Effect of Dietary Protein and Processing on Gut Microbiota-A Systematic Review

Shujian Wu, Zuhaib F Bhat, Rochelle S Gounder, Isam A Mohamed Ahmed, Fahad Y Al-Juhaimi, Yu Ding, Alaa E-D A Bekhit, Shujian Wu, Zuhaib F Bhat, Rochelle S Gounder, Isam A Mohamed Ahmed, Fahad Y Al-Juhaimi, Yu Ding, Alaa E-D A Bekhit

Abstract

The effect of diet on the composition of gut microbiota and the consequent impact on disease risk have been of expanding interest. The present review focuses on current insights of changes associated with dietary protein-induced gut microbial populations and examines their potential roles in the metabolism, health, and disease of animals. Preferred Reporting Items for Systematic Reviews and Meta-Analysis (PRISMA) protocol was used, and 29 highly relevant articles were obtained, which included 6 mouse studies, 7 pig studies, 15 rat studies, and 1 in vitro study. Analysis of these studies indicated that several factors, such as protein source, protein content, dietary composition (such as carbohydrate content), glycation of protein, processing factors, and protein oxidation, affect the digestibility and bioavailability of dietary proteins. These factors can influence protein fermentation, absorption, and functional properties in the gut and, consequently, impact the composition of gut microbiota and affect human health. While gut microbiota can release metabolites that can affect host physiology either positively or negatively, the selection of quality of protein and suitable food processing conditions are important to have a positive effect of dietary protein on gut microbiota and human health.

Keywords: dietary protein; gut microbiota; health; influence; meta-analysis; processing.

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Figure 1
Figure 1
Flowchart detailing the process of identifying and selecting studies.
Figure 2
Figure 2
The effect of different protein sources on gut microbiota.
Figure 3
Figure 3
The effect of diet composition on gut microbiota.
Figure 4
Figure 4
The effect of food processing on protein to influence gut microbiota.

References

    1. Agirman G., Hsiao E.Y. SnapShot: The microbiota-gut-brain axis. Cell. 2021;184:2524. doi: 10.1016/j.cell.2021.03.022.
    1. Hill J.H., Round J.L. SnapShot: Microbiota effects on host physiology. Cell. 2021;184:2796. doi: 10.1016/j.cell.2021.04.026.
    1. Danneskiold-Samsøe N.B., De Freitas Queiroz Barros H.D., Santos R., Bicas J.L., Cazarin C.B.B., Madsen L., Kristiansen K., Pastore G.M., Brix S., Maróstica Júnior M.R. Interplay between food and gut microbiota in health and disease. Food Res. Int. 2019;115:23–31. doi: 10.1016/j.foodres.2018.07.043.
    1. Wastyk H.C., Fragiadakis G.K., Perelman D., Dahan D., Merrill B.D., Yu F.B., Topf M., Gonzalez C.G., Van Treuren W., Han S., et al. Gut-microbiota-targeted diets modulate human immune status. Cell. 2021;184:4137–4153. doi: 10.1016/j.cell.2021.06.019.
    1. Olson C.A., Iñiguez A.J., Yang G.E., Fang P., Pronovost G.N., Jameson K.G., Rendon T.K., Paramo J., Barlow J.T., Ismagilov R.F., et al. Alterations in the gut microbiota contribute to cognitive impairment induced by the ketogenic diet and hypoxia. Cell Host Microbe. 2021;29:1378–1392.e6. doi: 10.1016/j.chom.2021.07.004.
    1. Zheng W., Duan M., Jia J., Song S., Ai C. Low-molecular alginate improved diet-induced obesity and metabolic syndrome through modulating the gut microbiota in BALB/c mice. Int. J. Biol. Macromol. 2021;187:811–820. doi: 10.1016/j.ijbiomac.2021.08.003.
