Skip to main content
Log in

Short-term feeding of probiotics and synbiotics modulates caecal microbiota during Salmonella Typhimurium infection but does not reduce shedding and invasion in chickens

  • Applied microbial and cell physiology
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

Positive modulation of gut microbiota in laying chickens may offer a strategy for reduction of Salmonella Typhimurium shedding and production of safer poultry products. In the current study, the caecal luminal microbiota of laying chicks was studied using 16S rRNA amplicon sequencing on DNA obtained from the chicks that were offered supplementation with commercial probiotics, synbiotics and/or Salmonella Typhimurium challenge. The load of Salmonella Typhimurium in various organs was quantified. Irrespective of the probiotics and synbiotics supplementation and Salmonella Typhimurium challenge, caecal microbiota was dominated by 22 distinct bacterial genera and 14 families that clustered into Actinobacteria, Proteobacteria and Firmicutes at phylum level. Taken together, probiotics and synbiotics supplementation increased (false discovery rate; FDR < 0.05) the abundance of Ruminococcus, Trabulsiella, Bifidobacterium, Holdemania and Oscillospira, indicating their role in maintaining gut health through lowering luminal pH and digestion of complex polysaccharides. Salmonella Typhimurium challenge decreased the abundance of Trabulsiella, Oscillospira, Holdemania, Coprococcus, Bifidobacterium and Lactobacillus and increased Klebsiella and Escherichia, indicating its role in caecal dysbiosis. Although probiotics and synbiotics supplementation positively modulated the caecal microbiota, they were not effective in significantly (P > 0.05) reducing Salmonella Typhimurium load in caecal tissue and invasion into vital organs such as liver and spleen. The early colonisation of laying chick caeca by probiotics and synbiotics had the potential to positively influence luminal microbiota; however, the microbial abundance and diversity were not sufficient to significantly reduce the shedding of Salmonella Typhimurium in faeces or invasion into internal organs during this study.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Adhikari P, Lee CH, Cosby DE, Cox NA, Kim WK (2018) Effect of probiotics on fecal excretion, colonization in internal organs and immune gene expression in the ileum of laying hens challenged with Salmonella Enteritidis. Poult Sci 98(3):1235–1242. https://doi.org/10.3382/ps/pey443

    Article  CAS  Google Scholar 

  • Azcarate-Peril MA, Butz N, Cadenas MB, Koci M, Ballou A, Mendoza M, Ali R, Hassan H (2018) An attenuated Salmonella enterica serovar Typhimurium strain and galacto-oligosaccharides accelerate clearance of Salmonella infections in poultry through modifications to the gut microbiome. Appl Environ Microbiol 84(5):e02526–e02517. https://doi.org/10.1128/aem.02526-17

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Babu US, Sommers K, Harrison LM, Balan KV (2012) Effects of fructooligosaccharide-inulin on Salmonella-killing and inflammatory gene expression in chicken macrophages. Vet Immunol Immunopathol 149(1):92–96. https://doi.org/10.1016/j.vetimm.2012.05.003

    Article  CAS  PubMed  Google Scholar 

  • Ballou AL, Ali RA, Mendoza MA, Ellis JC, Hassan HM, Croom WJ, Koci MD (2016) Development of the chick microbiome: how early exposure influences future microbial diversity. Front Vet Sci 3(2). https://doi.org/10.3389/fvets.2016.00002

  • Barrow PA, Lovell MA (1991) Experimental infection of egg-laying hens with Salmonella Enteritidis phage type 4. Avian Pathol 20(2):335–348. https://doi.org/10.1080/03079459108418769

    Article  CAS  PubMed  Google Scholar 

  • Bayer EA, Lamed R, White BA, Flint HJ (2008) From cellulosomes to cellulosomics. Chem Rec 8(6):364–377

    CAS  PubMed  Google Scholar 

  • Benakis C, Brea D, Caballero S, Faraco G, Moore J, Murphy M, Sita G, Racchumi G, Ling L, Pamer EG (2016) Commensal microbiota affects ischemic stroke outcome by regulating intestinal γδ T cells. Nat Med 22(5):516–523

