Microbiological diversity, formation, ecological role and research methods of the pig gut microbiota: a review



Cite item

Full Text

Abstract

В работе представлены данные исследований кишечной микробиоты свиней, играющей ключевую роль в поддержании здоровья и физиологии животных.

Целью данного обзора является обобщение экспериментальных данных, полученных разными группами исследователей о влиянии таких параметров как возраст, тип диеты и использование антибиотиков на состав и функциональную активность кишечной микробиоты свиней и их вклад в распространение генов антибиотикорезистентности (АРГ) в условиях животноводства. Особое внимание уделено формированию и динамике состава микробиоты поросят в неонатальном периоде. Рассмотрено влияние различных типов диеты на состав и функциональную активность кишечной микробиоты свиней, в том числе на экспрессию генов гликозидгидролаз и гликозилтрансфераз и возможности модулирования состава микробиоты посредством диеты, что может минимизировать последствия стресса при отъеме и повысить продуктивность животных. Особое внимание уделено роли кишечной микробиоты в метаболизме аминокислот, витаминов, липидов и желчных кислот, а также функциональной метагеномике микробного сообщества, позволяющей выявлять гены, связанные с адаптацией к различным типам рациона и патологическим состояниям.

This review presents data on studies of the intestinal microbiota of pigs, which plays a key role in the maintenance of animal health and physiology. The aim of this review is to describe the effects of age, diet and antibiotics on the composition and functional activity of the intestinal microbiota of pigs and the distribution of antibiotic resistance genes (ARGs) under livestock production conditions. This review summarises research data on the composition of the intestinal microbiota of pigs, with special attention paid to the formation and dynamics of the composition of the microbiota of piglets in the neonatal period. The influence of different types of diet on the composition and functional activity of the intestinal microbiota of pigs, including the expression of glycosidohydrolase and glycosyltransferase genes and the possibility of modulating the composition of the microbiota through diet, which can minimise the effects of stress at weaning and increase animal performance. Particular attention is given to the role of the gut microbiota in the metabolism of amino acids, vitamins, lipids and bile acids, and to the functional metagenomics of the microbial community, allowing the identification of genes associated with adaptation to different diet types and pathological conditions. The review also discusses the role of pigs in the spread of ARGs, including using metagenomic and metatranscriptomic profiling, as well as the risks associated with their introduction into the environment and the potential impact on animal and human health.

Full Text

Restricted Access

About the authors

Darya A Sedova

Don State Technical University;
Southern Federal University

Author for correspondence.
Email: dased0va@yandex.ru
ORCID iD: 0000-0003-1194-7251
SPIN-code: 6197-7220

Researcher of " MedCifra" Research Laboratory Faculty of Bioengineering and Veterinary Medicine DSTU

Postgraduate student of the Department of Ecology and Environmental Management, Academy of Biology and Biotechnology SFU

Russian Federation, 1 Gagarin Square, Rostov-on-Don, Russia, 344000; 105/42 B. Sadovaya st., Rostov-on-Don, Russia, 344006

Sergey N Golovin

Don State Technical University

Email: labbiobez@yandex.ru
ORCID iD: 0000-0002-1929-6345
SPIN-code: 5345-4005

Researcher of " MedCifra" Research Laboratory Faculty of Bioengineering and Veterinary Medicine DSTU

Russian Federation, 1 Gagarin Square, Rostov-on-Don, Russia, 344000

Sergey K Shebeko

Don State Technical University

Email: shebeko_sk@mail.ru
ORCID iD: 0000-0001-9350-7588
SPIN-code: 7913-5266

Cand. Sci. (Pharmacology), Professor, Faculty of Bioengineering and Veterinary Medicine DSTU 

Russian Federation, 1 Gagarin Square, Rostov-on-Don, Russia, 344000

Aleksey M Ermakov

Don State Technical University

Email: labbiobez@yandex.ru
ORCID iD: 0000-0002-9834-3989
SPIN-code: 5358-3424

Cand. Sci. (Biology), Professor, Dean of the Faculty of Bioengineering and Veterinary Medicine DSTU 

