Generic placeholder image

Current Protein & Peptide Science


ISSN (Print): 1389-2037
ISSN (Online): 1875-5550

Review Article

Influence of Probiotics on Dietary Protein Digestion and Utilization in the Gastrointestinal Tract

Author(s): Jing Wang and Haifeng Ji*

Volume 20, Issue 2, 2019

Page: [125 - 131] Pages: 7

DOI: 10.2174/1389203719666180517100339

Price: $65


Protein is essential to growth and metabolism. Many factors influence dietary protein digestion and utilization in the gastrointestinal tract. Probiotics have attracted increasing attention in recent years owing to their broad health benefits, which may include a positive influence on the digestion and utilization of proteins. Several observations support their potential role in protein digestion. For example, probiotics can regulate the intestinal microflora and thereby influence intestinal bacteria related to proteolysis. Probiotics can also induce host digestive protease and peptidase activity, and some can release exoenzymes involved in the digestion of proteins. In addition, probiotics can improve the absorption of small peptides and amino acids by improving the absorption ability of the epithelium and enhancing transport. Furthermore, probiotics can reduce harmful protein fermentation and thus decrease the toxicity of metabolites. In this review, the roles of probiotics in intestinal protein digestion and utilization and the potential mechanisms underlying these effects are discussed.

Keywords: Probiotic, protein, digestion, microflora, absorption, fermentation.