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bozkurt M, Bintaş E, Kırkan Ş, Akşit H, Küçükyılmaz K, Erbaş G, Cabuk M, Akşit D, Parın U, Ege G (2016) Comparative evaluation of dietary supplementation with mannan oligosaccharide and oregano essential oil in forced molted and fully fed laying hens between 82 and 106 weeks of age. Poult Sci 95(11):2576–2591

    CAS  PubMed  Google Scholar 

  • Bratburd JR, Keller C, Vivas E, Gemperline E, Li L, Rey FE, Currie CR (2018) Gut microbial and metabolic responses to Salmonella enterica serovar Typhimurium and Candida albicans. mBio 9(6):e02032–e02018. https://doi.org/10.1128/mBio.02032-18

    Article  PubMed  PubMed Central  Google Scholar 

  • Buts J-P, De Keyser N, De Raedemaeker L (1994) Saccharomyces boulardii enhances rat intestinal enzyme expression by endoluminal release of polyamines. Pediatr Res 36(4):522–527

    CAS  PubMed  Google Scholar 

  • Callaway TR, Dowd SE, Wolcott RD, Sun Y, McReynolds JL, Edrington TS, Byrd JA, Anderson RC, Krueger N, Nisbet DJ (2009) Evaluation of the bacterial diversity in cecal contents of laying hens fed various molting diets by using bacterial tag-encoded FLX amplicon pyrosequencing. Poult Sci 88(2):298–302

    CAS  PubMed  Google Scholar 

  • Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Meth 7(5):335

    CAS  Google Scholar 

  • Casey PG, Gardiner GE, Casey G, Bradshaw B, Lawlor PG, Lynch PB, Leonard FC, Stanton C, Ross RP, Fitzgerald GF, Hill C (2007) A five-strain probiotic combination reduces pathogen shedding and alleviates disease signs in pigs challenged with Salmonella enterica Serovar Typhimurium. Appl Environ Microbiol 73(6):1858–1863. https://doi.org/10.1128/aem.01840-06

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chang CH, Teng PY, Lee TT, Yu B (2019) The effects of the supplementation of multi-strain probiotics on intestinal microbiota, metabolites and inflammation of young SPF chickens challenged with Salmonella enterica subsp. enterica. Anim Sci J 90(6):737–746. https://doi.org/10.1111/asj.13205

    Article  CAS  PubMed  Google Scholar 

  • Chart H, Baskerville A, Humphrey T, Rowe B (1992) Serological responses of chickens experimentally infected with Salmonella enteritidis PT4 by different routes. Epidemiol Infect 109(2):297–302

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chen Y-S, Srionnual S, Onda T, Yanagida F (2007) Effects of prebiotic oligosaccharides and trehalose on growth and production of bacteriocins by lactic acid bacteria. Lett Appl Microbiol 45(2):190–193. https://doi.org/10.1111/j.1472-765X.2007.02167.x

    Article  CAS  PubMed  Google Scholar 

  • Cox NA, McHan F, Bailey JS, Shotts EB (1994) Effect of butyric or lactic acid on the in vivo colonization of Salmonella typhimurium. J Appl Poult Res 3(4):315–318

    Google Scholar 

  • Crhanova M, Hradecka H, Faldynova M, Matulova M, Havlickova H, Sisak F, Rychlik I (2011) Immune response of chicken gut to natural colonization by gut microflora and to Salmonella enterica serovar Enteritidis infection. Infect Immun 79(7):2755–2763

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cui Y, Wang Q, Liu S, Sun R, Zhou Y, Li Y (2017) Age-related variations in intestinal microflora of free-range and caged hens. Front Micro 8:1310–1310. https://doi.org/10.3389/fmicb.2017.01310

