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Comparative analysis of the ileal bacterial composition of post-weaned pigs fed different high-quality protein sources

Published online by Cambridge University Press:  06 February 2020

J. Ortman ,
S. M. Sinn ,
W. R. Gibbons ,
M. L. Brown ,
J. M. DeRouchey ,
B. St-Pierre ,
M. Saqui-Salces  and
C. L. Levesque
J. Ortman
Affiliation:
Department of Animal Science, South Dakota State University, PO Box 2170, Brookings, SD57007, USA
S. M. Sinn
Affiliation:
Department of Animal Science, South Dakota State University, PO Box 2170, Brookings, SD57007, USA
W. R. Gibbons
Affiliation:
Department of Biology and Microbiology, South Dakota State University, PO Box 2104, Brookings, SD57007, USA
M. L. Brown
Affiliation:
Department of Natural Resource Management, South Dakota State University, PO Box 2140, Brookings, SD57007, USA
J. M. DeRouchey
Affiliation:
Department of Animal Sciences and Industry, Kansas State University, 232 Weber Hall, Manhattan, KS66506, USA
B. St-Pierre
Affiliation:
Department of Animal Science, South Dakota State University, PO Box 2170, Brookings, SD57007, USA
M. Saqui-Salces
Affiliation:
Department of Animal Science, University of Minnesota, 1988 Fitch Avenue, St. Paul, MN55108, USA
C. L. Levesque*
Affiliation:
Department of Animal Science, South Dakota State University, PO Box 2170, Brookings, SD57007, USA
*
†E-mail: [email protected]
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Abstract

To further understand the contribution of feedstuff ingredients to gut health in swine, gut histology and intestinal bacterial profiles associated with the use of two high-quality protein sources, microbially enhanced soybean meal (MSBM) and Menhaden fishmeal (FM) were assessed. Weaned pigs were fed one of three experimental diets: (1) basic diet containing corn and soybean meal (Negative Control (NEG)), (2) basic diet + fishmeal (FM; Positive Control (POS)) and (3) basic diet + MSBM (MSBM). Phase I POS and MSBM diets (d 0 to d 7 post-wean) included FM or MSBM at 7.5%, while Phase II POS and MSBM diets (d 8 to d 21) included FM or MSBM at 5.0%. Gastrointestinal tissue and ileal digesta were collected from euthanised pigs at d 21 (eight pigs/diet) to assess gut histology and intestinal bacterial profiles, respectively. Data were analysed using Proc Mixed in SAS, with pig as the experimental unit and pig (treatment) as the random effect. Histological and immunohistochemical analyses of stomach and small intestinal tissue using haematoxylin–eosin, Periodic Acid Schiff/Alcian blue and inflammatory cell staining did not reveal detectable differences in host response to dietary treatment. Ileal bacterial composition profiles were obtained from next-generation sequencing of PCR generated amplicons targeting the V1 to V3 regions of the 16S rRNA gene. Lactobacillus-affiliated sequences were found to be the most highly represented across treatments, with an average relative abundance of 64.0%, 59.9% and 41.80% in samples from pigs fed the NEG, POS and MSBM diets, respectively. Accordingly, the three most abundant Operational Taxonomic Units (OTUs) were affiliated to Lactobacillus, showing a distinct abundance pattern relative to dietary treatment. One OTU (SD_Ssd_00001), most closely related to Lactobacillus amylovorus, was found to be more abundant in NEG and POS samples compared to MSBM (23.5% and 35.0% v. 9.2%). Another OTU (SD_Ssd_00002), closely related to Lactobacillus johnsonii, was more highly represented in POS and MSBM samples compared to NEG (14.0% and 15.8% v. 0.1%). Finally, OTU Sd_Ssd-00011, highest sequence identity to Lactobacillus delbrueckii, was found in highest abundance in ileal samples from MSBM-fed pigs (1.9% and 3.3% v. 11.3, in POS, NEG and MSBM, respectively). There was no effect of protein source on bacterial taxa to the genus level or diversity based on principal component analysis. Dietary protein source may provide opportunity to enhance presence of specific members of Lactobacillus genus that are associated with immune-modulating properties without altering overall intestinal bacterial diversity.