Graphical Abstract
Whitney, E.N.; Rolfes, S.R. Understanding Nutrition 14th ed.; Wadsworth, Cengage Learning, Belmont, ; , 2015.
Amara, A.A.; Shibl, A. Role of probiotics in health improvement, infection control and disease treatment and management. Saudi Pharm. J., 2015, 23, 107-114.
Kim, H.B.; Borewicz, K.; White, B.A.; Singer, R.S.; Sreevatsan, S. Tu, Z.J Isaacson, R.E. Microbial shifts in the swine distal gut in response to the treatment with antimicrobial growth promoter, tylosin. Proc. Natl. Acad. Sci. USA, 2012, 109, 15485-15490.
Yatsunenko, T.; Rey, F.E.; Manary, M.J.; Trehan, I.; Dominguez-Bello, M.G.; Contreras, M.; Magris, M.; Hidalgo, G.; Baldassano, R.N.; Anokhin, A.P.; Heath, A.C.; Warner, B.; Reeder, J.; Kuczynski, J.; Caporaso, J.G.; Lozupone, C.A.; Lauber, C.; Clemente, J.C.; Knights, D.; Knight, R.; Gordon, J.I. Human gut microbiome viewed across age and geography. Nature, 2012, 486, 222-227.
Sonnenburg, J.L.; Angenent, L.T.; Gordon, J.I. Getting a grip on things: How do communities of bacterial symbionts become established in our intestine? Nat. Immunol., 2004, 5, 569-573.
Bäckhed, F.; Ley, R.E.; Sonnenburg, J.L.; Peterson, D.A.; Gordon, J.I. Host bacterial mutualism in the human intestine. Science, 2005, 307, 1915-1920.
Human Microbiome Project Consortium. Structure, function and diversity of the healthy human microbiome. Nature, 2012, 486, 207-214.
Khadidja, B.; Salima, R.; Halima, Z.K.; Eddine, K.N. Specific aminopeptidases of indigenous Lactobacillus brevis and Lactobacillus plantarum. Afr. J. Biotechnol., 2012, 11, 15438-15445.
Schuchert-Shi, A.; Hauser, P.C. Peptic and tryptic digestion of peptides and proteins monitored by capillary electrophoresis with contactless conductivity detection. Anal. Biochem., 2009, 387, 202-207.
Rastall, R.A. Bacteria in the gut: Friends and foes and how to alter the balance. J. Nutr., 2004, 134, 2022S-2026S.
Hooper, L.V.; Midtvedt, T.; Gordon, J.I. How host microbial interactions shape the nutrient environment of the mammalian intestine. Annu. Rev. Nutr., 2002, 22, 283-307.
Resta, S.C. Effects of probiotics and commensals on intestinal epithelial physiology: implications for nutrient handling. J. Physiol., 2009, 587, 4169-4174.
Bergen, W.G.; Wu, G. Intestinal nitrogen recycling and utilization in health and disease. J. Nutr., 2009, 139, 821-825.
de Moreno de LeBlanc, A. LeBlanc, J.G Effect of probiotic administration on the intestinal microbiota, current knowledge and potential applications. World J. Gastroenterol., 2014, 20, 16518- 16528. .
Hill, C.; Guarner, F.; Reid, G.; Gibson, G.R.; Merenstein, D.J.; Pot, B.; Morelli, L.; Canani, R.B.; Flint, H.J.; Salminen, S.; Calder, P.C.; Sanders, M.E. The international scientific association for probiotics and prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nat. Rev. Gastroenterol. Hepatol., 2014, 11, 506-514.
Champagne, C.P.; Ross, R.P.; Saarela, M.; Hansen, K.F.; Charalampopoulos, D. Recommendations for the viability assessment of probiotics as concentrated cultures and in food matrices. Int. J. Food Microbiol., 2011, 149, 185-193.
Cammarota, M.; De Rosa, M.; Stellavato, A.; Lamberti, M.; Marzaioli, I.; Giuliano, M. In vitro evaluation of Lactobacillus plantarum DSMZ 12028 as a probiotic: emphasis on innate immunity. Int. J. Food Microbiol., 2009, 135, 90-98.
Fooks, L.J.; Fuller, R.; Gibson, G.R. Prebiotics, probiotics and human gut microbiology. Int. Dairy J., 1999, 9, 53-61.
Cotter, P.D.; Hill, C.; Ross, R.P. Bacteriocins: Developing innate immunity for food. Nat. Rev. Microbiol., 2005, 3, 777-788.
Servin, A.L. Antagonistic activities of lactobacilli and bifidobacteria against microbial pathogens. FEMS Microbiol. Rev., 2004, 28, 405-440.