    Article  Google Scholar 

  • Deriu E, Liu JZ, Pezeshki M, Edwards RA, Ochoa RJ, Contreras H, Libby SJ, Fang FC, Raffatellu M (2013) Probiotic bacteria reduce Salmonella Typhimurium intestinal colonization by competing for iron. Cell Host Microbe 14(1):26–37. https://doi.org/10.1016/j.chom.2013.06.007

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, Huber T, Dalevi D, Hu P, Andersen GL (2006) Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol 72(7):5069–5072

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ding XM, Li DD, Bai SP, Wang JP, Zeng QF, Su ZW, Xuan Y, Zhang KY (2017) Effect of dietary xylooligosaccharides on intestinal characteristics, gut microbiota, cecal short-chain fatty acids, and plasma immune parameters of laying hens. Poult Sci 97(3):874–881

    Google Scholar 

  • Donalson LM, McReynolds JL, Kim WK, Chalova VI, Woodward CL, Kubena LF, Nisbet DJ, Ricke SC (2008) The influence of a fructooligosaccharide prebiotic combined with alfalfa molt diets on the gastrointestinal tract fermentation, Salmonella Enteritidis infection, and intestinal shedding in laying hens. Poult Sci 87(7):1253–1262

    CAS  PubMed  Google Scholar 

  • Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26(19):2460–2461

    CAS  PubMed  Google Scholar 

  • Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Meth 10(10):996

    CAS  Google Scholar 

  • Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27(16):2194–2200

    CAS  PubMed  PubMed Central  Google Scholar 

  • Engels C, Ruscheweyh H-J, Beerenwinkel N, Lacroix C, Schwab C (2016) The common gut microbe Eubacterium hallii also contributes to intestinal propionate formation. Front Micro 7:713

    Google Scholar 

  • Fanning S, Hall LJ, van Sinderen D (2012) Bifidobacterium breve UCC2003 surface exopolysaccharide production is a beneficial trait mediating commensal-host interaction through immune modulation and pathogen protection. Gut Microbes 3(5):420–425

    PubMed  Google Scholar 

  • Fearnley E, Raupach J, Lagala F, Cameron S (2011) Salmonella in chicken meat, eggs and humans; Adelaide, South Australia, 2008. Int J Food Microbiol 146(3):219–227. https://doi.org/10.1016/j.ijfoodmicro.2011.02.004

    Article  PubMed  Google Scholar 

  • Fekry MI, Engels C, Zhang J, Schwab C, Lacroix C, Sturla SJ, Chassard C (2016) The strict anaerobic gut microbe Eubacterium hallii transforms the carcinogenic dietary heterocyclic amine 2-amino-1-methyl-6-phenylimidazo [4, 5-b] pyridine (PhIP). Environ Microbiol Rep 8(2):201–209

    CAS  PubMed  Google Scholar 

  • Forte C, Acuti G, Manuali E, Casagrande Proietti P, Pavone S, Trabalza-Marinucci M, Moscati L, Onofri A, Lorenzetti C, Franciosini M (2016) Effects of two different probiotics on microflora, morphology, and morphometry of gut in organic laying hens. Poult Sci 95(11):2528–2535

    CAS  PubMed  Google Scholar 

  • Fukata T, Sasai K, Miyamoto T, Baba E (1999) Inhibitory effects of competitive exclusion and fructooligosaccharide, singly and in combination, on Salmonella colonization of chicks. J Food Prot 62(3):229–233

    CAS  PubMed  Google Scholar 

  • Fuller R (1989) Probiotics in man and animals. J Appl Bacteriol 66(5):365–378

    CAS  PubMed  Google Scholar 

  • Gole VC, Torok V, Sexton M, Caraguel CGB, Chousalkar KK (2014) Association between indoor environmental contamination by Salmonella enterica and contamination of eggs on layer farms. J Clin Microbiol 52(9):3250–3258. https://doi.org/10.1128/jcm.00816-14

    Article  PubMed  PubMed Central  Google Scholar 

  • Goodrich JK, Davenport ER, Waters JL, Clark AG, Ley RE (2016) Cross-species comparisons of host genetic associations with the microbiome. Science 352(6285):532–535

