbiota and pig growth and body composition traitsEvidence is mainly of thederived link betweenfrom studies the intestinal comparing microbiota microbiota and diversity pig growth and and composition body composition in pigs traitsranked is mainly as extreme derived based from on studies these comparing production microbiota parameters. diversity We have and compositionsummarised infindings pigs ranked for asbacterial extreme diversity based on theseand differentially production parameters. abundant taxa We have from summarised two studies findings in which for bacterialthese data diversity were andavailable differentially (Table 1). abundant Data on taxa correlations from two of studies taxa with in which growth these and data body were composition available (Tabletraits from1). Data other on correlationsstudies are summarised of taxa with growthin the text. and Figure body composition1 also summarises traits fromsome othercommon studies findings. are summarised Although all in theare text. sequence Figure-based,1 also readers summarises should some be mindful common that findings. the studies Although summaris all areed sequence-based, here have used a readers range shouldof methods be mindful for structural that the and/or studies functional summarised analysis here of the have microbiota used a range, and these of methods methodologies for structural have andbeen/or detailed functional in Table analysis 1 and/or of the in microbiota, the text. Due and to thesethe enormity methodologies of the available have been data, detailed the focus in Tablein this1 andreview/or in will the text.mainly Due be to on the common enormity findings of the available across studies data, the, as focus it is inbeyond this review the scope will mainly of a single be on commonreview paper findings to discuss across all studies, pig growth as it is-associated beyond the taxa scope. of a single review paper to discuss all pig growth-associated taxa. FigureFigure 1. 1.Summary Summary of of feed feed effi efficiencyciency-associated-associated bacterial bacterial taxa taxa in pigs.in pigs. There There are are some some conflicting conflicting data fordata the for taxa the in taxa blue, in and blue the, and taxa the in taxa bold in are bold also are associated also associated with increased with increased body weight body and weight/or leanness. and/or leanness. Microorganisms 2020, 8, 1886 3 of 31 Table 1. Bacterial diversity within the gut microbiome of pigs ranked on growth/body composition traits and bacterial genera/species and related pathways/genes 1 linked with growth and body composition. Genera/Species More Genera/Species Less Functional Analysis ( = Bacterial Trait (Methodology Sample Type α- and β-Diversity Abundant in Animals Abundant in Animals Pathways Less Abundant# in Animals for Structural and (Total Number Age of Pigs Effects in Animals with with Better Production with Better Production with Better Production Traits; = Ref Functional Analysis of Pigs) Better Production Traits Traits, i.e., Heavier, Traits, i.e., Heavier, Pathways More Abundant in Animals" of Gut Microbiome) Lower Back Fat (Leaner) Lower Back Fat (Leaner) with Better Production Traits) 1 Lactococcus dioxin, xylene, benzoate degradation Higher α-diversity (ACE, " Body weight (16S Anaerotruncus Nucleotide-binding Chao1, and observed # rRNA gene Anaerococcus Eubacterium oligomerization domain-like receptor Faeces OTU indices) for heavier sequencing (V4) on Day 63 of age Sediminibacterium Bilophila (NLR) signalling [5] (n = 18) pigs. β-diversity effects at Illumina MiSeq + Butyrivibrio Bacteroides Alanine, aspartate, phylum but not # PICRUSt predictions) Prevotella glutamate metabolism genus level Corynebacterium Novobiocin biosynthesis # DNA repair and recombination " Pyrimidine metabolism " Secretion system Actinobacillus succinogenes " Lysozyme and chitinase degradation
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