DOI QR코드

DOI QR Code

Changes in Gut Microbial Community of Pig Feces in Response to Different Dietary Animal Protein Media

  • Jeong, Yujeong (Department of Applied Animal Science, College of Animal Life Science, Kangwon National University) ;
  • Park, Jongbin (Department of Animal Life Science, College of Animal Life Science, Kangwon National University) ;
  • Kim, Eun Bae (Department of Applied Animal Science, College of Animal Life Science, Kangwon National University)
  • Received : 2020.03.21
  • Accepted : 2020.05.28
  • Published : 2020.09.28

Abstract

Beef, pork, chicken and milk are considered representative protein sources in the human diet. Since the digestion of protein is important, the role of intestinal microflora is also important. Despite this, the pure effects of meat and milk intake on the microbiome are yet to be fully elucidated. To evaluate the effect of beef, pork, chicken and milk on intestinal microflora, we observed changes in the microbiome in response to different types of dietary animal proteins in vitro. Feces were collected from five 6-week-old pigs. The suspensions were pooled and inoculated into four different media containing beef, pork, chicken, or skim milk powder in distilled water. Changes in microbial communities were analyzed using 16S rRNA sequencing. The feces alone had the highest microbial alpha diversity. Among the treatment groups, beef showed the highest microbial diversity, followed by pork, chicken, and milk. The three dominant phyla were Proteobacteria, Firmicutes, and Bacteroidetes in all the groups. The most abundant genera in beef, pork, and chicken were Rummeliibacillus, Clostridium, and Phascolarctobacterium, whereas milk was enriched with Streptococcus, Lactobacillus, and Enterococcus. Aerobic bacteria decreased while anaerobic and facultative anaerobic bacteria increased in protein-rich nutrients. Functional gene groups were found to be over-represented in protein-rich nutrients. Our results provide baseline information for understanding the roles of dietary animal proteins in reshaping the gut microbiome. Furthermore, growth-promotion by specific species/genus may be used as a cultivation tool for uncultured gut microorganisms.

