In vitro characterization of lactic acid bacteria and bifidobacteria from wild and domestic pigs: probiotic potential for post-weaning piglets

. 2025 Jan 09 ; 25 (1) : 8. [epub] 20250109

Jazyk angličtina Země Anglie, Velká Británie Médium electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid39789429

Grantová podpora
QL24010234 Ministerstvo Zemědělství
QL24010234 Ministerstvo Zemědělství

Odkazy

PubMed 39789429
PubMed Central PMC11715547
DOI 10.1186/s12866-024-03711-9
PII: 10.1186/s12866-024-03711-9
Knihovny.cz E-zdroje

BACKGROUND: Gastrointestinal diseases in weaned piglets are a frequent cause of high morbidity and mortality in domestic pigs. The use of antibiotics is problematic due to increasing antibiotic resistance in bacterial populations, for which reason the use of suitable probiotics is highly recommended to maintain animal health and welfare. RESULTS: In this study, 57 strains of biologically safe lactic acid bacteria (LAB) and bifidobacteria originating from the gastrointestinal tract (GIT) of pigs were identified and characterized in terms of their probiotic properties for potential use in weaned piglets. These strains were divided into two sets based on their origin - from the GIT of wild boars (n = 41) and from the GIT of domestic pigs (n = 16). Strains obtained from wild boars exhibited greater taxonomic diversity compared to isolates from domestic pigs. While searching for coding sequences (CDS) encoding bacteriocins and bile salt hydrolases (BSH), no significant difference was detected between the two tested groups. On the other hand, CDS encoding adhesinlike factors were more frequent in the dataset isolated from wild boars than in the dataset obtained from domestic pigs. Moreover, more CDS encoding carbohydrateactive enzymes (CAZymes) were carried in the genomes of strains obtained from wild boars. Utilization of important selected carbohydrate substrates, such as starch, D-raffinose, D-mannose, Dcellobiose and gentiobiose, was confirmed by API testing. Antimicrobial activity against at least one of the five tested pathogens was found in 51% of wild boar strains but in none of the isolates from domestic pigs. CONCLUSION: This suggests that the intestinal microbiota of wild boars could serve as a promising source of probiotics for domestic pigs.

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Tang X, Xiong K, Fang R, Li M. Weaning stress and intestinal health of piglets: a review. Front Immunol. 2022;13:1–14. 10.3389/fimmu.2022.1042778. PubMed PMC

Blavi L, Solà-Oriol D, Llonch P, López-Vergé S, Martín-Orúe SM, Pérez JF. Management and feeding strategies in early life to increase piglet performance and welfare around weaning: a review. Animals. 2021;11:1–49. 10.3390/ani11020302. PubMed PMC

Chen L, Xu Y, Chen X, Fang C, Zhao L, Chen F. The maturing development of gut microbiota in commercial piglets during the weaning transition. Front Microbiol. 2017;8:1–13. 10.3389/fmicb.2017.01688. PubMed PMC

Gresse R, Chaucheyras-Durand F, Fleury MA, Van de Wiele T, Forano E, Blanquet-Diot S. Gut microbiota dysbiosis in Postweaning piglets: understanding the Keys to Health. Trends Microbiol. 2017;25:851–73. 10.1016/j.tim.2017.05.004. PubMed

Gebhardt JT, Tokach MD, Dritz SS, DeRouchey JM, Woodworth JC, Goodband RD, et al. Postweaning mortality in commercial swine production II: review of infectious contributing factors. Transl Anim Sci. 2020;4:485–506. 10.1093/TAS/TXAA052. PubMed PMC

Monger XC, Gilbert AA, Saucier L, Vincent AT. Antibiotic resistance: from pig to meat. Antibiotics. 2021;10:1–20. 10.3390/antibiotics10101209. PubMed PMC

Nguyet LTY, Keeratikunakorn K, Kaeoket K, Ngamwongsatit N. Antibiotic resistant Escherichia coli from diarrheic piglets from pig farms in Thailand that harbor colistin-resistant mcr genes. Sci Rep. 2022;12:1–10. 10.1038/s41598-022-13192-3. PubMed PMC

Martin MJ, Thottathil SE, Newman TB. Antibiotics overuse in animal agriculture: a call to action for health care providers. Am J Public Health. 2015;105:2409–10. 10.2105/AJPH.2015.302870. PubMed PMC

Road GW. Annex I list of the names, pharmaceutical forms, strengths of the medicinal products, route of administration, applicants and marketing authorisation holders in the member states. 2004;1–47.