Keywords

intestinemicrobiomemicrobially enhanced soybean mealnursery pigprotein source
Type
Research Article
Information
animal , Volume 14 , Issue 6 , June 2020 , pp. 1156 - 1166
Copyright
© The Animal Consortium 2020

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Footnotes

a

Present address: 1221 S Kipley Avenue, Indianapolis, IN 46203, USA

References

Altschul, SF, Madden, TL, Schaffer, AA, Zhang, J, Zhang, Z, Miller, W and Lipman, DJ 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research 25, 3389–3402.CrossRefGoogle ScholarPubMed
Avall-Jaaskelainen, S and Palva, A 2005. Lactobacillus surface layers and their applications. FEMS Microbiology Reviews 29, 511–529.CrossRefGoogle ScholarPubMed
Aziz, RK, Bartels, D, Best, AA, DeJongh, M, Disz, T, Edwards, RA, Formsma, K, Gerdes, S, Glass, EM, Kubal, M, Meyer, F, Olsen, GJ, Olson, R, Osterman, AL, Overbeek, RA, McNeil, LK, Paarmann, D, Paczian, T, Parrello, B, Pusch, GD, Reich, C, Stevens, R, Vassieva, O, Vonstein, V, Wilke, A, Zagnitko, O (2008). The RAST Server: rapid annotations using subsystems technology. BMC Genomics 9, 75. doi:10.1186/1471-2164-9-75.CrossRefGoogle ScholarPubMed
Berrocoso, J, Serrano, M, Cámara, L, Rebollar, P and Mateos, G 2012. Influence of diet complexity on productive performance and nutrient digestibility of weanling pigs. Animal Feed Science and Technology 171, 214–222.CrossRefGoogle Scholar
Bian, G, Shouqing, M, Zhingang, Z, Su, Y, Zoetendal, EG, Mackie, R, Liu, J, Mu, C, Huang, R, Smidt, H and Zhu, W 2016. 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. Environmental Microbiology 15, 1566–1577.CrossRefGoogle Scholar
Bird, AR and Conlon, MA 2015. Obesity, diet and the gut microbiota. Current Nutrition Reports 4, 340–347.CrossRefGoogle Scholar
Blaut, M and Clavel, T 2007. Metabolic diversity of the intestinal microbiota: implications for health and disease. The Journal of Nutrition 137, 751S–755S.CrossRefGoogle ScholarPubMed
Campbell, JM, Crenshaw, JD and Polo, J 2013. The biological stress of early weaned piglets. Journal of Animal Science and Biotechnology 4, 19–23.CrossRefGoogle ScholarPubMed
Edwards, U, Rogall, T, Blöcker, H, Emde, M and Böttger, EC 1989. Isolation and direct complete nucleotide determination of entire genes. Characterization of a gene coding for 16S ribosomal RNA. Nucleic Acids Research 17, 7843–7853.CrossRefGoogle ScholarPubMed
Eisenhut, M, Ruth, W, Haimovich, M, Bauwe, H, Kaplan, A and Hagemann, M 2008. The photorespiratory glycolate metabolism is essential for cyanobacteria and might have been conveyed endosymbiontically to plants. PNAS 105, 17199–17204. doi:10.1073/pnas.0807043105.CrossRefGoogle ScholarPubMed
FAO 2014. The Status of fishery resources The State of world fisheries and Aquaculture, pp. 37–40. Food and Agriculture Organization on the United Nations, Rome, Italy.Google Scholar
Food and Drug Administration (FDA ) 2013. Guidance for Industry #209 The judicious use of medically important antimicrobial drugs in food-producing animals. Retrieved on 4 August 2018 from https://www.fda.gov/downloads/AnimalVeterinary/GuidanceComplianceEnforcement/GuidanceforIndustry/UCM216936.pdfGoogle Scholar
Friesen, KG, Goodband, RD, Nelssen, JL, Blecha, F, Reddy, DN, Reddy, PG and Kats, LJ 1993. The effect of pre- and postweaning exposure to soybean meal on growth performance and on the immune response in the early-weaned pig. Journal of Animal Science 71, 2089–2098.CrossRefGoogle ScholarPubMed
Fuller, R 1989. Probiotics in man and animals. Journal of Applied Microbiology 66, 365–378.Google ScholarPubMed
Government of Canada 2018. Responsible use of medically important antimicrobials in animals. Retrieved on 2 October 2018 from https://www.canada.ca/en/public-health/services/antibiotic-antimicrobial-resistance/animals/actions/responsible-use-antimicrobials.htmlGoogle Scholar
