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]. 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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