    1. Diether N., Willing B. Microbial fermentation of dietary protein: An important factor in diet–microbe–host interaction. Microorganisms. 2019;7:19. doi: 10.3390/microorganisms7010019.
    1. Fan P., Li L., Rezaei A., Eslamfam S., Che D., Ma X. Metabolites of dietary protein and peptides by intestinal microbes and their impacts on gut. Curr. Prot. Pept. Sci. 2015;16:646–654. doi: 10.2174/1389203716666150630133657.
    1. Kim E., Kim D., Park J. Changes of mouse gut microbiota diversity and composition by modulating dietary protein and carbohydrate contents: A pilot study. Prevent. Nutr. Food Sci. 2016;21:57–61. doi: 10.3746/pnf.2016.21.1.57.
    1. Bekhit A., Giteru S.G., Holman B., Hopkins D.L. Total volatile basic nitrogen and trimethylamine in muscle foods: Potential formation pathways and effects on human health. Comp. Rev. Food Sci. Food Saf. 2021;20:3620–3666. doi: 10.1111/1541-4337.12764.
    1. Portune K.J., Beaumont M., Davila A., Tomé D., Blachier F., Sanz Y. Gut microbiota role in dietary protein metabolism and health-related outcomes: The two sides of the coin. Trends Food Sci. Technol. 2016;57:213–232. doi: 10.1016/j.tifs.2016.08.011.
    1. 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. doi: 10.1038/ajg.2010.192.
    1. Batterham R.L., Heffron H., Kapoor S., Chivers J.E., Chandarana K., Herzog H., Le Roux C.W., Thomas E.L., Bell J.D., Withers D.J. Critical role for peptide YY in protein-mediated satiation and body-weight regulation. Cell Metab. 2006;4:223–233. doi: 10.1016/j.cmet.2006.08.001.
    1. Moher D., Shamseer L., Clarke M., Ghersi D., Liberati A., Petticrew M., Shekelle P., Stewart L.A. Preferred reporting items for systematic review and meta-analysis protocols (PRISMA-P) 2015 statement. Syst. Rev. 2015;4:1. doi: 10.1186/2046-4053-4-1.
    1. Liu X., Blouin J., Santacruz A., Lan A., Andriamihaja M., Wilkanowicz S., Benetti P., Tomé D., Sanz Y., Blachier F., et al. High-protein diet modifies colonic microbiota and luminal environment but not colonocyte metabolism in the rat model: The increased luminal bulk connection. Am. J. Physiol.-Gastrointest. Liver Physiol. 2014;307:G459–G470. doi: 10.1152/ajpgi.00400.2013.
    1. Boudry G., Jamin A., Chatelais L., Gras-Le G.C., Michel C., Le Huerou-Luron I. Dietary protein excess during neonatal life alters colonic microbiota and mucosal response to inflammatory mediators later in life in female pigs. J. Nutr. 2013;143:1225–1232. doi: 10.3945/jn.113.175828.
    1. Mu C., Yang Y., Luo Z., Guan L., Zhu W. The colonic microbiome and epithelial transcriptome are altered in rats fed a high-protein diet compared with a normal-protein diet. J. Nutr. 2016;146:474–483. doi: 10.3945/jn.115.223990.
    1. Mu C., Yang Y., Luo Z., Zhu W. Temporal microbiota changes of high-protein diet intake in a rat model. Anaerobe. 2017;47:218–225. doi: 10.1016/j.anaerobe.2017.06.003.
    1. Kar S.K., Jansman A.J.M., Benis N., Ramiro-Garcia J., Schokker D., Kruijt L., Stolte E.H., Taverne-Thiele J.J., Smits M.A., Wells J.M. Dietary protein sources differentially affect microbiota, mTOR activity and transcription of mTOR signaling pathways in the small intestine. PLoS ONE. 2017;12:e188282. doi: 10.1371/journal.pone.0188282.