Rychen, G.; Nunes, C.S. Effects of 3 microbial probiotics on postprandial porto-arterial concentration differences of glucose, galactose and aminonitrogen in the young pig. Br. J. Nutr., 1995, 74, 19-26.
De Preter, V.; Geboes, K.; Verbrugghe, K.; De Vuyst, L.; Vanhoutte, T.; Huys, G.; Swings, J.; Pot, B.; Verbeke, K. The in vivo use of the stable isotope-labelled biomarkers lactose-[15N]ureide and [2H4]tyrosine to assess the effects of pro- and prebiotics on the intestinal flora of healthy human volunteers. Br. J. Nutr., 2004, 92, 439-446.
Huang, C.H.; Qiao, S.Y.; Li, D.F.; Piao, X.S.; Ren, J.P. Effects of Lactobacilli on the performance, diarrhea incidence, VFA concentration and gastrointestinal microbial flora of weanling pigs. Asian-Austr. J. Anim. Sci., 2004, 17, 401-409.
Keller, D.; Van Dinter, R.; Cash, H.; Farmer, S.; Venema, K. Bacillus coagulans GBI-30, 6086 increases plant protein digestion in a dynamic, computer-controlled in vitro model of the small intestine (TIM-1). Benef. Microbes, 2017, 8, 491-496.
Zhang, R.; Zhou, M.; Tu, Y.; Zhang, N.F.; Deng, K.D.; Ma, T.; Diao, Q.Y. Effect of oral administration of probiotics on growth performance, apparent nutrient digestibility and stress related indicators in Holstein calves. J. Anim. Physiol. Anim. Nutr. , 2006, 100, 33-38.
Cai, L.; Indrakumar, S.; Kiarie, E.; Kim, I.H. Effects of a multistrain Bacillus species-based direct-fed microbial on growth performance, nutrient digestibility, blood profile, and gut health in nursery pigs fed corn-soybean meal-based diets. J. Anim. Sci., 2015, 93, 4336-4342
Ranganathan, N.; Ranganathan, P.; Friedman, E.A.; Joseph, A.; Delano, B.; Goldfarb, D.S.; Tam, P.; Rao, A.V.; Anteyi, E.; Musso, C.G. Pilot study of probiotic dietary supplementation for promoting healthy kidney function in patients with chronic kidney disease. Adv. Ther., 2010, 27, 634-647.
Kohn, R.A.; Dinneen, M.M.; Russek-Cohen, E. Using blood urea nitrogen to predict nitrogen excretion and efficiency of nitrogen utilization in cattle, sheep, goats, horses, pigs, and rats. J. Anim. Sci., 2005, 83, 879-889.
Apgar, G.A.; Kornegay, E.T.; Lindemann, M.D.; Wood, C.M. The effect of feeding various levels of Bifidobacterium-Globosum-A on the performance, gastrointestinal measurements, and immunity of weanling pigs and on the performance and carcass measurements of growing-finishing pigs. J. Anim. Sci., 1993, 71, 2173-2179.
Maukonen, J., Saarela, M. In: Human gut microbiota: does diet matter? In: Conference on ‘Diet, gut microbiology and human health’, London, England, December 11-12, 2013; Janice, E., Eds.; Proceeding of the nutrition society: Aberdeen, UK, 2015; pp. 23- 36.
Shadnoush, M.; Hosseini, R.S.; Khalilnezhad, A.; Navai, L.; Goudarzi, H.; Vaezjalali, M. Effects of probiotics on gut microbiota in patients with inflammatory bowel disease: A double-blind, placebo-controlled clinical trial. Korean J. Gastroenterol., 2015, 65, 215-221.
Blackburn, T.H.; Hobson, P.N. Further studies on the isolation of proteolytic bacteria from the sheep rumen. J. Gen. Microbiol., 1962, 29, 69-81.
Geoffrey, P.H.; Colin, G.O.; Yvonne, G.; Margaret, E.B. Isolation of proteolytic rumen bacteria by use of selective medium containing leaf fraction 1 protein (ribulosebisphosphate carboxylase). Appl. Environ. Microbiol., 1983, 45, 1780-1784.
Xing, Z.; Tang, W.; Geng, W.; Zheng, Y.; Wang, Y. In vitro and in vivo evaluation of the probiotic attributes of Lactobacillus kefiranofaciens XL10 isolated from Tibetan kefir grain. Appl. Microbiol. Biotechnol., 2017, 101, 2467-2477.
Ray, A.K.; Ghosh, K.; Ringø, E. Enzyme-producing bacteria isolated from fish gut: A review. Aquacult. Nutr., 2012, 18, 465-492.
Dawood, M.A.; Koshio, S.; Ishikawa, M.; El-Sabagh, M.; Esteban, M.A.; Zaineldin, A.I. Probiotics as an environment-friendly approach to enhance red sea bream, Pagrus major growth, immune response and oxidative status. Fish Shellfish Immunol., 2016, 57, 170-178.