Hou C, Zeng X, Yang F, Liu H, Qiao S. Study and use of the probiotic Lactobacillus reuteri in pigs: a review. J Anim Sci Biotechnol. 2015;6:1–8. 10.1186/s40104-015-0014-3. PubMed PMC

Bielecka M. Probiotics in food. Chemical and Functional properties of Food Components. 3rd ed. 2006;413–26. 10.1201/9781420009613.ch16.

Keresztény T, Libisch B, Orbe SC, Nagy T, Kerényi Z, Kocsis R, et al. Isolation and characterization of lactic acid Bacteria with probiotic attributes from different parts of the gastrointestinal tract of Free-living wild boars in Hungary. Probiotics Antimicrob Proteins. 2023. 10.1007/s12602-023-10113-2. PubMed PMC

Marchwińska K, Gwiazdowska D. Isolation and probiotic potential of lactic acid bacteria from swine feces for feed additive composition. Arch Microbiol. 2022;204:1–21. 10.1007/s00203-021-02700-0. PubMed PMC

Zhong Y, Fu D, Deng Z, Tang W, Mao J, Zhu T, et al. Lactic acid Bacteria mixture isolated from Wild Pig alleviated the gut inflammation of mice challenged by Escherichia coli. Front Immunol. 2022;13:1–13. 10.3389/fimmu.2022.822754. PubMed PMC

Singh A, Kumar S, Vinay VV, Tyagi B, Choudhury PK, Rashmi HM, et al. Autochthonous Lactobacillus spp. isolated from Murrah buffalo calves show potential application as probiotic. Curr Res Biotechnol. 2021;3:109–19. 10.1016/j.crbiot.2021.04.002.

Varada VV, Kumar S, Chhotaray S, Tyagi AK. Host-specific probiotics feeding influence growth, gut microbiota, and fecal biomarkers in buffalo calves. AMB Express. 2022;12:12. 10.1186/s13568-022-01460-4. PubMed PMC

Kwoji ID, Aiyegoro OA, Okpeku M, Adeleke MA. Multi-strain probiotics: synergy among isolates enhances biological activities. Biology. 2021;10:1–20. 10.3390/biology10040322. PubMed PMC

Lambo MT, Chang X, Liu D. The recent trend in the use of multistrain probiotics in livestock production: an overview. Animals. 2021;11:1–15. 10.3390/ani11102805. PubMed PMC

Lee WJ, Ryu S, Kang AN, Song M, Shin M, Oh S, et al. Molecular characterization of gut microbiome in weaning pigs supplemented with multi-strain probiotics using metagenomic, culturomic, and metabolomic approaches. Anim Microbiome. 2022;4:4. 10.1186/s42523-022-00212-w. PubMed PMC

Elshaghabee FMF, Rokana N. Mitigation of antibiotic resistance using probiotics, prebiotics and synbiotics. A review. Environ Chem Lett. 2022;20:1295–308. 10.1007/s10311-021-01382-w.

Muñoz-Atienza E, Gómez-Sala B, Araújo C, Campanero C, Del Campo R, Hernández PE, et al. Antimicrobial activity, antibiotic susceptibility and virulence factors of lactic acid Bacteria of aquatic origin intended for use as probiotics in aquaculture. BMC Microbiol. 2013;13:13. 10.1186/1471-2180-13-15. PubMed PMC

Patel AK, Singhania RR, Pandey A, Chincholkar SB. Probiotic bile salt hydrolase: current developments and perspectives. Appl Biochem Biotechnol. 2010;162:166–80. 10.1007/s12010-009-8738-1. PubMed

Su W, Gong T, Jiang Z, Lu Z, Wang Y. The role of Probiotics in alleviating Postweaning Diarrhea in Piglets from the perspective of intestinal barriers. Front Cell Infect Microbiol. 2022;12:1–12. 10.3389/fcimb.2022.883107. PubMed PMC

Liao SF, Nyachoti M. Using probiotics to improve swine gut health and nutrient utilization. Anim Nutr. 2017;3:331–43. 10.1016/j.aninu.2017.06.007. PubMed PMC

Cao H, Yang X, Peng C, Wang Y, Guo Q, Su H. Gut microbiota reveals the environmental adaption in gastro-intestinal tract of wild boar in karst region of Southwest China. Ann Microbiol. 2022;72. 10.1186/s13213-022-01669-5.