Russian Federation, 1 Gagarin Square, Rostov-on-Don, Russia, 344000

References

  1. Wang C, Li P, Yan Q, et al. Characterization of the pig gut microbiome and antibiotic resistome in industrialized feedlots in China. mSystems. 2019;4(6):e00206-19. doi: 10.1128/msystems.00206-19
  2. Yang J, Chen R, Peng Y, Chai J, Li Y, Deng F. The role of gut archaea in the pig gut microbiome: a mini-review. Front Microbiol. 2023;14:1284603. doi: 10.3389/fmicb.2023.1284603
  3. Rowan JP, Durrance KL, Combs GE, Fisher LZ. The digestive tract of the pig. Gainesville: Animal Science Department, Florida Cooperative Extension Service, Institute of Food and Agricultural Sciences, University of Florida; 1997.
  4. Thomson JR, Friendship RM. Digestive system. In: Zimmerman JJ, Karriker LA, Ramirez A, Schwartz KJ, Stevenson GW, Zhang J, editors. Diseases of Swine. 11th ed. USA: John Wiley & Sons; 2019. P:234-263.
  5. Isaacson R, Kim HB. The intestinal microbiome of the pig. Anim Health Res Rev. 2012;13(1):100-109. doi: 10.1017/S1466252312000084
  6. Holman DB, Kommadath A, Tingley JP, Abbott DW. Novel Insights into the Pig Gut Microbiome Using Metagenome-Assembled Genomes. Microbiol Spectr. 2022;10(4):e0238022. doi: 10.1128/spectrum.02380-22
  7. Kennedy NA, Walker AW, Berry SH, et al. The impact of different DNA extraction kits and laboratories upon the assessment of human gut microbiota composition by 16S rRNA gene sequencing. PLoS One. 2014;9(2):e88982. doi: 10.1371/journal.pone.0088982
  8. Chen C, Zhou Y, Fu H, et al. Expanded catalog of microbial genes and metagenome-assembled genomes from the pig gut microbiome. Nat Commun. 2021;12(1):1106. doi: 10.1038/s41467-021-21295-0
  9. Fernandez M, Thompson J, Calle A. Novel feed additive delivers antimicrobial copper and influences fecal microbiota in pigs. Microbiol Spectr. 2024;12(6):e0428023. doi: 10.1128/spectrum.04280-23
  10. Chen X, Xu J, Ren E, Su Y, Zhu W. Co-occurrence of early gut colonization in neonatal piglets with microbiota in the maternal and surrounding delivery environments. Anaerobe. 2018;49:30-40. doi: 10.1016/j.anaerobe.2017.12.002
  11. Quan J, Xu C, Ruan D, et al. Composition, function, and timing: exploring the early-life gut microbiota in piglets for probiotic interventions. J Anim Sci Biotechnol. 2023;14(1):143. Published 2023 Nov 13. doi: 10.1186/s40104-023-00943-z
  12. Bian G, Ma S, Zhu Z, et al. Age, introduction of solid feed and weaning are more important determinants of gut bacterial succession in piglets than breed and nursing mother as revealed by a reciprocal cross-fostering model. Environ Microbiol. 2016;18(5):1566-1577. doi: 10.1111/1462-2920.13272
  13. Konstantinov SR, Awati AA, Williams BA, et al. Post-natal development of the porcine microbiota composition and activities. Environ Microbiol. 2006;8(7):1191-1199. doi: 10.1111/j.1462-2920.2006.01009.x
  14. Choudhury R, Middelkoop A, de Souza JG, et al. Impact of early-life feeding on local intestinal microbiota and digestive system development in piglets. Sci Rep. 2021;11(1):4213. doi: 10.1038/s41598-021-83756-2
  15. Fulde M, Sommer F, Chassaing B, et al. Neonatal selection by Toll-like receptor 5 influences long-term gut microbiota composition. Nature. 2018;560(7719):489-493. doi: 10.1038/s41586-018-0395-5
