Gut Microbial Ecology in Pigs—Impact on the Gut and Beyond

A special issue of Microorganisms (ISSN 2076-2607). This special issue belongs to the section "Gut Microbiota".

Deadline for manuscript submissions: closed (30 April 2022) | Viewed by 33080

Special Issue Editors


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Guest Editor
Department of Animal Science, Aarhus University, Blichers Allé 20, Postboks 50, DK-8830 Tjele, Demark
Interests: microbial ecosystem in the gastrointestinal tract of pigs; fermentation; feeding; animal physiology; animal nutrition

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Guest Editor
Department of Animal and Poultry Science, Saskatoon, University of Saskatchewan, Saskatchewan, SK, Canada
Interests: nutritional physiology and intestinal microbial ecology; functional foods and feeds; molecular microbial ecology; gnotobiology

Special Issue Information

Dear Colleagues,

Intensive research focusing on the composition of the pig gastrointestinal microbiota, its functionality, and the produced metabolites has indicated and demonstrated the great impact of the microbiome on animal health, welfare, performance and, more recently, behavior. At the same time, this research has highlighted the immense complexity of the interplay among members of the gut microbiota and the host and, as a consequence, the numerous known and unknown factors involved.

The aim of the present Special Issue is to provide the most recent knowledge regarding the pig gut microbial ecosystem. This will be attempted by covering aspects like: gut microbiome complexity (incl. bacteriome, mycobiome, and virome); the various pathways whereby the gut microbiome may impact the host gut and beyond; host-related factors versus external factors affecting the gut microbiome; strategies for host phenotype improvement via gut microbiome modulation; and methodological aspects of deciphering the host–gut microbiome interplay.

Dr. Nuria Canibe
Prof. Dr. Andrew Van Kessel
Guest Editors

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Keywords

  • health
  • microbiome
  • host behavior
  • host phenotype
  • methodology
  • pig

Published Papers (7 papers)