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gophna U, Konikoff T, Nielsen HB (2017) Oscillospira and related bacteria–From metagenomic species to metabolic features. Environ Microbiol 19(3):835–841

    CAS  PubMed  Google Scholar 

  • Haghighi HR, Abdul-Careem MF, Dara RA, Chambers JR, Sharif S (2008) Cytokine gene expression in chicken cecal tonsils following treatment with probiotics and Salmonella infection. Vet Microbiol 126(1):225–233. https://doi.org/10.1016/j.vetmic.2007.06.026

    Article  CAS  PubMed  Google Scholar 

  • Hooper LV, Wong MH, Thelin A, Hansson L, Falk PG, Gordon JI (2001) Molecular analysis of commensal host-microbial relationships in the intestine. Science 291(5505):881–884

    CAS  PubMed  Google Scholar 

  • Huang P, Zhang Y, Xiao K, Jiang F, Wang H, Tang D, Liu D, Liu B, Liu Y, He X (2018) The chicken gut metagenome and the modulatory effects of plant-derived benzylisoquinoline alkaloids. Microbiome 6(1):211

    PubMed  PubMed Central  Google Scholar 

  • Juricova H, Videnska P, Lukac M, Faldynova M, Babak V, Havlickova H, Sisak F, Rychlik I (2013) Influence of Salmonella enterica serovar Enteritidis infection on the development of the cecum microbiota in newly hatched chicks. Appl Environ Microbiol 79(2):745–747. https://doi.org/10.1128/aem.02628-12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kubasova T, Kollarcikova M, Crhanova M, Karasova D, Cejkova D, Sebkova A, Matiasovicova J, Faldynova M, Pokorna A, Cizek A (2019) Contact with adult hen affects development of caecal microbiota in newly hatched chicks. PLoS One 14(3):e0212446

    PubMed  PubMed Central  Google Scholar 

  • Kurtoglu V, Kurtoglu F, Seker E, Coskun B, Balevi T, Polat E (2004) Effect of probiotic supplementation on laying hen diets on yield performance and serum and egg yolk cholesterol. Food Addit Contam 21(9):817–823

    CAS  PubMed  Google Scholar 

  • Liu L, Lin L, Zheng L, Tang H, Fan X, Xue N, Li M, Liu M, Li X (2018) Cecal microbiome profile altered by Salmonella enterica, serovar Enteritidis inoculation in chicken. Gut Pathog 10(1):34–14. https://doi.org/10.1186/s13099-018-0261-x

    Article  PubMed  PubMed Central  Google Scholar 

  • Luoma A, Markazi A, Shanmugasundaram R, Murugesan GR, Mohnl M, Selvaraj R (2017) Effect of synbiotic supplementation on layer production and cecal Salmonella load during a Salmonella challenge. Poult Sci 96(12):4208–4216

    CAS  PubMed  Google Scholar 

  • Mackie RI, Aminov RI, Hu W, Klieve AV, Ouwerkerk D, Sundset MA, Kamagata Y (2003) Ecology of uncultivated Oscillospira species in the rumen of cattle, sheep, and reindeer as assessed by microscopy and molecular approaches. Appl Environ Microbiol 69(11):6808–6815

    CAS  PubMed  PubMed Central  Google Scholar 

  • Marcq C, Cox E, Szalo IM, Thewis A, Beckers Y (2011) Salmonella Typhimurium oral challenge model in mature broilers: bacteriological, immunological, and growth performance aspects. Poult Sci 90(1):59–67

    CAS  PubMed  Google Scholar 

  • McWhorter AR, Chousalkar KK (2018) A long-term efficacy trial of a live, attenuated Salmonella Typhimurium vaccine in layer hens. Front Micro 9:1380–1380. https://doi.org/10.3389/fmicb.2018.01380

    Article  Google Scholar 

  • Mikulski D, Jankowski J, Naczmanski J, Mikulska M, Demey V (2012) Effects of dietary probiotic (Pediococcus acidilactici) supplementation on performance, nutrient digestibility, egg traits, egg yolk cholesterol, and fatty acid profile in laying hens. Poult Sci 91(10):2691–2700