Bertschinger, H.U.; Eggenberger, E.; Jucker, H.; Pfirter, H.P. Evaluation of low nutrient, high fibre diets for the prevention of porcine Escherichia coli enterotoxaemia. Vet. Microbiol., 1979, 3, 281-290.
Rist, V.T.; Weiss, E.; Sauer, N.; Mosenthin, R.; Eklund, M. Effect of dietary protein supply originating from soybean meal or casein on the intestinal microbiota of piglets. Anaerobe, 2014, 25, 72-79.
Heo, J.M.; Kim, J.C.; Hansen, C.F.; Mullan, B.P.; Hampson, D.J.; Pluske, J.R. Effects of feeding low protein diets to piglets on plasma urea nitrogen, faecal ammonia nitrogen, the incidence of diarrhea and performance after weaning. Arch. Anim. Nutr., 2008, 62, 343-358.
Mackie, R.I.; Stroot, P.G.; Varel, V.H. Biochemical identification and biological origin of key odor components in livestock waste. J. Anim. Sci., 1998, 76, 1331-1342.
Blachier, F.; Mariotti, F.; Huneau, J.F.; Tome, D. Effects of amino acid-derived luminal metabolites on the colonic epithelium and physiopathological consequences. Amino Acids, 2007, 33, 547-562.
Long, C.L.; Jeevanandam, M.; Kinney, T.D. Metabolism and recycling of urea in man. Am. J. Clin. Nutr., 1978, 31, 1367-1382.
Ushakova, N.A.; Nekrasovb, R.V.; Pravdinc, I.V.; Sverchkovad, N.V.; Kolomiyetsd, E.I.; Pavlova, D.S. Mechanisms of the effects of probiotics on symbiotic digestion. Biol. Bull., 2015, 42, 394-400.
De Preter, V.; Vanhoutte, T.; Huys, G.; Swings, J.; De Vuyst, L.; Rutgeerts, P.; Verbeke, K. Effects of Lactobacillus casei Shirota, Bifidobacterium breve, and oligofructose-enriched inulin on colonic nitrogen- protein metabolism in healthy humans. Am. J. Physiol. Gastrointest. Liver Physiol., 2007, 292, G358-G368.
Suzer, C.; Çoban, D.; Kamaci, H.O.; Saka, Ş.; Firat, K.; Otgucuoğlu, Ö.; Küçüksari, H. Lactobacillus spp. bacteria as probiotics in gilthead sea bream (Sparus aurata, L.) larvae: effects on growth performance and digestive enzyme activities. Aquaculture, 2008, 280, 140-145.
Iehata, S.; Inagaki, T.; Okunishi, S.; Nakano, M.; Tanaka, R.; Maeda, H. Colonization and probiotic effects of lactic acid bacteria in the gut of abalone Haliotis gigantea. Fish. Sci., 2009, 75, 1285-1293.
Tovar-Ramírez, D.; Zambonino, J.; Cahu, C.; Gatesoupe, F.J.; Vázquez-Juárez, R.; Lésel, R. Effect of live yeast incorporation in compound diet on digestive enzyme activity in sea bass (Dicentrarchus labrax) larvae. Aquaculture, 2002, 204, 113-123.
Askarian, F.; Kousha, A.; Salma, W.; Ringø, E. The effect of lactic acid bacteria administration on growth, digestive enzymes activity and gut microbiota in Persian sturgeon (Acipenser persicus) and beluga (Huso huso) fry. Aquacult. Nutr., 2011, 17, 488-497.
Liu, H.; Wang, S.; Cai, Y.; Guo, X.; Cao, Z.; Zhang, Y.; Liu, S.; Yuan, W.; Zhu, W.; Zheng, Y.; Xie, Z.; Guo, W.; Zhou, Y. Dietary administration of Bacillus subtilis HAINUP40 enhances growth, digestive enzyme activities, innate immune responses and disease resistance of tilapia, Oreochromis niloticus. Fish Shellfish Immunol., 2017, 60, 326-333.
Martin, L.; Pieper, R.; Kröger, S.; Goodarzi, B.F.; Vahjen, W.; Neumann, K.; Van Kessel, A.G.; Zentek, J. Influence of age and Enterococcus faecium NCIMB 10415 on development of small intestinal digestive physiology in piglets. Anim. Feed Sci. Tech., 2012, 175, 65-75.
Macedo, A.C.; Tavares, T.G.; Malcata, F.X. Purification and characterization of an intracellular aminopeptidase from a wild strain of Lactobacillus plantarum isolated from traditional Serra da Estrela cheese. Enzyme Microb. Technol., 2003, 32, 41-48.