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Research

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15 pages, 1430 KiB  
Article
Relationships among Fecal, Air, Oral, and Tracheal Microbial Communities in Pigs in a Respiratory Infection Disease Model
by Robert Valeris-Chacin, Amanda Sponheim, Eduardo Fano, Richard Isaacson, Randall S. Singer, Joel Nerem, Fernando L. Leite and Maria Pieters
Microorganisms 2021, 9(2), 252; https://doi.org/10.3390/microorganisms9020252 - 27 Jan 2021
Cited by 9 | Viewed by 2905
Abstract
The association of the lower respiratory tract microbiome in pigs with that of other tissues and environment is still unclear. This study aimed to describe the microbiome of tracheal and oral fluids, air, and feces in the late stage of Mycoplasma hyopneumoniae infection [...] Read more.
The association of the lower respiratory tract microbiome in pigs with that of other tissues and environment is still unclear. This study aimed to describe the microbiome of tracheal and oral fluids, air, and feces in the late stage of Mycoplasma hyopneumoniae infection in pigs, and assess the association between the tracheal microbiome and those from air, feces, and oral fluids. Tracheal fluids (n = 73), feces (n = 71), oropharyngeal fluids (n = 8), and air (n = 12) were collected in seeder pigs (inoculated with M. hyopneumoniae) and contact pigs (113 days post exposure to seeder pigs). After DNA extraction, the V4 region from 16S rRNA gene was sequenced and reads were processed using Divisive Amplicon Denoising Algorithm (DADA2). Clostridium and Streptococcus were among the top five genera identified in all sample types. Mycoplasma hyopneumoniae in tracheal fluids was associated with a reduction of diversity and increment of M. hyorhinis, Glaesserella parasuis, and Pasteurella multocida in tracheal fluids, as well as a reduction of Ruminiclostridium, Barnesiella, and Lactobacillus in feces. Air contributed in a greater proportion to bacteria in the trachea compared with feces and oral fluids. In conclusion, evidence suggests the existence of complex interactions between bacterial communities from distant and distinct niches. Full article
(This article belongs to the Special Issue Gut Microbial Ecology in Pigs—Impact on the Gut and Beyond)
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20 pages, 2914 KiB  
Article
A Multi-Omics Protocol for Swine Feces to Elucidate Longitudinal Dynamics in Microbiome Structure and Function
by Laurin Christopher Gierse, Alexander Meene, Daniel Schultz, Theresa Schwaiger, Claudia Karte, Charlotte Schröder, Haitao Wang, Christine Wünsche, Karen Methling, Bernd Kreikemeyer, Stephan Fuchs, Jörg Bernhardt, Dörte Becher, Michael Lalk, KoInfekt Study Group, Tim Urich and Katharina Riedel
Microorganisms 2020, 8(12), 1887; https://doi.org/10.3390/microorganisms8121887 - 28 Nov 2020
Cited by 14 | Viewed by 3682
Abstract
Swine are regarded as promising biomedical models, but the dynamics of their gastrointestinal microbiome have been much less investigated than that of humans or mice. The aim of this study was to establish an integrated multi-omics protocol to investigate the fecal microbiome of [...] Read more.
Swine are regarded as promising biomedical models, but the dynamics of their gastrointestinal microbiome have been much less investigated than that of humans or mice. The aim of this study was to establish an integrated multi-omics protocol to investigate the fecal microbiome of healthy swine. To this end, a preparation and analysis protocol including integrated sample preparation for meta-omics analyses of deep-frozen feces was developed. Subsequent data integration linked microbiome composition with function, and metabolic activity with protein inventories, i.e., 16S rRNA data and expressed proteins, and identified proteins with corresponding metabolites. 16S rRNA gene amplicon and metaproteomics analyses revealed a fecal microbiome dominated by Prevotellaceae, Lactobacillaceae, Lachnospiraceae, Ruminococcaceae and Clostridiaceae. Similar microbiome compositions in feces and colon, but not ileum samples, were observed, showing that feces can serve as minimal-invasive proxy for porcine colon microbiomes. Longitudinal dynamics in composition, e.g., temporal decreased abundance of Lactobacillaceae and Streptococcaceae during the experiment, were not reflected in microbiome function. Instead, metaproteomics and metabolomics showed a rather stable functional state, as evident from short-chain fatty acids (SCFA) profiles and associated metaproteome functions, pointing towards functional redundancy among microbiome constituents. In conclusion, our pipeline generates congruent data from different omics approaches on the taxonomy and functionality of the intestinal microbiome of swine. Full article
(This article belongs to the Special Issue Gut Microbial Ecology in Pigs—Impact on the Gut and Beyond)
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20 pages, 3573 KiB  
Article
Discovery of Predictors of Mycoplasma hyopneumoniae Vaccine Response Efficiency in Pigs: 16S rRNA Gene Fecal Microbiota Analysis