Keywords

References

  1. Pereira PM, Vicente AF. 2013. Meat nutritional composition and nutritive role in the human diet. Meat. Sci. 93: 586-592. https://doi.org/10.1016/j.meatsci.2012.09.018
  2. Alcantara JMA, Sanchez-Delgado G, Martinez-Tellez B, Labayen I, Ruiz JR. 2019. Impact of cow's milk intake on exercise performance and recovery of muscle function: a systematic review. J. Int. Soc. Sports. Nutr. 16: 22. https://doi.org/10.1186/s12970-019-0288-5
  3. Hess J, Slavin J. 2016. Defining "protein" foods. Nutr. Today 51: 117-120. https://doi.org/10.1097/NT.0000000000000157
  4. LeBlanc JG, Matar C, Valdez JC, LeBlanc J, Perdigon G. 2002. Immunomodulating effects of peptidic fractions issued from milk fermented with Lactobacillus helveticus. J. Dairy Sci. 85: 2733-2742. https://doi.org/10.3168/jds.S0022-0302(02)74360-9
  5. Fernandez M, Zuniga M. 2006. Amino acid catabolic pathways of lactic acid bacteria. Crit. Rev. Microbiol. 32: 155-183. https://doi.org/10.1080/10408410600880643
  6. Khalid NM, Marth EH. 1990. Proteolytic activity by strains of Lactobacillus plantarum and Lactobacillus casei. J. Dairy Sci. 73: 3068-3076. https://doi.org/10.3168/jds.S0022-0302(90)78994-1
  7. Jandhyala SM, Talukdar R, Subramanyam C, Vuyyuru H, Sasikala M, Nageshwar Reddy D. 2015. Role of the normal gut microbiota. World J. Gastroenterol. 21: 8787-8803. https://doi.org/10.3748/wjg.v21.i29.8787
  8. Clemente JC, Ursell LK, Parfrey LW, Knight R. 2012. The impact of the gut microbiota on human health: an integrative view. Cell 148: 1258-1270. https://doi.org/10.1016/j.cell.2012.01.035
  9. Lin L, Zhang J. 2017. Role of intestinal microbiota and metabolites on gut homeostasis and human diseases. BMC Immunol. 18: 2. https://doi.org/10.1186/s12865-016-0187-3
  10. Bibbo S, Ianiro G, Giorgio V, Scaldaferri F, Masucci L, Gasbarrini A, et al. 2016. The role of diet on gut microbiota composition. Eur. Rev. Med. Pharmacol. Sci. 20: 4742-4749.
  11. Zhang Z, Li D, Tang R. 2019. Changes in mouse gut microbial community in response to the different types of commonly consumed meat. Microorganisms 7: 76. https://doi.org/10.3390/microorganisms7030076
  12. Xue Z, Zhang J, Zhang R, Huang Z, Wan Q, Zhang Z. 2019. Comparative analysis of gut bacterial communities in housefly larvae fed different diets using a high-throughput sequencing approach. FEMS Microbiol. Lett. 366: fnz126.
  13. Zhu Y, Lin X, Zhao F, Shi X, Li H, Li Y, et al. 2015. Meat, dairy and plant proteins alter bacterial composition of rat gut bacteria. Sci. Rep. 5: 15220. https://doi.org/10.1038/srep15220
  14. Han GG, Lee JY, Jin GD, Park J, Choi YH, Chae BJ, et al. 2017. Evaluating the association between body weight and the intestinal microbiota of weaned piglets via 16S rRNA sequencing. Appl. Microbiol. Biotechnol. 101: 5903-5911. https://doi.org/10.1007/s00253-017-8304-7
  15. Lim J-S, Yang SH, Kim B-S, Lee EY. 2018. Comparison of microbial communities in swine manure at various temperatures and storage times. Asian-australas. J. Anim. Sci. 31: 1373. https://doi.org/10.5713/ajas.17.0704
  16. Costa A, Lopez-Villalobos N, Sneddon NW, Shalloo L, Franzoi M, De Marchi M, et al. 2019. Invited review: Milk lactose-current status and future challenges in dairy cattle. J. Dairy Sci. 102: 5883-5898. https://doi.org/10.3168/jds.2018-15955
  17. Ammar EM, Wang X, Rao CV. 2018. Regulation of metabolism in Escherichia coli during growth on mixtures of the non-glucose sugars: arabinose, lactose, and xylose. Sci. Rep. 8: 609. https://doi.org/10.1038/s41598-017-18704-0