    CAS  PubMed  Google Scholar 

  • Milani C, Lugli GA, Duranti S, Turroni F, Mancabelli L, Ferrario C, Mangifesta M, Hevia A, Viappiani A, Scholz M (2015) Bifidobacteria exhibit social behavior through carbohydrate resource sharing in the gut. Sci Rep 5:15782

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mon KKZ, Saelao P, Halstead MM, Chanthavixay G, Chang H-C, Garas L, Maga EA, Zhou H (2015) Salmonella enterica serovars Enteritidis infection alters the indigenous microbiota diversity in young layer chicks. Front Vet Sci 2:61

    PubMed  PubMed Central  Google Scholar 

  • Montgomery L (1988) Isolation of human colonic fibrolytic bacteria. Lett Appl Microbiol 6(3):55–57

    Google Scholar 

  • Moon YH, Iakiviak M, Bauer S, Mackie RI, Cann IKO (2011) Biochemical analyses of multiple endoxylanases from the rumen bacterium Ruminococcus albus 8 and their synergistic activities with accessory hemicellulose-degrading enzymes. Appl Environ Microbiol 77(15):5157–5169

    CAS  PubMed  PubMed Central  Google Scholar 

  • Naqid IA, Owen JP, Maddison BC, Gardner DS, Foster N, Tchórzewska MA, La Ragione RM, Gough KC (2015) Prebiotic and probiotic agents enhance antibody-based immune responses to Salmonella Typhimurium infection in pigs. Anim Feed Sci Technol 201:57–65. https://doi.org/10.1016/j.anifeedsci.2014.12.005

    Article  CAS  Google Scholar 

  • Ngunjiri JM, Taylor KJM, Abundo MC, Jang H, Elaish M, Kc M, Ghorbani A, Wijeratne S, Weber BP, Johnson TJ, Lee C-W (2019) Farm stage, bird age and body site dominantly affect the quantity, taxonomic composition, and dynamics of respiratory and gut microbiota of commercial layer chickens. Appl Environ Microbiol 85(9):e03137–e03118. https://doi.org/10.1128/aem.03137-18

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nordentoft S, Mølbak L, Bjerrum L, De Vylder J, Van Immerseel F, Pedersen K (2011) The influence of the cage system and colonisation of Salmonella Enteritidis on the microbial gut flora of laying hens studied by T-RFLP and 454 pyrosequencing. BMC Microbiol 11(1):187. https://doi.org/10.1186/1471-2180-11-187

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ocejo M, Oporto B, Hurtado A (2019) 16S rRNA amplicon sequencing characterization of caecal microbiome composition of broilers and free-range slow-growing chickens throughout their productive lifespan. Sci Rep 9(1):2506. https://doi.org/10.1038/s41598-019-39323-x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • O'Hara AM, O'Regan P, Fanning Á, O'Mahony C, MacSharry J, Lyons A, Bienenstock J, O'Mahony L, Shanahan F (2006) Functional modulation of human intestinal epithelial cell responses by Bifidobacterium infantis and Lactobacillus salivarius. Immunology 118(2):202–215. https://doi.org/10.1111/j.1365-2567.2006.02358.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Park JW, Jeong JS, Lee SI, Kim IH (2016) Effect of dietary supplementation with a probiotic (Enterococcus faecium) on production performance, excreta microflora, ammonia emission, and nutrient utilization in ISA brown laying hens. Poult Sci 95(12):2829–2835

    CAS  PubMed  Google Scholar 

  • Penha Filho RAC, Díaz SJA, Fernando FS, Chang Y-F, Andreatti Filho RL, Berchieri Junior A (2015) Immunomodulatory activity and control of Salmonella Enteritidis colonization in the intestinal tract of chickens by Lactobacillus based probiotic. Vet Immunol Immunopathol 167(1):64–69. https://doi.org/10.1016/j.vetimm.2015.06.006