by Peris M. Munyaka, Fany Blanc, Jordi Estellé, Gaëtan Lemonnier, Jean-Jacques Leplat, Marie-Noëlle Rossignol, Déborah Jardet, Graham Plastow, Yvon Billon, Benjamin P. Willing and Claire Rogel-Gaillard
Microorganisms 2020, 8(8), 1151; https://doi.org/10.3390/microorganisms8081151 - 29 Jul 2020
Cited by 10 | Viewed by 3072
Abstract
The gut microbiota comprises a large and diverse community of bacteria that play a significant role in swine health. Indeed, there is a tight association between the enteric immune system and the overall composition and richness of the microbiota, which is key in [...] Read more.
The gut microbiota comprises a large and diverse community of bacteria that play a significant role in swine health. Indeed, there is a tight association between the enteric immune system and the overall composition and richness of the microbiota, which is key in the induction, training and function of the host immunity, and may therefore, influence the immune response to vaccination. Using vaccination against Mycoplasma hyopneumoniae (M. hyo) as a model, we investigated the potential of early-life gut microbiota in predicting vaccine response and explored the post-vaccination dynamics of fecal microbiota at later time points. At 28 days of age (0 days post-vaccination; dpv), healthy piglets were vaccinated, and a booster vaccine was administered at 21 dpv. Blood samples were collected at 0, 21, 28, 35, and 118 dpv to measure M. hyo-specific IgG levels. Fecal samples for 16S rRNA gene amplicon sequencing were collected at 0, 21, 35, and 118 dpv. The results showed variability in antibody response among individual pigs, whilst pre-vaccination operational taxonomic units (OTUs) primarily belonging to Prevotella, [Prevotella], Anaerovibrio, and Sutterella appeared to best-predict vaccine response. Microbiota composition did not differ between the vaccinated and non-vaccinated pigs at post-vaccination time points, but the time effect was significant irrespective of the animals’ vaccination status. Our study provides insight into the role of pre-vaccination gut microbiota composition in vaccine response and emphasizes the importance of studies on full metagenomes and microbial metabolites aimed at deciphering the role of specific bacteria and bacterial genes in the modulation of vaccine response. Full article
(This article belongs to the Special Issue Gut Microbial Ecology in Pigs—Impact on the Gut and Beyond)
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16 pages, 3570 KiB  
Article
Temporal Dynamics of the Gut Bacteriome and Mycobiome in the Weanling Pig
by Ann M. Arfken, Juli Foster Frey and Katie Lynn Summers
Microorganisms 2020, 8(6), 868; https://doi.org/10.3390/microorganisms8060868 - 9 Jun 2020
Cited by 38 | Viewed by 3868
Abstract
Weaning is a period of environmental changes and stress that results in significant alterations to the piglet gut microbiome and is associated with a predisposition to disease, making potential interventions of interest to the swine industry. In other animals, interactions between the bacteriome [...] Read more.
Weaning is a period of environmental changes and stress that results in significant alterations to the piglet gut microbiome and is associated with a predisposition to disease, making potential interventions of interest to the swine industry. In other animals, interactions between the bacteriome and mycobiome can result in altered nutrient absorption and susceptibility to disease, but these interactions remain poorly understood in pigs. Recently, we assessed the colonization dynamics of fungi and bacteria in the gastrointestinal tract of piglets at a single time point post-weaning (day 35) and inferred interactions were found between fungal and bacterial members of the porcine gut ecosystem. In this study, we performed a longitudinal assessment of the fecal bacteriome and mycobiome of piglets from birth through the weaning transition. Piglet feces in this study showed a dramatic shift over time in the bacterial and fungal communities, as well as an increase in network connectivity between the two kingdoms. The piglet fecal bacteriome showed a relatively stable and predictable pattern of development from Bacteroidaceae to Prevotellaceae, as seen in other studies, while the mycobiome demonstrated a loss in diversity over time with a post-weaning population dominated by Saccharomycetaceae. The mycobiome demonstrated a more transient community that is likely driven by factors such as diet or environmental exposure rather than an organized pattern of colonization and succession evidenced by fecal sample taxonomic clustering with nursey feed samples post-weaning. Due to the potential tractability of the community, the mycobiome may be a viable candidate for potential microbial interventions that will alter piglet health and growth during the weaning transition. Full article
(This article belongs to the Special Issue Gut Microbial Ecology in Pigs—Impact on the Gut and Beyond)
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Review