    1. Xie Y., Wang C., Zhao D., Zhou G., Li C. Processing method altered mouse intestinal morphology and microbial composition by affecting digestion of meat proteins. Front. Microbiol. 2020;11:511. doi: 10.3389/fmicb.2020.00511.
    1. Zhao F., Zhou G., Liu X., Song S., Xu X., Hooiveld G., Müller M., Liu L., Kristiansen K., Li C. Dietary protein sources differentially affect the growth of Akkermansia muciniphila and maintenance of the gut mucus barrier in mice. Mol. Nutr. Food Res. 2019;63:1900589. doi: 10.1002/mnfr.201900589.
    1. Qi H., Xiang Z., Han G., Yu B., Huang Z., Chen D. Effects of different dietary protein sources on cecal microflora in rats. Afr. J. Biotechnol. 2011;10:3704–3708.
    1. An C., Kuda T., Yazaki T., Takahashi H., Kimura B. Caecal fermentation, putrefaction and microbiotas in rats fed milk casein, soy protein or fish meal. Appl. Microbiol. Biotechnol. 2014;98:2779–2787. doi: 10.1007/s00253-013-5271-5.
    1. Zhao F., Song S., Ma Y., Xu X., Zhou G., Li C. A short-term feeding of dietary casein increases abundance of Lactococcus lactis and upregulates gene expression involving obesity prevention in cecum of young rats compared with dietary chicken protein. Front. Microbiol. 2019;10:511. doi: 10.3389/fmicb.2019.02411.
    1. Zhu Y., Lin X., Zhao F., Shi X., Li H., Li Y., Zhu W., Xu X., Li C., Zhou G. Meat, dairy and plant proteins alter bacterial composition of rat gut bacteria. Sci. Rep. 2015;5:15220. doi: 10.1038/srep15220.
    1. Zhu Y., Lin X., Li H., Li Y., Shi X., Zhao F., Xu X., Li C., Zhou G. Intake of meat proteins substantially increased the relative abundance of genus Lactobacillus in rat feces. PLoS ONE. 2016;11:e152678. doi: 10.1371/journal.pone.0152678.
    1. Zhao F., Huang Z., Zhou G., Li H., Xu X., Li C. Dietary proteins rapidly altered the microbial composition in rat caecum. Curr. Microbiol. 2017;74:1447–1452. doi: 10.1007/s00284-017-1339-2.
    1. Zhu Y., Shi X., Lin X., Ye K., Xu X., Li C., Zhou G. Beef, chicken, and soy proteins in diets induce different gut microbiota and metabolites in rats. Front. Microbiol. 2017;8:1395. doi: 10.3389/fmicb.2017.01395.
    1. Yu H., Qiu N., Meng Y., Keast R. A comparative study of the modulation of the gut microbiota in rats by dietary intervention with different sources of egg-white proteins. J. Sci. Food Agric. 2020;100:3622–3629. doi: 10.1002/jsfa.10387.
    1. Han K., Jin W., Mao Z., Dong S., Zhang Q., Yang Y., Chen B., Wu H., Zeng M. Microbiome and butyrate production are altered in the gut of rats fed a glycated fish protein diet. J. Funct. Foods. 2018;47:423–433. doi: 10.1016/j.jff.2018.06.007.
    1. Oberli M., Douard V., Beaumont M., Jaoui D., Devime F., Laurent S., Chaumontet C., Mat D., Le Feunteun S., Michon C., et al. Lipo-protein emulsion structure in the diet affects protein digestion kinetics, intestinal mucosa parameters and microbiota composition. Mol. Nutr. Food Res. 2018;62:1700570. doi: 10.1002/mnfr.201700570.
    1. Beaumont M., Jaoui D., Douard V., Mat D., Koeth F., Goustard B., Mayeur C., Mondot S., Hovaghimian A., Le Feunteun S., et al. Structure of protein emulsion in food impacts intestinal microbiota, caecal luminal content composition and distal intestine characteristics in rats. Mol. Nutr. Food Res. 2017;61:1700078. doi: 10.1002/mnfr.201700078.