  18. Bodini S, Nunziangeli L, Santori F. 2007. Influence of amino acids on low-density Escherichia coli responses to nutrient downshifts. J. Bacteriol. 189: 3099-3105. https://doi.org/10.1128/JB.01753-06
  19. Juers DH, Matthews BW, Huber RE. 2012. LacZ $\beta$‐galactosidase: structure and function of an enzyme of historical and molecular biological importance. Protein Sci. 21: 1792-1807 https://doi.org/10.1002/pro.2165
  20. Gao Z, Daliri EB, Wang J, Liu D, Chen S, Ye X, et al. 2019. Inhibitory effect of lactic acid bacteria on foodborne pathogens: a review. J. Food Prot. 82: 441-453. https://doi.org/10.4315/0362-028X.JFP-18-303
  21. Leclerc H, Mossel D, Edberg S, Struijk C. 2001. Advances in the bacteriology of the coliform group: their suitability as markers of microbial water safety. Annu. Rev. Microbiol. 55: 201-234. https://doi.org/10.1146/annurev.micro.55.1.201
  22. Lindberg A-M, Ljungh Å, Ahrne S, Löfdahl S, Molin G. 1998. Enterobacteriaceae found in high numbers in fish, minced meat and pasteurised milk or cream and the presence of toxin encoding genes. Int. J. Food Microbiol. 39: 11-17. https://doi.org/10.1016/S0168-1605(97)00104-9
  23. Dai Z-L, Wu G, Zhu W-Y. 2011. Amino acid metabolism in intestinal bacteria: links between gut ecology and host health. Front. Biosci. 16: 1768-1786. https://doi.org/10.2741/3820
  24. Byun R, Carlier JP, Jacques NA, Marchandin H, Hunter N. 2007. Veillonella denticariosi sp. nov., isolated from human carious dentine. Int. J. Syst. Evol. Microbiol. 57: 2844-2848. https://doi.org/10.1099/ijs.0.65096-0
  25. Sahlin K. 1986. Muscle fatigue and lactic acid accumulation. Acta Physiol. Scand. Suppl. 556: 83-91.
  26. Edman AC, Lexell J, Sjostrom M, Squire JM. 1988. Structural diversity in muscle fibres of chicken breast. Cell. Tissue Res. 251: 281-289. https://doi.org/10.1007/BF00215835
  27. Zhao J, Zhang X, Liu H, Brown MA, Qiao S. 2019. Dietary protein and gut microbiota composition and function. Curr. Protein Pept. Sci. 20: 145-154. https://doi.org/10.2174/1389203719666180514145437
  28. Stackebrandt E, Osawa R. 2015. Phascolarctobacterium. pp. 1-4. Bergey's Manual of Systematics of Archaea Bacteria.
  29. Wu F, Guo X, Zhang J, Zhang M, Ou Z, Peng YJE, et al. 2017. Phascolarctobacteriumáfaecium abundant colonization in human gastrointestinal tract. Exp. Ther. Med. 14: 3122-3126. https://doi.org/10.3892/etm.2017.4878
  30. Slobodkin A. 2014. The Family Peptostreptococcaceae, pp. 291-302. In: Rosenberg E., Delong EF, Lory S, Stackebrandt E, Thompson F (eds.), The Prokaryotes, Springer, Berlin, Heidelberg
  31. Li M, Li Y, Fan X, Qin Y, He Y, Lv Y. 2019. Draft genome sequence of Rummeliibacillus sp. strain TYF005, a physiologically recalcitrant bacterium with high ethanol and salt tolerance isolated from spoilage vinegar. Microbiol. Resour. Announc. 8: e00244-00219.
  32. Her J, Kim J. 2013. Rummeliibacillus suwonensis sp. nov., isolated from soil collected in a mountain area of South Korea. J. Microbiol. 51: 268-272. https://doi.org/10.1007/s12275-013-3126-5
  33. Junpadit P, Suksaroj TT, Boonsawang P. 2017. Transformation of palm oil mill effluent to terpolymer polyhydroxyalkanoate and biodiesel using Rummeliibacillus pycnus strain TS 8. Waste Biomass. Valor. 8: 1247-1256. https://doi.org/10.1007/s12649-016-9711-1
  34. Tan HY, Chen SW, Hu SY. 2019. Improvements in the growth performance, immunity, disease resistance, and gut microbiota by the probiotic Rummeliibacillus stabekisii in Nile tilapia (Oreochromis niloticus). Fish Shellfish Immunol. 92: 265-275. https://doi.org/10.1016/j.fsi.2019.06.027