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31 pages, 877 KiB  
Review
Impact of Intestinal Microbiota on Growth and Feed Efficiency in Pigs: A Review
by Gillian E. Gardiner, Barbara U. Metzler-Zebeli and Peadar G. Lawlor
Microorganisms 2020, 8(12), 1886; https://doi.org/10.3390/microorganisms8121886 - 28 Nov 2020
Cited by 65 | Viewed by 9092
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 [...] Read more.
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. Full article
(This article belongs to the Special Issue Gut Microbial Ecology in Pigs—Impact on the Gut and Beyond)
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23 pages, 984 KiB  
Review
Impact of Fermentable Protein, by Feeding High Protein Diets, on Microbial Composition, Microbial Catabolic Activity, Gut Health and beyond in Pigs
by Hanlu Zhang, Nikkie van der Wielen, Bart van der Hee, Junjun Wang, Wouter Hendriks and Myrthe Gilbert
Microorganisms 2020, 8(11), 1735; https://doi.org/10.3390/microorganisms8111735 - 5 Nov 2020
Cited by 36 | Viewed by 3438
Abstract
In pigs, high protein diets have been related to post-weaning diarrhoea, which may be due to the production of protein fermentation metabolites that were shown to have harmful effects on the intestinal epithelium in vitro. In this review, we discussed in vivo effects [...] Read more.
In pigs, high protein diets have been related to post-weaning diarrhoea, which may be due to the production of protein fermentation metabolites that were shown to have harmful effects on the intestinal epithelium in vitro. In this review, we discussed in vivo effects of protein fermentation on the microbial composition and their protein catabolic activity as well as gut and overall health. The reviewed studies applied different dietary protein levels, which was assumed to result in contrasting fermentable protein levels. A general shift to N-utilisation microbial community including potential pathogens was observed, although microbial richness and diversity were not altered in the majority of the studies. Increasing dietary protein levels resulted in higher protein catabolic activity as evidenced by increased concentration of several protein fermentation metabolites like biogenic amines in the digesta of pigs. Moreover, changes in intestinal morphology, permeability and pro-inflammatory cytokine concentrations were observed and diarrhoea incidence was increased. Nevertheless, higher body weight and average daily gain were observed upon increasing dietary protein level. In conclusion, increasing dietary protein resulted in higher proteolytic fermentation, altered microbial community and intestinal physiology. Supplementing diets with fermentable carbohydrates could be a promising strategy to counteract these effects and should be further investigated. Full article
(This article belongs to the Special Issue Gut Microbial Ecology in Pigs—Impact on the Gut and Beyond)
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22 pages, 912 KiB  
Review
Prevotella in Pigs: The Positive and Negative Associations with Production and Health
by Samat Amat, Hannah Lantz, Peris M. Munyaka and Benjamin P. Willing
Microorganisms 2020, 8(10), 1584; https://doi.org/10.3390/microorganisms8101584 - 14 Oct 2020
Cited by 63 | Viewed by 6095
Abstract
A diverse and dynamic microbial community (known as microbiota) resides within the pig gastrointestinal tract (GIT). The microbiota contributes to host health and performance by mediating nutrient metabolism, stimulating the immune system, and providing colonization resistance against pathogens. Manipulation of gut microbiota to [...] Read more.
A diverse and dynamic microbial community (known as microbiota) resides within the pig gastrointestinal tract (GIT). The microbiota contributes to host health and performance by mediating nutrient metabolism, stimulating the immune system, and providing colonization resistance against pathogens. Manipulation of gut microbiota to enhance growth performance and disease resilience in pigs has recently become an active area of research in an era defined by increasing scrutiny of antimicrobial use in swine production. In order to develop microbiota-targeted strategies, or to identify potential next-generation probiotic strains originating from the endogenous members of GIT microbiota in pigs, it is necessary to understand the role of key commensal members in host health. Many, though not all, correlative studies have associated members of the genus Prevotella with positive outcomes in pig production, including growth performance and immune response; therefore, a comprehensive review of the genus in the context of pig production is needed. In the present review, we summarize the current state of knowledge about the genus Prevotella in the intestinal microbial community of pigs, including relevant information from other animal species that provide mechanistic insights, and identify gaps in knowledge that must be addressed before development of Prevotella species as next-generation probiotics can be supported. Full article
(This article belongs to the Special Issue Gut Microbial Ecology in Pigs—Impact on the Gut and Beyond)
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