Gustavo Hermes, R, Molist, F, Francisco Perez, J, Gomez de Segura, A, Ywazaki, M, Davin, R, Nofrarias, M, Korhonen, TK, Virkola, R and Martin-Orue, SM 2013. Casein glycomacropeptide in the diet may reduce Escherichia coli attachment to the intestinal mucosa and increase the intestinal lactobacilli of early weaned piglets after an enterotoxigenic E. coli K88 challenge. British Journal of Nutrition 109, 1001–1012.CrossRefGoogle ScholarPubMed
Heinritz, SN, Weiss, E, Eklund, M, Aumiller, T, Louis, S, Rings, A, Messner, S, Camarinha-Silva, A, Seifert, J, Bischoff, SC and Mosenthin, R 2016. Intestinal microbiota and microbial metabolites are changed in a pig model fed a high-fat/low-fiber or a low-fat/high-fiber diet. PLoS One 11, e0154329.CrossRefGoogle ScholarPubMed
Hötzel, MJ, de Souza, GP, Dalla Costa, OA and Machado Filho, LCP 2011. Disentangling the effects of weaning stressors on piglets’ behaviour and feed intake: changing the housing and social environment. Applied Animal Behaviour Science 135, 44–50.CrossRefGoogle Scholar
Hynönen, U and Palva, A 2013. Lactobacillus surface layer proteins: structure, function and applications. Applied Microbiology and Biotechnology 97, 5225–5243.CrossRefGoogle ScholarPubMed
Kant, R, Blom, J, Palva, A, Siezen, RJ and de Vos, WM 2011. Comparative genomics of Lactobacillus. Microbial Biotechnology 4, 323–332.CrossRefGoogle ScholarPubMed
Kindon, H, Pothoulakis, C, Thim, L, Lynch-Devaney, K and Podolsky, DK 1995. Trefoil peptide protection of intestinal epithelial barrier function: cooperative interaction with mucin glycoprotein. Gastroenterology 109, 516–523.CrossRefGoogle ScholarPubMed
Kitazawa, H, Watanabe, H, Shimosato, T, Kawai, Y, Itoh, T and Saito, T 2003. Immunostimulatory oligonucleotide, CpG-like motif exists in Lactobacillus delbrueckii ssp. bulgaricus NIAI B6. International Journal of Food Microbiology 85, 11–21.CrossRefGoogle ScholarPubMed
Koepke, JR, Kaushik, RS, Gibbons, WR, Brown, M and Levesque, CL 2017. Evaluation of a bioprocessed soybean meal on nursery pig performance and immune status. Journal of Animal Science 95, 5030–5039.CrossRefGoogle ScholarPubMed
Lalles, J 1993. Soy products as protein sources for preruminants and young pigs. In Soy in animal nutrition (ed. Drackley, JK), pp. 106–125. Federation of Animal Science Societies, Savoy, IL, USA.Google Scholar
Lane, DJ, Pace, B, Olsen, GJ, Stahl, DA, Sogin, ML and Pace, NR 1985. Rapid determination of 16S ribosomal RNA sequences for phylogenetic analyses. Proceedings of the National Academy of Sciences 82, 6955–6959.CrossRefGoogle ScholarPubMed
Levesque, CL, Hooda, S, Swanson, KS and de Lange, K 2014. Alterations in ileal mucosa bacteria related to diet complexity and growth performance in young pigs. PLoS ONE 9, e108472.CrossRefGoogle ScholarPubMed
Makkink, CA, Megulescu, GP, Guixin, Q and Verstegen, MWA 1994. Effect of dietary protein source on feed intake, growth, pancreatic enzyme activities, and jejunal morphology in newly-weaned pigs. British Journal of Nutrition 72, 353–368.CrossRefGoogle Scholar
Morowitz, MJ, Carlisle, E and Alverdy, JC 2011. Contributions of intestinal bacteria to nutrition and metabolism in the critically ill. The Surgical Clinics of North America 91, 771–785.CrossRefGoogle ScholarPubMed
National Research Council (NRC) 2012. Nutrient requirements of swine, 11th revised edition. National Academies Press, Washington, DC, USA.Google Scholar
Nollet, H, Deprez, P, Van Driessche, E and Muylle, E 1999. Protection of just weaned pigs against infection with F18 + Escherichia coli by non-immune plasma powder. Veterinary Microbiology 65, 37–45.CrossRefGoogle ScholarPubMed
Omar, JM, Chan, Y-M, Jones, ML, Prakash, S and Jones, PJH 2013. Lactobacillus fermentum and Lactobacillus amylovorus as probiotics alter body adiposity and gut microflora in healthy persons. Journal of Functional Foods 5, 116–123.CrossRefGoogle Scholar