Wei L, Zhou W, Zhu Z. Comparison of changes in gut microbiota in wild boars and domestic pigs using 16S rRNA gene and Metagenomics Sequencing Technologies. Animals. 2022;12:12. 10.3390/ani12172270. PubMed PMC

Ding J, Cui X, Wang X, Zhai F, Wang L, Zhu L. Multi-omics analysis of gut microbiota and metabolites reveals contrasting profiles in domestic pigs and wild boars across urban environments. Front Microbiol. 2024;15:1–15. 10.3389/fmicb.2024.1450306. PubMed PMC

Vedel G, Triadó-Margarit X, Linares O, Moreno-Rojas JM, de la Peña E, García-Bocanegra I, Jímenez-Martín D, Carranza J, Casamayor EO. Exploring the potential links between gut microbiota composition and natural populations management in wild boar (Sus scrofa). Microbiol Res. 2023;274:127444. 10.1016/j.micres.2023.127444. PubMed

Wang X, Zhang Y, Wen Q, Wang Y, Wang Z, Tan Z, Wu K. Sex differences in intestinal microbial composition and function of hainan specialwild boar. Animals. 2020;10:1–13. 10.3390/ani10091553. PubMed PMC

Bravo M, Combes T, Martinez FO, Risco D, Gonçalves P, Garcia-Jimenez WL, Cerrato R, Fernandez-Llario P, Gutierrez-Merino J. Wildlife symbiotic Bacteria are indicators of the Health Status of the host and its ecosystem. Appl Environ Microbiol. 2022;88:88. 10.1128/AEM.01385-21. PubMed PMC

Li M, Wang Y, Cui H, Li Y, Sun Y, Qiu HJ. Characterization of lactic acid Bacteria isolated from the gastrointestinal tract of a wild boar as potential probiotics. Front Vet Sci. 2020;7:1–10. 10.3389/fvets.2020.00049. PubMed PMC

Ewels P, Magnusson M, Lundin S, Käller M, MultiQC. Summarize analysis results for multiple tools and samples in a single report. Bioinformatics. 2016;32:3047–8. 10.1093/bioinformatics/btw354. PubMed PMC

Wick RR, Judd LM, Gorrie CL, Holt KE, Unicycler. Resolving bacterial genome assemblies from short and long sequencing reads. PLoS Comput Biol. 2017;13:1–22. 10.1371/journal.pcbi.1005595. PubMed PMC

Nurk S, Meleshko D, Korobeynikov A, Pevzner PA. MetaSPAdes: a new versatile metagenomic assembler. Genome Res. 2017;27:824–34. 10.1101/gr.213959.116. PubMed PMC

Jain C, Rodriguez-R LM, Phillippy AM, Konstantinidis KT, Aluru S. High throughput ANI analysis of 90K prokaryotic genomes reveals clear species boundaries. Nat Commun. 2018;9:1–8. 10.1038/s41467-018-07641-9. PubMed PMC

Seemann T, Prokka. Rapid prokaryotic genome annotation. Bioinformatics. 2014;30:2068–9. 10.1093/bioinformatics/btu153. PubMed

Huerta-Cepas J, Szklarczyk D, Heller D, Hernández-Plaza A, Forslund SK, Cook H, et al. EggNOG 5.0: a hierarchical, functionally and phylogenetically annotated orthology resource based on 5090 organisms and 2502 viruses. Nucleic Acids Res. 2019;47:D309-14. 10.1093/nar/gky1085. PubMed PMC

Buchfink B, Reuter K, Drost HG. Sensitive protein alignments at tree-of-life scale using DIAMOND. Nat Methods. 2021;18:366–8. 10.1038/s41592-021-01101-x. PubMed PMC