    Article  CAS  PubMed  Google Scholar 

  • Pourabedin M, Xu Z, Baurhoo B, Chevaux E, Zhao X (2014) Effects of mannan oligosaccharide and virginiamycin on the cecal microbial community and intestinal morphology of chickens raised under suboptimal conditions. Can J Microbiol 60(5):255–266. https://doi.org/10.1139/cjm-2013-0899

    Article  CAS  PubMed  Google Scholar 

  • Robert C, Bernalier-Donadille A (2003) The cellulolytic microflora of the human colon: evidence of microcrystalline cellulose-degrading bacteria in methane-excreting subjects. FEMS Microbiol Ecol 46(1):81–89

    CAS  PubMed  Google Scholar 

  • Savignac HM, Kiely B, Dinan TG, Cryan JF (2014) Bifidobacteria exert strain-specific effects on stress-related behavior and physiology in BALB/c mice. Neurogastroenterol Motil 26(11):1615–1627

    CAS  PubMed  Google Scholar 

  • Shang HM, Hu TM, Lu YJ, Wu HX (2010) Effects of inulin on performance, egg quality, gut microflora and serum and yolk cholesterol in laying hens. Br Poult Sci 51(6):791–796. https://doi.org/10.1080/00071668.2010.531005

    Article  CAS  PubMed  Google Scholar 

  • Shini S, Shini A, Blackall PJ (2013) The potential for probiotics to prevent reproductive tract lesions in free-range laying hens. Anim Prod Sci 53(12):1298–1308. https://doi.org/10.1071/AN12337

    Article  Google Scholar 

  • Sommer F, Anderson JM, Bharti R, Raes J, Rosenstiel P (2017) The resilience of the intestinal microbiota influences health and disease. Nat Rev Microbiol 15:630–638. https://doi.org/10.1038/nrmicro.2017.58

    Article  CAS  PubMed  Google Scholar 

  • Spinler JK, Taweechotipatr M, Rognerud CL, Ou CN, Tumwasorn S, Versalovic J (2008) Human-derived probiotic Lactobacillus reuteri demonstrate antimicrobial activities targeting diverse enteric bacterial pathogens. Anaerobe 14(3):166–171. https://doi.org/10.1016/j.anaerobe.2008.02.001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stanley D, Denman SE, Hughes RJ, Geier MS, Crowley TM, Chen H, Haring VR, Moore RJ (2012) Intestinal microbiota associated with differential feed conversion efficiency in chickens. Appl Microbiol Biotechnol 96(5):1361–1369

    CAS  PubMed  Google Scholar 

  • Stappenbeck TS, Hooper LV, Gordon JI (2002) Developmental regulation of intestinal angiogenesis by indigenous microbes via Paneth cells. Proc Natl Acad Sci U S A 99(24):15451–15455

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tang SGH, Sieo CC, Ramasamy K, Saad WZ, Wong HK, Ho YW (2017) Performance, biochemical and haematological responses, and relative organ weights of laying hens fed diets supplemented with prebiotic, probiotic and synbiotic. BMC Vet Res 13(1):248

    PubMed  PubMed Central  Google Scholar 

  • Treem WR, Ahsan N, Shoup M, Hyams JS (1994) Fecal short-chain fatty acids in children with inflammatory bowel disease. J Pediatr Gastroenterol Nutr 18(2):159–164

    CAS  PubMed  Google Scholar 

  • Van Coillie E, Goris J, Cleenwerck I, Grijspeerdt K, Botteldoorn N, Van Immerseel F, De Buck J, Vancanneyt M, Swings J, Herman L, Heyndrickx M (2007) Identification of Lactobacilli isolated from the cloaca and vagina of laying hens and characterization for potential use as probiotics to control Salmonella Enteritidis. J Appl Microbiol 102(4):1095–1106. https://doi.org/10.1111/j.1365-2672.2006.03164.x