Pluske, JR, Hampson, DJ and Williams, IH 1997. Factors influencing the structure and function of the small intestine in the weaned pig: a review. Livestock Production Science 51, 215–236.CrossRefGoogle Scholar
Pridmore, RD, Berger, B, Desiere, F, Vilanova, D, Barretto, C, Pittet, AC, Zwahlen, MC, Rouvet, M, Altermann, E, Barrangou, R, Mollet, B, Mercenier, A, Klaenhammer, T, Arigoni, F and Schell, MA 2004. The genome sequence of the probiotic intestinal bacterium Lactobacillus johnsonii NCC 533. Proceedings of the National Academy of Science USA 101, 2512–2517.CrossRefGoogle ScholarPubMed
Quan, J, Cai, G, Ye, J, Yang, M, Ding, R, Wang, X, Zheng, E, Fu, D, Li, S and Zhou, S 2018. A global comparison of the microbiome compositions of three gut locations in commercial pigs with extreme feed conversion ratios. Scientific Reports 8, 4536.CrossRefGoogle ScholarPubMed
Schleifer, K and Ludwig, W 1995. Phylogenetic relationships of lactic acid bacteria. In The genera of lactic acid bacteria. The lactic acid bacteria (eds. Wood, BJB and Holzapfel, WH), pp. 7–18. Springer, Boston, MA, USA.CrossRefGoogle Scholar
Schloss, PD, Westcott, SL, Ryabin, T, Hall, JR, Hartmann, M, Hollister, EB, Lesniewski, RA, Oakley, BB, Parks, DH and Robinson, CJ 2009. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Applied and Environmental Microbiology 75, 7537–7541.CrossRefGoogle ScholarPubMed
Schwab, C and Ganzle, M 2011. Lactic acid bacteria fermentation of human milk oligosaccharide components, human milk oligosaccharides and galactooligosaccharides. FEMS Microbiology Letters 315, 141–148.CrossRefGoogle ScholarPubMed
Sillanpää, J, Martínez, B, Antikainen, J, Toba, T, Kalkkinen, N, Tankka, S, Lounatmaa, K, Keränen, J, Höök, M, Westerlund-Wikström, B, Pouwels, PH and Korhonen, TK 2000. Characterization of the collagen-binding S-layer protein CbsA of Lactobacillus crispatus. Journal of Bacteriology 182, 6440–6450.CrossRefGoogle ScholarPubMed
Sinn, S, Gibbons, W, Brown, M, DeRouchey, J and Levesque, C 2016. Evaluation of microbially enhanced soybean meal as an alternative to fishmeal in weaned pig diets. Animal 11, 1–10. doi:10.1017/S1751731116002020.Google ScholarPubMed
St-Pierre, B, Cersosimo, LM, Ishaq, SL and Wright, A-DG 2015. Toward the identification of methanogenic archaeal groups as targets of methane mitigation in livestock animals. Frontiers in Microbiology 6, 776.CrossRefGoogle Scholar
Taverniti, V, Stuknyte, M, Minuzzo, M, Arioli, S, De Noni, I, Scabiosi, C, Cordova, ZM, Junttila, I, Hamalainen, S, Turpeinen, H, Mora, D, Karp, M, Pesu, M and Guglielmetti, S 2013. S-layer protein mediates the stimulatory effect of Lactobacillus helveticus MIMLh5 on innate immunity. Applied and Environmental Microbiology 79, 1221–1231.CrossRefGoogle ScholarPubMed
Ventura, M, Jankovic, I, Walker, DC, Pridmore, RC and Zink, R 2002. Identification and characterization of novel surface proteins in Lactobacillus johnsonii and Lactobacillus gasseri. Applied and Environmental Microbiology 68, 6172–6181. doi:10.1128/AEM.68.12.6172-6181.2002.CrossRefGoogle ScholarPubMed
Wang, Q, Garrity, GM, Tiedje, JM and Cole, JR 2007. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Applied and Environmental Microbiology 73, 5261–5267.CrossRefGoogle ScholarPubMed
Wiyaporn, M, Thongsong, B and Kalandakanond-Thongsong, S 2013. Growth and small intestine histomorphology of low and normal birth weight piglets during the early suckling period. Livestock Science 158, 215–222.CrossRefGoogle Scholar
Xiao, Z and Xu, P 2007. Acetoin metabolism in bacteria. Critical Reviews in Microbiology 33, 127–140.CrossRefGoogle Scholar
Yuan, L, Chang, J, Yin, Q, Lu, M, Di, Y, Wang, P, Wang, Z, Wang, E and Lu, F 2016. Fermented soybean meal improves the growth performance, nutrient digestibility, and microbial flora in piglets. Animal Nutrition 3, 19–24.CrossRefGoogle ScholarPubMed
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