Zhang H, Yohe T, Huang L, Entwistle S, Wu P, Yang Z, et al. DbCAN2: a meta server for automated carbohydrate-active enzyme annotation. Nucleic Acids Res. 2018;46:W95-101. 10.1093/nar/gky418. PubMed PMC

Steinegger M, Söding J. Clustering huge protein sequence sets in linear time. Nat Commun. 2018;9:9. 10.1038/s41467-018-04964-5. PubMed PMC

Jia B, Raphenya AR, Alcock B, Waglechner N, Guo P, Tsang KK, et al. CARD 2017: expansion and model-centric curation of the comprehensive antibiotic resistance database. Nucleic Acids Res. 2017;45:D566-73. 10.1093/nar/gkw1004. PubMed PMC

Zankari E, Hasman H, Cosentino S, Vestergaard M, Rasmussen S, Lund O, et al. Identification of acquired antimicrobial resistance genes. J Antimicrob Chemother. 2012;67:2640–4. 10.1093/jac/dks261. PubMed PMC

Gupta SK, Padmanabhan BR, Diene SM, Lopez-Rojas R, Kempf M, Landraud L, et al. ARG-annot, a new bioinformatic tool to discover antibiotic resistance genes in bacterial genomes. Antimicrob Agents Chemother. 2014;58:212–20. 10.1128/AAC.01310-13. PubMed PMC

Doster E, Lakin SM, Dean CJ, Wolfe C, Young JG, Boucher C, et al. MEGARes 2.0: a database for classification of antimicrobial drug, biocide and metal resistance determinants in metagenomic sequence data. Nucleic Acids Res. 2020;48:D561-9. 10.1093/nar/gkz1010. PubMed PMC

Feldgarden M, Brover V, Haft DH, Prasad AB, Slotta DJ, Tolstoy I, et al. Validating the AMRFINder tool and resistance gene database by using antimicrobial resistance genotype-phenotype correlations in a collection of isolates. Antimicrob Agents Chemother. 2019;63:1–19. 10.1128/AAC.00483-19. PubMed PMC

Moravkova M, Kostovova I, Kavanova K, Pechar R, Stanek S, Brychta A, et al. Antibiotic susceptibility, Resistance Gene determinants and corresponding genomic regions in Lactobacillus amylovorus isolates derived from Wild boars and Domestic pigs. Microorganisms. 2023;11:11. 10.3390/microorganisms11010103. PubMed PMC

Kavanova K, Kostovova I, Moravkova M, Kubasova T, Babak V, Crhanova M. Comparative Genome Analysis and characterization of the Probiotic properties of lactic acid Bacteria isolated from the gastrointestinal tract of wild boars in the Czech Republic. Probiotics Antimicrob Proteins. 2024. 10.1007/s12602-024-10259-7. PubMed

Mu Q, Tavella VJ, Luo XM. Role of Lactobacillus reuteri in human health and diseases. Front Microbiol. 2018;9:1–17. 10.3389/fmicb.2018.00757. PubMed PMC

Klose V, Bayer K, Kern C, Goelß F, Fibi S, Wegl G. Antibiotic resistances of intestinal lactobacilli isolated from wild boars. Vet Microbiol. 2014;168:240–4. 10.1016/j.vetmic.2013.11.014. PubMed

Horvathova K, Modrackova N, Splichal I, Splichalova A, Amin A, Ingribelli E, et al. Defined Pig Microbiota with a potential protective effect against infection with Salmonella Typhimurium. Microorganisms. 2023;11:1–13. 10.3390/microorganisms11041007. PubMed PMC

Ma J, Duan Y, Li R, Liang X, Li T, Huang X, et al. Gut microbial profiles and the role in lipid metabolism in Shaziling pigs. Anim Nutr. 2022;9:345–56. 10.1016/j.aninu.2021.10.012. PubMed PMC

Shen J, Zhang J, Zhao Y, Lin Z, Ji L, Ma X. Tibetan pig-derived probiotic Lactobacillus amylovorus SLZX20-1 improved intestinal function via producing enzymes and regulating intestinal Microflora. Front Nutr. 2022;9:1–15. 10.3389/fnut.2022.846991. PubMed PMC