    1. Ortman J., Sinn S.M., Gibbons W.R., Brown M.L., DeRouchey J.M., St-Pierre B., Saqui-Salces M., Levesque C.L. Comparative analysis of the ileal bacterial composition of post-weaned pigs fed different high-quality protein sources. Animal. 2020;14:1156–1166. doi: 10.1017/S1751731120000014.
    1. Opheim M., Strube M.L., Sterten H., Overland M., Kjos N.P. Atlantic salmon (Salmo salar) protein hydrolysate in diets for weaning piglets horizontal line effect on growth performance, intestinal morphometry and microbiota composition. Arch. Anim. Nutr. 2016;70:44–56. doi: 10.1080/1745039X.2015.1117694.
    1. Rist V.T.S., 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. doi: 10.1016/j.anaerobe.2013.10.003.
    1. Li R., Chang L., Hou G., Song Z., Fan Z., He X., Hou D. Colonic microbiota and metabolites response to different dietary protein sources in a Piglet model. Front. Nutr. 2019;6:151. doi: 10.3389/fnut.2019.00151.
    1. Yu M., Li Z., Chen W., Rong T., Wang G., Ma X. Hermetia illucens larvae as a potential dietary protein source altered the microbiota and modulated mucosal immune status in the colon of finishing pigs. J. Anim. Sci. Biotechnol. 2019;10:50. doi: 10.1186/s40104-019-0358-1.
    1. Schutkowski A., König B., Kluge H., Hirche F., Henze A., Schwerdtle T., Lorkowski S., Dawczynski C., Gabel A., Große I., et al. Metabolic footprint and intestinal microbial changes in response to dietary proteins in a pig model. J. Nutr. Biochem. 2019;67:149–160. doi: 10.1016/j.jnutbio.2019.02.004.
    1. Yang Y., Wu H., Dong S., Jin W., Han K., Ren Y., Zeng M. Glycation of fish protein impacts its fermentation metabolites and gut microbiota during in vitro human colonic fermentation. Food Res. Int. 2018;113:189–196. doi: 10.1016/j.foodres.2018.07.015.
    1. Ge Y., Lin S., Li B., Yang Y., Tang X., Shi Y., Sun J., Le G. Oxidized pork induces oxidative stress and inflammation by altering gut microbiota in mice. Mol. Nutr. Food Res. 2020;64:1901012. doi: 10.1002/mnfr.201901012.
    1. Van Hecke T., Vossen E., Goethals S., Boon N., De Vrieze J., De Smet S. In vitro and in vivo digestion of red cured cooked meat: Oxidation, intestinal microbiota and fecal metabolites. Food Res. Int. 2021;142:110203. doi: 10.1016/j.foodres.2021.110203.
    1. Snelson M., Clarke R.E., Nguyen T.V., Penfold S.A., Forbes J.M., Tan S.M., Coughlan M.T. Long term high protein diet feeding alters the microbiome and increases intestinal permeability, systemic inflammation and kidney injury in mice. Mol. Nutr. Food Res. 2021;65:2000851. doi: 10.1002/mnfr.202000851.
    1. Nasrollahzadeh M., Nezafat Z., Shafiei N. Proteins in Food Industry. Elsevier; Amsterdam, The Netherlands: 2021. Biopolymer-Based Metal Nanoparticle Chemistry for Sustainable Applications.
    1. Hicks L.M., Verbeek C.J.R. Meat Industry Protein by-Products: Sources and Characteristics. In: Gurpreet S.D., editor. Protein Byproducts. Academic Press; Edmonton, AB, Canada: 2016.
    1. Feher J. Protein Structure. In: Joseph F., editor. Quantitative Human Physiology. Academic Press; Richmond, VA, USA: 2012. pp. 100–109.