Pastar, I.; Tonic, I.; Golic, N.; Kojic, M.; van Kranenburg, R.; Kleerebezem, M.; Topisirovic, L.; Jovanovic, G. Identification and genetic characterization of a novel proteinase, PrtR, from the human isolate Lactobacillus rhamnosus BGT10. Appl. Environ. Microbiol., 2003, 69, 5802-5811.
Pugsley, A.P.; Schwartz, M. Export and secretion of proteins by bacteria. FEMS Microbiol. Lett., 1985, 32, 3-38.
Wang, Y.; Gu, Q. Effect of probiotic on growth performance and digestive enzyme activity of Arbor Acres broilers. Res. Vet. Sci., 2010, 89, 163-167.
Konings, W.N. The cell membrane and the struggle for life of lactic acid bacteria. AntonieVan Leeuwenhoek, 2002, 82, 3-27.
Law, J.; Haandrikman, A. Proteolytic enzymes of lactic acid bacteria. Int. Dairy J., 1997, 7, 1-11.
Bron, P.A.; Kleerebezem, M.; Brummer, R.J.; Cani, P.D.; Mercenier, A.; MacDonald, T.T.; Garcia-Ródenas, C.L.; Wells, J.M. Can probiotics modulate human disease by impacting intestinal barrier function?Br. J. Nutr., 2017, 117, 93-107,
Karczewski, J.; Troost, F.J.; Konings, I.; Dekker, J.; Kleerebezem, M.; Brummer, R.J.; Wells, J.M. Regulation of human epithelial tight junction proteins by Lactobacillus plantarum in vivo and protective effects on the epithelial barrier. Am. J. Physiol. Gastrointest. Liver Physiol., 2010, 298, 851-859.
Standen, B.T.; Rodiles, A.; Peggs, D.L.; Davies, S.J.; Santos, G.A.; Merrifield, D.L. Modulation of the intestinal microbiota and morphology of tilapia, Oreochromis niloticus, following the application of a multi-species probiotic. Appl. Microbiol. Biotechnol., 2015, 99, 8403-8417.
Kleessen, B.; Hartmann, L.; Blaut, M. Fructans in the diet cause alterations of intestinal mucosal architecture, released mucins and mucosa-associated bifidobacteria in gnotobiotic rats. Br. J. Nutr., 2003, 89, 597-606.
Hague, A.; Butt, A.J.; Paraskeva, C. The role of butyrate in human colonic epithelial cells: An energy source or inducer of differentiation and apoptosis? Proc. Nutr. Soc., 1996, 55, 937-943.
Singh, B.; Halestrap, A.P.; Paraskeva, C. Butyrate can act as a stimulator of growth or inducer of apoptosis in human colonic epithelial cell lines depending on the presence of alternative energy sources. Carcinogenesis, 1997, 18, 1265-1270.
Daniel, H. Molecular and integrative physiology of intestinal peptide transport. Annu. Rev. Physiol., 2004, 66, 361-384.
Chen, H.Q.; Shen, T.Y.; Zhou, Y.K.; Zhang, M.; Chu, Z.X.; Hang, X.M.; Qin, H.L. Lactobacillus plantarum consumption increases PepT1-mediated amino acid absorption by enhancing protein kinase C activity in spontaneously colitic mice. J. Nutr., 2010, 140, 2201-2206
Neudeck, B.L.; Loeb, J.M.; Faith, N.G. Lactobacillus casei alters hPEPT1- mediated glycylsarcosine uptake in Caco-2 cells. J. Nutr., 2004, 134, 1120-1123.
Wenzel, U.; Meissner, B.; Doring, F.; Daniel, H. PEPT1-mediated uptake of dipeptides enhances the intestinal absorption of amino acids via transport system b(0,+). J. Cell. Physiol., 2001, 186, 251-259.
Fernandez-Alarcon, M.F.; Trottier, N.; Steibel, J.P.; Lunedo, R.; Campos, D.M.; Santana, A.M.; Pizauro, J.M., Jr; Furlan, R.L.; Furlan, L.R. Interference of age and supplementation of direct-fed microbial and essential oil in the activity of digestive enzymes and expression of genes related to transport and digestion of carbohydrates and proteins in the small intestine of broilers.Poult. Sci., 2017, 96, 2920-2930. ,
Venema, K. Role of gut microbiota in the control of energy and carbohydrate metabolism. Curr. Opin. Clin. Nutr. Metab. Care, 2010, 13, 432-438.
Walter, J.; Ley, R. The human gut microbiome: ecology and recent evolutionary changes. Annu. Rev. Microbiol., 2011, 65, 411-429.
Nyangale, E.P.; Mottram, D.S.; Gibson, G.R. Gut microbial activity, implications for health and disease: The potential role of metabolite analysis. J. Proteome Res., 2012, 11, 5573-5585.