  16. Kurkjian HM, Akbari MJ, Momeni B. The impact of interactions on invasion and colonization resistance in microbial communities. PLoS Comput Biol. 2021;17(1):e1008643. doi: 10.1371/journal.pcbi.1008643
  17. Newberry RC., Wood-Gush DG. (1985). The suckling behaviour of domestic pigs in a semi-natural environment. Behaviour. 1985;95(1-2):11-25. doi: 10.1163/156853985X00028
  18. Knecht D, Cholewińska P, Jankowska-Mąkosa A, Czyż K. Development of Swine's Digestive Tract Microbiota and Its Relation to Production Indices-A Review. Animals (Basel). 2020;10(3):527. doi: 10.3390/ani10030527
  19. Rhouma M, Fairbrother JM, Beaudry F, Letellier A. Post weaning diarrhea in pigs: risk factors and non-colistin-based control strategies. Acta Vet Scand. 2017;59(1):31. doi: 10.1186/s13028-017-0299-7
  20. Varel VH, Yen JT. Microbial perspective on fiber utilization by swine. J Anim Sci. 1997;75(10):2715-2722. doi: 10.2527/1997.75102715x
  21. Xiong X, Tan B, Song M, et al. Nutritional Intervention for the Intestinal Development and Health of Weaned Pigs. Front Vet Sci. 2019;6:46. doi: 10.3389/fvets.2019.00046
  22. Kuller WI, Soede NM, van Beers-Schreurs HM, et al. Effects of intermittent suckling and creep feed intake on pig performance from birth to slaughter. J Anim Sci. 2007;85(5):1295-1301. doi: 10.2527/jas.2006-177
  23. Xiao L, Estellé J, Kiilerich P, et al. A reference gene catalogue of the pig gut microbiome. Nat Microbiol. 2016;1:16161. doi: 10.1038/nmicrobiol.2016.161
  24. Rahman R, Fouhse JM, Ju T, et al. A comparison of wild boar and domestic pig microbiota does not reveal a loss of microbial species but an increase in alpha diversity and opportunistic genera in domestic pigs. Microbiol Spectr. 2024;12(10):e0084324. doi: 10.1128/spectrum.00843-24
  25. Quan J, Cai G, Ye J, et al. A global comparison of the microbiome compositions of three gut locations in commercial pigs with extreme feed conversion ratios. Sci Rep. 2018;8(1):4536. doi: 10.1038/s41598-018-22692-0
  26. Gryaznova MV, Dvoretskaya YD, Syromyatnikov MY, et al. Changes in the Microbiome Profile in Different Parts of the Intestine in Piglets with Diarrhea. Animals. 2022; 12(3):320. doi: 10.3390/ani12030320
  27. Korchagina AY, Bryndina LV. Determination of the species diversity of theintestinal microbiome pigs in order to create a consortium of microorganisms for wastewater treatment from organic pollutants. Proceedings of the Russian science conference «Zdorov''esberegajushhie tehnologii, kachestvo i bezopasnost'' pishhevoj produkcii; 2021 Nov 19; Saratov. P. 179-184. (In Russ)
  28. Gryaznova M, Smirnova Y, Burakova I, Morozova P, Nesterova E, Gladkikh M, Mikhaylov E, Syromyatnikov M. Characteristics of the Fecal Microbiome of Piglets with Diarrhea Identified Using Shotgun Metagenomics Sequencing. Animals. 2023; 13(14):2303. doi: 10.3390/ani13142303
  29. Syromyatnikov MY, Shabunin SV, Nesterova EY, et al. Abundance of bacterial antibiotic resistance genes in swine during the fattening period (Sus scrofa domesticus). Educational Establishment "Vitebsk State Academy of Veterinary Medicine". 2023;59(4):85-89. (in Russ.) doi: 10.52368/2078-0109-2023-59-4-96-101