    1. Wu G. Dietary protein intake and human health. Food Funct. 2016;7:1251–1265. doi: 10.1039/C5FO01530H.
    1. Wu S., Bekhit A.E.A., Wu Q., Chen M., Liao X., Wang J., Ding Y. Bioactive peptides and gut microbiota: Candidates for a novel strategy for reduction and control of neurodegenerative diseases. Trends Food Sci. Technol. 2021;108:164–176. doi: 10.1016/j.tifs.2020.12.019.
    1. Zhao J., Zhang X., Liu H., Brown M.A., Qiao S. Dietary protein and gut microbiota composition and function. Curr. Prot. Pept. Sci. 2019;20:145. doi: 10.2174/1389203719666180514145437.
    1. Lund M.N., Heinonen M., Baron C.P., Estévez M. Protein oxidation in muscle foods: A review. Mol. Nutr. Food Res. 2011;55:83–95. doi: 10.1002/mnfr.201000453.
    1. Vlieg J.E.V.H., Veiga P., Zhang C., Derrien M., Zhao L. Impact of microbial transformation of food on health-from fermented foods to fermentation in the gastro-intestinal tract. Curr. Opin. Biotechnol. 2011;22:211–219. doi: 10.1016/j.copbio.2010.12.004.
    1. Wu L., Tang Z., Chen H., Ren Z., Ding Q., Liang K., Sun Z. Mutual interaction between gut microbiota and protein/amino acid metabolism for host mucosal immunity and health. Anim. Nutr. 2021;7:11–16. doi: 10.1016/j.aninu.2020.11.003.
    1. Yin J., Li Y., Han H., Liu Z., Zeng X., Li T., Yin Y. Long-term effects of lysine concentration on growth performance, intestinal microbiome, and metabolic profiles in a pig model. Food Funct. 2018;9:4153–4163. doi: 10.1039/C8FO00973B.
    1. Yang Y., Zhang Y., Xu Y., Luo T., Ge Y., Jiang Y., Shi Y., Sun J., Le G. Dietary methionine restriction improves the gut microbiota and reduces intestinal permeability and inflammation in high-fat-fed mice. Food Funct. 2019;10:5952–5968. doi: 10.1039/C9FO00766K.
    1. Windey K., De Preter V., Verbeke K. Relevance of protein fermentation to gut health. Mol. Nutr. Food Res. 2012;56:184–196. doi: 10.1002/mnfr.201100542.
    1. Li R., Hou G.F., Song Z.H., Zhao J.F., Fan Z.Y., Hou D., He X. Nutritional value of enzyme-treated soybean meal, concentrated degossypolized cottonseed protein, dried porcine solubles and fish meal for 10- to −20 kg pigs. Anim. Feed Sci. Technol. 2019;252:23–33. doi: 10.1016/j.anifeedsci.2019.04.002.
    1. Dangin M., Boirie Y., Garcia-Rodenas C., Gachon P., Fauquant J., Callier P., Ballevre O., Beaufrere B. The digestion rate of protein is an independent regulating factor of postprandial protein retention. Am. J. Physiol. Endocrinol. Metab. 2001;280:E340–E348. doi: 10.1152/ajpendo.2001.280.2.E340.
    1. Uhe A.M., Collier G.R., O’Dea K. A comparison of the effects of beef, chicken and fish protein on satiety and amino acid profiles in lean male subjects. J. Nutr. 1992;122:467–472. doi: 10.1093/jn/122.3.467.
    1. Fouillet H., Juillet B., Gaudichon C., Mariotti F., Tomé D., Bos C. Absorption kinetics are a key factor regulating postprandial protein metabolism in response to qualitative and quantitative variations in protein intake. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2009;297:R1691–R1705. doi: 10.1152/ajpregu.00281.2009.