Kim JS, Choe H, Kim KM, Lee YR, Rhee MS, Park DS. Lactobacillus porci sp. Nov., isolated from small intestine of a swine. Int J Syst Evol Microbiol. 2018;68:3118–24. 10.1099/ijsem.0.002949. PubMed

Killer J, Havlík J, Bunešová V, Vlková E, Benada O. Pseudoscardovia radai sp. nov., a representative of the family Bifidobacteriaceae isolated from the digestive tract of a wild pig (Sus scrofa scrofa). Int J Syst Evol Microbiol. 2014;64:2932–8. 10.1099/ijs.0.063230-0. PubMed

Holman DB, Gzyl KE, Kommadath A. The gut microbiome and resistome of conventionally vs. pasture-raised pigs. Microb Genom. 2023;9:1–11. 10.1099/mgen.0.001061. PubMed PMC

Huang J, Zhang W, Fan R, Liu Z, Huang T, Li J, et al. Composition and functional diversity of fecal bacterial community of wild boar, commercial pig and domestic native pig as revealed by 16S rRNA gene sequencing. Arch Microbiol. 2020;202:843–57. 10.1007/s00203-019-01787-w. PubMed

Muscariello L, De Siena B, Marasco R. Lactobaccellssurfaceuproteinsoinvolvedvolved in Interactionmucus Mucus and Extracellular Matrix Components. Curr Microbiol. 2020;77:3831–41. 10.1007/s00284-020-02243-5. PubMed PMC

Ayyash MM, Abdalla AK, AlKalbani NS, Baig MA, Turner MS, Liu SQ, et al. Invited review: characterization of new probiotics from dairy and nondairy products—insights into acid tolerance, bile metabolism and tolerance, and adhesion capability. J Dairy Sci. 2021;104:8363–79. 10.3168/jds.2021-20398. PubMed

Guo XH, Kim JM, Nam HM, Park SY, Kim JM. Screening lactic acid bacteria from swine origins for multistrain probiotics based on in vitro functional properties. Anaerobe. 2010;16:321–6. 10.1016/j.anaerobe.2010.03.006. PubMed

Vizoso Pinto MG, Franz CMAP, Schillinger U, Holzapfel WH. Lactobacillus spp. with in vitro probiotic properties from human faeces and traditional fermented products. Int J Food Microbiol. 2006;109:205–14. 10.1016/j.ijfoodmicro.2006.01.029. PubMed

Devi SM, Archer AC, Halami PM. Screening, characterization and in Vitro evaluation of Probiotic properties among lactic acid Bacteria through comparative analysis. Probiotics Antimicrob Proteins. 2015;7:181–92. 10.1007/s12602-015-9195-5. PubMed

Luo R, Liu C, Li Y, Liu Q, Su X, Peng Q, et al. Comparative Genomics Analysis of Habitat Adaptation by Lactobacillus kefiranofaciens. Foods. 2023;12:12. 10.3390/foods12081606. PubMed PMC

Simons A, Alhanout K, Duval RE. Bacteriocins, antimicrobial peptides from bacterial origin: Overview of their biology and their impact against multidrug-resistant bacteria. Microorganisms. 2020;8:639. 10.3390/microorganisms8050639. PubMed PMC

Collins FWJ, O’Connor PM, O’Sullivan O, Gómez-Sala B, Rea MC, Hill C, et al. Bacteriocin Gene-Trait matching across the complete Lactobacillus pan-genome. Sci Rep. 2017;7:1–14. 10.1038/s41598-017-03339-y. PubMed PMC

Park S, Kim JA, Jang HJ, Kim DH, Kim Y. Complete genome sequence of functional probiotic candidate Lactobacillus amylovorus CACC736. J Anim Sci Technol. 2023;65:473–7. 10.5187/jast.2022.e85. PubMed PMC

Khan H, Flint SH, Yu PL. Determination of the mode of action of enterolysin A, produced by Enterococcus faecalis B9510. J Appl Microbiol. 2013;115:484–94. 10.1111/jam.12240. PubMed

Jia Y, Yang B, Ross P, Stanton C, Zhang H, Zhao J, et al. Comparative genomics analysis of Lactobacillus mucosae from different niches. Genes. 2020;11:11. 10.3390/genes11010095. PubMed PMC

Qin S, Du H, Zeng W, Bai A, Liu J, Chen F, et al. Identification and characterisation of potential probiotic lactic acid Bacteria extracted from Pig Faeces. J Pure Appl Microbiol. 2023;17:788–98. 10.22207/JPAM.17.2.04.