  30. Lysenko YA, Koshaev AG, Belyak VA, et al. Analysis, isolation and identification of the microbiome from the ceca of the intestines of industrial pigs. Izvestiya of Timiryazev Agricultural Academy. 2024;(4):168-183. doi: 10.26897/0021-342X-2024-4-168-183
  31. Dumont MG, Pommerenke B, Casper P. Using stable isotope probing to obtain a targeted metatranscriptome of aerobic methanotrophs in lake sediment. Environ Microbiol Rep. 2013;5(5):757-764. doi: 10.1111/1758-2229.12078
  32. Xu J, Xu R, Jia M, Su Y, Zhu W. Metatranscriptomic analysis of colonic microbiota's functional response to different dietary fibers in growing pigs. Anim Microbiome. 2021;3(1):45. doi: 10.1186/s42523-021-00108-1
  33. Gosalbes MJ, Durbán A, Pignatelli M, et al. Metatranscriptomic approach to analyze the functional human gut microbiota. PLoS One. 2011;6(3):e17447. doi: 10.1371/journal.pone.0017447
  34. Shan T, Li L, Simmonds P, Wang C, Moeser A, Delwart E. The fecal virome of pigs on a high-density farm. J Virol. 2011;85(22):11697-11708. doi: 10.1128/JVI.05217-11
  35. Urubschurov V, Janczyk P, Souffrant WB, Freyer G, Zeyner A. Establishment of intestinal microbiota with focus on yeasts of unweaned and weaned piglets kept under different farm conditions. FEMS Microbiol Ecol. 2011;77(3):493-502. doi: 10.1111/j.1574-6941.2011.01129.x
  36. Chen Q, Lyu W, Pan C, et al. Tracking investigation of archaeal composition and methanogenesis function from parental to offspring pigs. Sci Total Environ. 2024;927:172078. doi: 10.1016/j.scitotenv.2024.172078
  37. Meene A, Gierse L, Schwaiger T, et al. Archaeome structure and function of the intestinal tract in healthy and H1N1 infected swine. Front Microbiol. 2023;14:1250140. doi: 10.3389/fmicb.2023.1250140
  38. Crespo-Piazuelo D, Estellé J, Revilla M, et al. Characterization of bacterial microbiota compositions along the intestinal tract in pigs and their interactions and functions. Sci Rep. 2018;8(1):12727. doi: 10.1038/s41598-018-30932-6
  39. Lamendella R, Domingo JW, Ghosh S, Martinson J, Oerther DB. Comparative fecal metagenomics unveils unique functional capacity of the swine gut. BMC Microbiol. 2011;11:103. doi: 10.1186/1471-2180-11-103
  40. Velayudhan DE, Kim IH, Nyachoti CM. Characterization of dietary energy in Swine feed and feed ingredients: a review of recent research results. Asian-Australas J Anim Sci. 2015;28(1):1-13. doi: 10.5713/ajas.14.0001R
  41. Tiwari UP, Singh AK, Jha R. Fermentation characteristics of resistant starch, arabinoxylan, and β-glucan and their effects on the gut microbial ecology of pigs: A review. Anim Nutr. 2019;5(3):217-226. doi: 10.1016/j.aninu.2019.04.003
  42. Li H, Han L, Zhou F, et al. Ningxiang Pig-Derived Microbiota Affects the Growth Performance, Gut Microbiota, and Serum Metabolome of Nursery Pigs. Animals (Basel). 2024;14(17):2450. doi: 10.3390/ani14172450
  43. Pandey S, Kim ES, Cho JH, et al. Swine gut microbiome associated with non-digestible carbohydrate utilization. Front Vet Sci. 2023;10:1231072. doi: 10.3389/fvets.2023.1231072
  44. Tang X, Zhang L, Wang L, et al. Multi-Omics Analysis Reveals Dietary Fiber's Impact on Growth, Slaughter Performance, and Gut Microbiome in Durco × Bamei Crossbred Pig. Microorganisms. 2024;12(8):1674. doi: 10.3390/microorganisms12081674