    1. Kostic A.D., Gevers D., Pedamallu C.S., Michaud M., Duke F., Earl A.M., Ojesina A.I., Jung J., Bass A.J., Tabernero J., et al. Genomic analysis identifies association of Fusobacterium with colorectal carcinoma. Genome Res. 2012;22:292–298. doi: 10.1101/gr.126573.111.
    1. Thursby E., Juge N. Introduction to the human gut microbiota. Biochem. J. 2017;474:1823–1836. doi: 10.1042/BCJ20160510.
    1. Higuchi Y., Hosojima M., Kabasawa H., Kuwahara S., Goto S., Toba K., Kaseda R., Tanaka T., Kitamura N., Takihara H., et al. Rice endosperm protein administration to juvenile mice regulates gut microbiota and suppresses the development of high-fat diet-induced obesity and related disorders in adulthood. Nutrients. 2019;11:2919. doi: 10.3390/nu11122919.
    1. Ashaolu T.J. Soy bioactive peptides and the gut microbiota modulation. Appl. Microbiol. Biotechnol. 2020;104:9009–9017. doi: 10.1007/s00253-020-10799-2.
    1. Huang H., Krishnan H.B., Pham Q., Yu L.L., Wang T.T.Y. Soy and gut microbiota: Interaction and implication for human health. J. Agric. Food Chem. 2016;64:8695–8709. doi: 10.1021/acs.jafc.6b03725.
    1. Han W., Zhuang X., Liu Q., Sun B., Miao H., Zhang X. Fermented soy whey induced changes on intestinal microbiota and metabolic influence in mice. Food Sci. Hum. Wellness. 2022;11:41–48. doi: 10.1016/j.fshw.2021.07.005.
    1. Kumar S., Bhat Z.F., Kumar P. Functional meat and meat products. In: Mandal P.K., Biswas A.K., editors. Animal Products Technology. Studium Press; New Delhi, India: 2013. pp. 404–455.
    1. Bhat Z.F., Bhat H. Fibre-based functional meat products. Asian J. Food Agro-Ind. 2011;4:261–273.
    1. Mariotti F. Plant Protein, Animal Protein, and Protein Quality. Academic Press; Cambridge, MA, USA: 2017. Vegetarian and plant-based diets in health and disease prevention; pp. 621–642.
    1. Pereira P.M.D.C., Vicente A.F.D.R. Meat nutritional composition and nutritive role in the human diet. Meat Sci. 2013;93:586–592. doi: 10.1016/j.meatsci.2012.09.018.
    1. Gilbert J.A., Bendsen N.T., Tremblay A., Astrup A. Effect of proteins from different sources on body composition. Nutr. Metab. Cardiovasc. Dis. 2011;21:B16–B31. doi: 10.1016/j.numecd.2010.12.008.
    1. Rodriguez N.R., Miller S.L. Effective translation of current dietary guidance: Understanding and communicating the concepts of minimal and optimal levels of dietary protein. Am. J. Clinic. Nutr. 2015;101:1353S–1358S. doi: 10.3945/ajcn.114.084095.
    1. Aguirre M., Eck A., Koenen M.E., Savelkoul P.H.M., Budding A.E., Venema K. Diet drives quick changes in the metabolic activity and composition of human gut microbiota in a validated in vitro gut model. Res. Microbiol. 2016;167:114–125. doi: 10.1016/j.resmic.2015.09.006.
    1. Kim E., Coelho D., Blachier F. Review of the association between meat consumption and risk of colorectal cancer. Nutr. Res. 2013;33:983–994. doi: 10.1016/j.nutres.2013.07.018.
    1. Stecher B., Hardt W. Mechanisms controlling pathogen colonization of the gut. Curr. Opin. Microbiol. 2010;14:82–91. doi: 10.1016/j.mib.2010.10.003.
    1. Amaretti A., Gozzoli C., Simone M., Raimondi S., Righini L., Pérez-Brocal V., García-López R., Moya A., Rossi M. Profiling of protein degraders in cultures of human gut microbiota. Front. Microbiol. 2019;10:2614. doi: 10.3389/fmicb.2019.02614.