Macfarlane, G.T.; Macfarlane, S. Bacteria, colonic fermentation, and gastrointestinal health. J. AOAC Int., 2012, 95, 50-60.
Windey, K.; De Preter, V.; Verbeke, K. Relevance of protein fermentation to gut health. Mol. Nutr. Food Res., 2012, 56, 184-196.
Jantchou, P.; Morois, S.; Clavel-Chapelon, F.; Boutron-Ruault, M.C.; Carbonnel, F. Animal protein intake and risk of inflammatory bowel disease: The E3N prospective study. Am. J. Gastroenterol., 2010, 105, 2195-2201.
Gill, C.I.; Rowland, I.R. Diet and cancer: Assessing the risk. Br. J. Nutr., 2002, 88, S73-S87.
Ma, N.; Tian, Y.; Wu, Y.; Ma, X. Contributions of the interaction between dietary protein and gut microbiota to intestinal health. Curr. Protein Pept. Sci., 2017, 18, 795-808.
Bansal, T.; Alaniz, R.C.; Wood, T.K.; Jayaraman, A. The bacterial signal indole increases epithelial-cell tight-junction resistance and attenuates indicators of inflammation. Proc. Natl. Acad. Sci. USA, 2010, 107, 228-233.
Fan, P.; Song, P.; Li, L.; Huang, C.; Chen, J.; Yang, W.; Qiao, S.; Wu, G.; Zhang, G.; Ma, X. Roles of biogenic amines in intestinal signaling. Curr. Protein Pept. Sci., 2017, 18, 532-540.
Sharma, P.; Sharma, B.C.; Puri, V.; Sarin, S.K. An open-label randomized controlled trial of lactulose and probiotics in the treatment of minimal hepatic encephalopathy. Eur. J. Gastroenterol. Hepatol., 2008, 20, 506-511.
Forsyth, C.B.; Farhadi, A.; Jakate, S.M.; Tang, Y.; Shaikh, M.; Keshavarzian, A. Lactobacillus GG treatment ameliorates alcohol-induced intestinal oxidative stress, gut leakiness, and liver injury in a rat model of alcoholic steatohepatitis. Alcohol, 2009, 43, 163-172.
Ling, W.H.; Korpela, R.; Mykkänen, H.; Salminen, S.; Hänninen, O. Lactobacillus strain GG supplementation decreases colonic hydrolytic and reductive enzyme activities in healthy female adults. J. Nutr., 1994, 124, 18-23.
De Preter, V.; Coopmans, T.; Rutgeerts, P.; Verbeke, K. Influence of long-term administration of lactulose and Saccharomyces boulardii on the colonic generation of phenolic compounds in healthy human subjects. J. Am. Coll. Nutr., 2006, 25, 541-549.
Takayama, F.; Taki, K.; Niwa, T. Bifidobacterium in gastro-resistant seamless capsule reduces serum levels of indoxyl sulfate in patients on hemodialysis. Am. J. Kidney Dis., 2003, 41, S142-S145.
Ndagijimana, M.; Laghi, L.; Vitali, B.; Placucci, G. Brigidi, P. Guerzoni, M.E. Effect of a synbiotic food consumption on human gut metabolic profiles evaluated by (1)H nuclear magnetic resonance spectroscopy. Int. J. Food Microbiol., 2009, 134, 147-153.
Vitali, B.; Ndagijimana, M.; Cruciani, F.; Carnevali, P.; Candela, M.; Guerzoni, M.E.; Brigidi, P. Impact of a synbiotic food on the gut microbial ecology and metabolic profiles. BMC Microbiol., 2010, 10, 4.
Ranganathan, N.; Patel, B.; Ranganathan, P.; Marczely, J.; Dheer, R.; Chordia, T.; Dunn, S.R.; Friedman, E.A. Probiotic amelioration of azotemia in 5/6th nephrectomized Sprague-Dawley rats. Sci. World J., 2005, 24, 652-660.
Taki, K.; Takayamam, F.; Niwa, T. Beneficial effects of Bifidobacteria in a gastroresistant seamless capsule on hyperhomocysteinemia in hemodialysis patients. J. Ren. Nutr., 2005, 15, 77-80.
Meijers, B.K.; De Preter, V.; Verbeke, K.; Vanrenterghem, Y.; Evenepoel, P. p-Cresyl sulfate serum concentrations in haemodialysis patients are reduced by the prebiotic oligofructose-enriched inulin. Nephrol. Dial. Transplant., 2010, 25, 219-224.
De Preter, V.; Ghebretinsae, A.H.; Abrahantes, J.C.; Windey, K.; Rutgeerts, P.; Verbeke, K. Impact of the synbiotic combination of Lactobacillus casei shirota and oligofructose-enriched inulin on the fecal volatile metabolite profile in healthy subjects. Mol. Nutr. Food Res., 2011, 55, 714-722.

Rights & Permissions Print Export Cite as
© 2024 Bentham Science Publishers | Privacy Policy