  45. Zhang L, Yue Y, Shi M, et al. Dietary Luffa cylindrica (L.) Roem promotes branched-chain amino acid catabolism in the circulation system via gut microbiota in diet-induced obese mice. Food Chem. 2020;320:126648. doi: 10.1016/j.foodchem.2020.126648
  46. Zhang J, Jiang Q, Du Z, et al. Knowledge graph-derived feed efficiency analysis via pig gut microbiota. Sci Rep. 2024;14(1):13939. doi: 10.1038/s41598-024-64835-6
  47. Pieper R, Kröger S, Richter JF, et al. Fermentable fiber ameliorates fermentable protein-induced changes in microbial ecology, but not the mucosal response, in the colon of piglets. J Nutr. 2012;142(4):661-667. doi: 10.3945/jn.111.156190
  48. Liu G, Gu K, Liu X, et al. Dietary glutamate enhances intestinal immunity by modulating microbiota and Th17/Treg balance-related immune signaling in piglets after lipopolysaccharide challenge. Food Res Int. 2023;166:112597. doi: 10.1016/j.foodres.2023.112597
  49. Yang Q, Huang X, Zhao S, et al. Structure and Function of the Fecal Microbiota in Diarrheic Neonatal Piglets. Front Microbiol. 2017;8:502. doi: 10.3389/fmicb.2017.00502
  50. Liao SF, Ji F, Fan P, Denryter K. Swine Gastrointestinal Microbiota and the Effects of Dietary Amino Acids on Its Composition and Metabolism. Int J Mol Sci. 2024;25(2):1237. doi: 10.3390/ijms25021237
  51. Gryaznova MV, Smirnova YD, Burakova IY, et al. Analysis of the genes of enzymes of metabolic pathways in the intestines of the newborn piglets with diarrhea. Bulletin Of Veterinary Pharmacology. 2023;4:163-174. (in Russ.) doi: 10.17238/issn2541-8203.2023.4.163
  52. Yang H, Huang X, Fang S, et al. Uncovering the composition of microbial community structure and metagenomics among three gut locations in pigs with distinct fatness. Sci Rep. 2016;6:27427. doi: 10.1038/srep27427
  53. Thacker, P.A. Alternatives to antibiotics as growth promoters for use in swine production: A review. J. Anim. Sci. Biotechnol. 2013, 4, 35.
  54. Li, J. Current status and prospects for in-feed antibiotics in the different stages of pork production—A review. Asian Australas. J. Anim. Sci. 2017, 30, 1667–1673.
  55. Lekagul A, Tangcharoensathien V, Yeung S. Patterns of antibiotic use in global pig production: A systematic review. Vet Anim Sci. 2019;7:100058. doi: 10.1016/j.vas.2019.100058
  56. Munk P, Yang D, Röder T, et al. The European livestock resistome. mSystems. 2024;9(4):e0132823. doi: 10.1128/msystems.01328-23
  57. Forcina G, Pérez-Pardal L, Carvalheira J, Beja-Pereira A. Gut Microbiome Studies in Livestock: Achievements, Challenges, and Perspectives. Animals (Basel). 2022;12(23):3375. doi: 10.3390/ani12233375
  58. Keum GB, Kim ES, Cho J, et al. Analysis of antibiotic resistance genes in pig feces during the weaning transition using whole metagenome shotgun sequencing. J Anim Sci Technol. 2023;65(1):175-182. doi: 10.5187/jast.2022.e103
  59. Wang Y, Hu Y, Liu F, et al. Integrated metagenomic and metatranscriptomic profiling reveals differentially expressed resistomes in human, chicken, and pig gut microbiomes. Environ Int. 2020;138:105649. doi: 10.1016/j.envint.2020.105649
  60. Wang C, Dong D, Strong PJ, et al. Microbial phylogeny determines transcriptional response of resistome to dynamic composting processes. Microbiome. 2017;5(1):103. doi: 10.1186/s40168-017-0324-0