    Article  CAS  PubMed  Google Scholar 

  • Videnska P, Sedlar K, Lukac M, Faldynova M, Gerzova L, Cejkova D, Sisak F, Rychlik I (2014) Succession and replacement of bacterial populations in the caecum of egg laying hens over their whole life. PLoS One 9(12):e115142

    PubMed  PubMed Central  Google Scholar 

  • Vinolo MA, Rodrigues HG, Hatanaka E, Sato FT, Sampaio SC, Curi R (2011) Suppressive effect of short-chain fatty acids on production of proinflammatory mediators by neutrophils. J Nutr Biochem 22(9):849–855

    CAS  PubMed  Google Scholar 

  • Volf J, Polansky O, Varmuzova K, Gerzova L, Sekelova Z, Faldynova M, Babak V, Medvecky M, Smith AL, Kaspers B (2016) Transient and prolonged response of chicken cecum mucosa to colonization with different gut microbiota. PLoS One 11(9):e0163932

    PubMed  PubMed Central  Google Scholar 

  • Vollenweider S, Evers S, Zurbriggen K, Lacroix C (2010) Unraveling the hydroxypropionaldehyde (HPA) system: an active antimicrobial agent against human pathogens. J Agric Food Chem 58(19):10315–10322

    CAS  PubMed  Google Scholar 

  • Williams Smith H, Tucker JF (1980) The virulence of Salmonella strains for chickens: their excretion by infected chickens. J Hyg (Lond) 84(3):479–488

    CAS  Google Scholar 

  • Zakrzewski M, Proietti C, Ellis JJ, Hasan S, Brion M-J, Berger B, Krause L (2016) Calypso: a user-friendly web-server for mining and visualizing microbiome–environment interactions. Bioinformatics 33(5):782–783

    PubMed Central  Google Scholar 

  • Zhang ZF, Kim IH (2013) Effects of probiotic supplementation in different energy and nutrient density diets on performance, egg quality, excreta microflora, excreta noxious gas emission, and serum cholesterol concentrations in laying hens. J Anim Sci 91(10):4781–4787

    CAS  PubMed  Google Scholar 

  • Zhang JL, Xie QM, Ji J, Yang WH, Wu YB, Li C, Ma JY, Bi YZ (2012) Different combinations of probiotics improve the production performance, egg quality, and immune response of layer hens. Poult Sci 91(11):2755–2760

    CAS  PubMed  Google Scholar 

  • Zhang J, Kobert K, Flouri T, Stamatakis A (2013) PEAR: a fast and accurate Illumina Paired-End reAd mergeR. Bioinformatics 30(5):614–620

    PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

Help in sample collection from Nitish Narendra Joat (The University of Adelaide) is acknowledged. Critical editorial comments on the manuscript by Juliet Roberts (University of New England, Australia) are highly acknowledged.

Funding

This study was financially supported by the Australian Eggs Limited under grant number 1FS802UA to Kapil K. Chousalkar. The funding body was not involved in the collection, analysis and interpretation of the data or writing of the manuscript.

Author information

Authors and Affiliations

Authors

Contributions

K.K.C. developed the hypothesis and designed the experimental work. S.K. and K.K.C. performed the experimental work, analysed the data and wrote the manuscript. Both the authors reviewed and approved the manuscript for publication.

Corresponding author

Correspondence to Kapil K. Chousalkar.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest

Ethics statement

The Animal Ethics Committee at the University of Adelaide approved the work (approval number S-2017-080) in accordance with the guidelines specified in “Australian code for the care and use of animals for scientific purposes, 8th edition (2013).” Standard Operative Procedures were followed for caring and processing of the experimental chicks.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

ESM 1

(PDF 1156 kb).

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Khan, S., Chousalkar, K.K. Short-term feeding of probiotics and synbiotics modulates caecal microbiota during Salmonella Typhimurium infection but does not reduce shedding and invasion in chickens. Appl Microbiol Biotechnol 104, 319–334 (2020). https://doi.org/10.1007/s00253-019-10220-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-019-10220-7

Keywords

Navigation