Maldonado NC, Ficoseco CA, Mansilla FI, Melián C, Hébert EM, Vignolo GM, et al. Identification, characterization and selection of autochthonous lactic acid bacteria as probiotic for feedlot cattle. Livest Sci. 2018;212:99–110. 10.1016/j.livsci.2018.04.003.

Angmo K, Kumari A, Monika, Savitri, Chand Bhalla T. Antagonistic activities of lactic acid bacteria from fermented foods and beverage of Ladakh against Yersinia enterocolitica in refrigerated meat. Food Biosci. 2016;13:26–31. 10.1016/j.fbio.2015.12.004.

Jha R, Berrocoso JD. Review: Dietary fiber utilization and its effects on physiological functions and gut health of swine. Animal. 2015;9:1441–52. 10.1017/S1751731115000919. PubMed PMC

Macfarlane GT, Macfarlane S. Bacteria, colonic fermentation, and gastrointestinal health. J AOAC Int. 2012;95(1):50–60. 10.5740/jaoacint.SGE_Macfarlane. PubMed

Hii SL, Tan JS, Ling TC, Ariff A, Bin. Pullulanase: Role in starch hydrolysis and potential industrial applications. Enzyme Res. 2012;2012:921362. 10.1155/2012/921362. PubMed PMC

Telles FG, Saleh MAD, de Paula VRC, Alvarenga PVA, Leonel M, Araújo LF, et al. Pig diets formulated with different sources of starch based in vitro kinetics of starch digestion. Livest Sci. 2023;268:105149. 10.1016/j.livsci.2022.105149.

Park KH, Kim TJ, Cheong TK, Kim JW, Oh BH, Svensson B. Structure, specificity and function of cyclomaltodextrinase, a multispecific enzyme of the alpha-amylase family. Biochim Biophys Acta. 2020;1478(2):165–85. 10.1016/s0167-4838(00)00041-8. PubMed

Fan W, Li Z, Li C, Gu Z, Hong Y, Cheng L, et al. Catalytic activity enhancement of 1,4-α-glucan branching enzyme by N-terminal modification. Food Chem X. 2023;20:100888. 10.1016/j.fochx.2023.100888. PubMed PMC

Li D, Fei T, Wang Y, Zhao Y, Dai L, Fu X, et al. A cold-active 1,4-α-glucan branching enzyme from Bifidobacterium longum reduces the retrogradation and enhances the slow digestibility of wheat starch. Food Chem. 2020;324:126855. 10.1016/j.foodchem.2020.126855. PubMed

Kanwal F, Ren D, Kanwal W, Ding M, Su J, Shang X. The potential role of nondigestible Raffinose family oligosaccharides as prebiotics. Glycobiology. 2023;33:274–88. 10.1093/glycob/cwad015. PubMed

Buron-Moles G, Chailyan A, Dolejs I, Forster J, Mikš MH. Uncovering carbohydrate metabolism through a genotype-phenotype association study of 56 lactic acid bacteria genomes. Appl Microbiol Biotechnol. 2019;103:3135–52. 10.1007/s00253-019-09701-6. PubMed PMC

Ucar RA, Pérez-Díaz IM, Dean LL. Gentiobiose and cellobiose content in fresh and fermenting cucumbers and utilization of such disaccharides by lactic acid bacteria in fermented cucumber juice medium. Food Sci Nutr. 2020;8:5798–810. 10.1002/fsn3.1830. PubMed PMC

Navarro DMDL, Abelilla JJ, Stein HH. Structures and characteristics of carbohydrates in diets fed to pigs: a review. J Anim Sci Biotechnol. 2019;10:1–17. 10.1186/s40104-019-0345-6. PubMed PMC

Elbein AD, Pan YT, Pastuszak I, Carroll D. New insights on trehalose: a multifunctional molecule. Glycobiology. 2003;13:17–27. 10.1093/glycob/cwg047. PubMed

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