  61. Neher TP, Soupir ML, Andersen DS, O’Neill ML, Howe A. Comparison of antibiotic resistance genes in swine manure storage pits of Iowa, USA. Frontiers in Antibiotics. 2023;2:1116785. doi: 10.3389/frabi.2023.1116785
  62. Michaelis C, Grohmann E. Horizontal Gene Transfer of Antibiotic Resistance Genes in Biofilms. Antibiotics (Basel). 2023;12(2):328. doi: 10.3390/antibiotics12020328
  63. Wang N, Guo X, Yan Z, et al. A Comprehensive Analysis on Spread and Distribution Characteristic of Antibiotic Resistance Genes in Livestock Farms of Southeastern China. PLoS One. 2016;11(7):e0156889. doi: 10.1371/journal.pone.0156889
  64. Zalewska M, Błażejewska A, Czapko A, Popowska M. Pig manure treatment strategies for mitigating the spread of antibiotic resistance. Scientific Reports. 2023;13(1):11999. doi: 10.1038/s41598-023-39204-4
  65. Wang C, Dong D, Strong PJ, et al. Microbial phylogeny determines transcriptional response of resistome to dynamic composting processes. Microbiome. 2017;5(1):103. doi: 10.1186/s40168-017-0324-0
  66. Selvam A, Xu D, Zhao Z, Wong JW. Fate of tetracycline, sulfonamide and fluoroquinolone resistance genes and the changes in bacterial diversity during composting of swine manure. Bioresour Technol. 2012;126:383-390. doi: 10.1016/j.biortech.2012.03.045
  67. Scicchitano D, Leuzzi D, Babbi G, et al. Dispersion of antimicrobial resistant bacteria in pig farms and in the surrounding environment. Anim Microbiome. 2024;6(1):17. doi: 10.1186/s42523-024-00305-8
  68. Donnik IM, Bykova OA, Lysova YY., et al. Dynamics of antibiotic susceptibility of Enterococcus faecium strains at the dairy farms in the regions with various levels of agrocoenosis contamination. Veterinaria Kubani. 2019;1:7-10. (in Russ.) doi: 10.33861/2071-8020-2019-1-7-10
  69. Krivonogova AS, Moiseeva KV, Lysova YY. Antibiotic susceptibility of cattle microflora in the technogenic polluted areas. Legal regulation in veterinary medicine. 2017;3:159-161. (in Russ.)
  70. Syromyatnikov MY, Shabunin SV, Nesterova EY, et al. Abundance of bacterial antibiotic resistance genes in swine during the fattening period (Sus scrofa domesticus). Educational Establishment "Vitebsk State Academy of Veterinary Medicine". 2023;59(4):96-101. (in Russ.) doi: 10.52368/2078-0109-2023-59-4-96-101.
  71. Syromyatnikov MY, Shabunin SV, Nesterova EY, et al. Assessment of the relative abundance of antibiotic resistance genes of bacteria in the gut of piglets (Sus scrofa domesticus) in the early neonatal period. Educational Establishment "Vitebsk State Academy of Veterinary Medicine". 2023;59(4):89-95. (in Russ.) doi: 10.52368/2078-0109-2023-59-4-89-95
  72. Syromyatnikov MY, Shabunin SV, Nesterova EY, et al. Analysis of antibiotic resistance genes of Escherichia coli from the gut of the piglets with diarrhea. Educational Establishment "Vitebsk State Academy of Veterinary Medicine". 2024;60(2):95-100. (in Russ.) doi: 10.52368/2078-0109-2024-60-2-95-100

Supplementary files

Supplementary Files
Action
1. JATS XML

Copyright (c) Eco-Vector



СМИ зарегистрировано Федеральной службой по надзору в сфере связи, информационных технологий и массовых коммуникаций (Роскомнадзор).
Регистрационный номер и дата принятия решения о регистрации СМИ: серия ПИ № ФС 77 - 89324 от 21.04.2025.