    1. Wexler H.M. Bacteroides: The good, the bad, and the nitty-gritty. Clin. Microbiol. Rev. 2007;20:593–621. doi: 10.1128/CMR.00008-07.
    1. Smith E.A., Macfarlane G.T. Enumeration of amino acid fermenting bacteria in the human large intestine: Effects of pH and starch on peptide metabolism and dissimilation of amino acids. Fem. Microbiol. Ecol. 1998;25:355–368. doi: 10.1111/j.1574-6941.1998.tb00487.x.
    1. Zackular J.P., Baxter N.T., Iverson K.D., Sadler W.D., Petrosino J.F., Chen G.Y., Schloss P.D., Blaser M.J. The gut microbiome modulates colon tumorigenesis. Mbio. 2013;4:e692. doi: 10.1128/mBio.00692-13.
    1. Zhu Q., Jin Z., Wu W., Gao R., Guo B., Gao Z., Yang Y., Qin H., Hold G.L. Analysis of the intestinal lumen microbiota in an animal model of colorectal cancer. PLoS ONE. 2014;9:e90849. doi: 10.1371/journal.pone.0090849.
    1. Varsha K.K., Nampoothiri K.M. Appraisal of lactic acid bacteria as protective cultures. Food Cont. 2016;69:61–64. doi: 10.1016/j.foodcont.2016.04.032.
    1. Durica-Mitic S., Gopel Y., Gorke B. Carbohydrate utilization in bacteria: Making the most out of sugars with the help of small regulatory RNAs. Microbiol. Spectr. 2018;6:2. doi: 10.1128/microbiolspec.RWR-0013-2017.
    1. Zhang T., Li Q., Cheng L., Buch H., Zhang F. Akkermansia muciniphila is a promising probiotic. Microb. Biotechnol. 2019;12:1109–1125. doi: 10.1111/1751-7915.13410.
    1. Parker B.J., Wearsch P.A., Veloo A., Rodriguez-Palacios A. The genus Alistipes: Gut bacteria with emerging implications to inflammation, cancer, and mental health. Front. Immunol. 2020;11:906. doi: 10.3389/fimmu.2020.00906.
    1. Drewes J.L., Domingue J.C., Housseau F. Microbiota, Mucosal Immunity, and Colon Cancer. Elsevier Inc.; Amsterdam, The Netherlands: 2020. pp. 157–209.
    1. Nakamura S., Kuda T., Midorikawa Y., Takahashi H., Kimura B. Typical gut indigenous bacteria in ICR mice fed a normal or soy protein-based low-protein diet. Curr. Res. Food Sci. 2021;4:295–300. doi: 10.1016/j.crfs.2021.04.001.
    1. Ramos S., Martín M.Á. Impact of diet on gut microbiota. Curr. Opin. Food Sci. 2021;37:83–90. doi: 10.1016/j.cofs.2020.09.006.
    1. Mokkala K., Houttu N., Cansev T., Laitinen K. Interactions of dietary fat with the gut microbiota: Evaluation of mechanisms and metabolic consequences. Clin. Nutr. 2020;39:994–1018. doi: 10.1016/j.clnu.2019.05.003.
    1. Payling L., Fraser K., Loveday S.M., Sims I., Roy N., McNabb W. The effects of carbohydrate structure on the composition and functionality of the human gut microbiota. Trends Food Sci. Technol. 2020;97:233–248. doi: 10.1016/j.tifs.2020.01.009.
    1. Mithul Aravind S., Wichienchot S., Tsao R., Ramakrishnan S., Chakkaravarthi S. Role of dietary polyphenols on gut microbiota, their metabolites and health benefits. Food Res. Int. 2021;142:110189. doi: 10.1016/j.foodres.2021.110189.