  35. Shim Y, Kim J, Hosseindoust A, Ingale SL, Choi Y, Kim M J, et al. 2017. Effects of supplementation of multienzymes in diets containing different energy levels on growth performance, nutrient digestibility, blood metabolites, microbiota and intestinal morphology of broilers. Ann. Anim. Resour. Sci. 28: 97-107. https://doi.org/10.12718/AARS.2017.28.3.97
  36. Giraffa G. 2003. Functionality of enterococci in dairy products. Int. J. Food Microbiol. 88: 215-222. https://doi.org/10.1016/S0168-1605(03)00183-1
  37. Iyer R, Tomar S, Maheswari TU, Singh R. 2010. Streptococcus thermophilus strains: multifunctional lactic acid bacteria. Int. Dairy J. 20: 133-141. https://doi.org/10.1016/j.idairyj.2009.10.005
  38. Siegumfeldt H, Bjorn Rechinger K, Jakobsen M. 2000. Dynamic changes of intracellular pH in individual lactic acid bacterium cells in response to a rapid drop in extracellular pH. Appl. Environ. Microbiol. 66: 2330-2335. https://doi.org/10.1128/AEM.66.6.2330-2335.2000
  39. Rajagopal S, Sandine WJJods. 1990. Associative growth and proteolysis of Streptococcus thermophilus and Lactobacillus bulgaricus in skim milk. J. Dairy Sci. 73: 894-899. https://doi.org/10.3168/jds.S0022-0302(90)78745-0
  40. Akerstedt M, Wredle E, Lam V, Johansson M. 2012. Protein degradation in bovine milk caused by Streptococcus agalactiae. J. Dairy Res. 79: 297-303. https://doi.org/10.1017/S0022029912000301
  41. Krzysciak W, Pluskwa KK, Jurczak A, Koscielniak D. 2013. The pathogenicity of the Streptococcus genus. Eur. J. Clin. Microbiol. Infect. Dis. 32: 1361-1376. https://doi.org/10.1007/s10096-013-1914-9
  42. Giard JC, Laplace JM, Rincé A, Pichereau V, Benachour A, Leboeuf C, et al. 2001. The stress proteome of Enterococcus faecalis. Electrophoresis 22: 2947-2954. https://doi.org/10.1002/1522-2683(200108)22:14<2947::AID-ELPS2947>3.0.CO;2-K
  43. Madsen L, Myrmel LS, Fjære E, Liaset B, Kristiansen K. 2017. Links between dietary protein sources, the gut microbiota, and obesity. Front. Physiol. 8: 1047. https://doi.org/10.3389/fphys.2017.01047
  44. Yu J, Kroll JS. 1999. DsbA: A protein-folding catalyst contributing to bacterial virulence. Microbes Infect. 1: 1221-1228. https://doi.org/10.1016/S1286-4579(99)00239-7
  45. Smith EA, Macfarlane GT. 1997. Dissimilatory amino Acid metabolism in human colonic bacteria. Anaerobe 3: 327-337. https://doi.org/10.1006/anae.1997.0121
  46. de Vos WM, Vaughan EE. 1994. Genetics of lactose utilization in lactic acid bacteria. FEMS Microbiol. Rev. 15: 217-237. https://doi.org/10.1111/j.1574-6976.1994.tb00136.x
  47. Kubota H, Senda S, Nomura N, Tokuda H, Uchiyama H. 2008. Biofilm formation by lactic acid bacteria and resistance to environmental stress. J. Biosci. Bioeng. 106: 381-386. https://doi.org/10.1263/jbb.106.381
  48. Jefferson KK. 2004. What drives bacteria to produce a biofilm? FEMS Microbiol. Lett. 236: 163-173. https://doi.org/10.1111/j.1574-6968.2004.tb09643.x
  49. Olsen I. 2015. Biofilm-specific antibiotic tolerance and resistance. Eur. J. Clin. Microbiol. Infect. Dis. 34: 877-886. https://doi.org/10.1007/s10096-015-2323-z
  50. Donlan RM. 2002. Biofilms: microbial life on surfaces. Emerg. Infect. Dis. 8: 881-890. https://doi.org/10.3201/eid0809.020063
  51. Bacun-Druzina V, Mrvcic J, Butorac A, Gjuracic KJMczupipm. 2009. The influence of gene transfer on the lactic acid bacteria evolution. Mljekarstvo 59: 181-192.
  52. Parsek MR, Singh PK. 2003. Bacterial biofilms: an emerging link to disease pathogenesis. Annu. Rev. Microbiol. 57: 677-701. https://doi.org/10.1146/annurev.micro.57.030502.090720
  53. Davis BM, Waldor MK. 2002. Mobile genetic elements and bacterial pathogenesis, pp. 1040-1059. Mobile DNA II, Ed. American Society of Microbiology