    1. Ma N., Tian Y., Wu Y., Ma X. Contributions of the interaction between dietary protein and gut microbiota to intestinal health. Curr. Prot. Pept. Sci. 2017;18:795–808. doi: 10.2174/1389203718666170216153505.
    1. Nakata T., Kyoui D., Takahashi H., Kimura B., Kuda T. Inhibitory effects of soybean oligosaccharides and water-soluble soybean fibre on formation of putrefactive compounds from soy protein by gut microbiota. Int. J. Biol. Macromol. 2017;97:173–180. doi: 10.1016/j.ijbiomac.2017.01.015.
    1. Biddle A., Stewart L., Blanchard J., Leschine S. Untangling the genetic basis of fibrolytic specialization by Lachnospiraceae and Ruminococcaceae in diverse gut communities. Diversity. 2013;5:627–640. doi: 10.3390/d5030627.
    1. Russell W.R., Gratz S.W., Duncan S.H., Holtrop G., Ince J., Scobbie L., Duncan G., Johnstone A.M., Lobley G.E., Wallace R.J., et al. High-protein, reduced-carbohydrate weight-loss diets promote metabolite profiles likely to be detrimental to colonic health. Am. J. Clin. Nutr. 2011;93:1062–1072. doi: 10.3945/ajcn.110.002188.
    1. Shen F., Niu F., Li J., Su Y., Liu Y., Yang Y. Interactions between tea polyphenol and two kinds of typical egg white proteins—ovalbumin and lysozyme: Effect on the gastrointestinal digestion of both proteins in vitro. Food Res. Int. 2014;59:100–107. doi: 10.1016/j.foodres.2014.01.070.
    1. Mirmoghtadaie L., Aliabadi S.S., Hosseini S.M. Recent approaches in physical modification of protein functionality. Food Chem. 2016;199:619–627. doi: 10.1016/j.foodchem.2015.12.067.
    1. Mitra B., Rinnan Å., Ruiz-Carrascal J. Tracking hydrophobicity state, aggregation behaviour and structural modifications of pork proteins under the influence of assorted heat treatments. Food Res. Int. 2017;101:266–273. doi: 10.1016/j.foodres.2017.09.027.
    1. Neis E.P.J.G., Dejong C.H., Rensen S.S. The role of microbial amino acid metabolism in host metabolism. Nutrients. 2015;7:2930–2946. doi: 10.3390/nu7042930.
    1. Davila A.M., Blachier F., Gotteland M., Andriamihaja M., Benetti P.H., Sanz Y., Tome D. Intestinal luminal nitrogen metabolism: Role of the gut microbiota and consequences for the host. Pharmacol. Res. 2013;69:114–126. doi: 10.1016/j.phrs.2013.01.003.
    1. 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. doi: 10.1007/s00726-006-0477-9.
    1. Bhat Z.F., Morton J.D., Bekhit A.E.A., Kumar S., Bhat H.F. Emerging processing technologies for improved digestibility of muscle proteins. Trends Food Sci. Technol. 2021;110:226–239. doi: 10.1016/j.tifs.2021.02.010.
    1. Bhat Z.F., Morton J.D., Bekhit A.E.D.A., Kumar S., Bhat H.F. Processing technologies for improved digestibility of milk proteins. Trends Food Sci. Technol. 2021;118:1–16. doi: 10.1016/j.tifs.2021.09.017.
    1. Bhat Z.F., Morton J.D., Bekhit A.E.D.A., Kumar S., Bhat H.F. Processing technologies for improved digestibility of egg proteins. Comp. Rev. Food Sci. 2021;20:1–36.
    1. Zhang Z., Zhang X., Chen W., Zhou P. Conformation stability, in vitro digestibility and allergenicity of tropomyosin from shrimp (Exopalaemon modestus) as affected by high intensity ultrasound. Food Chem. 2018;245:997–1009. doi: 10.1016/j.foodchem.2017.11.072.
    1. Rysman T., Van Hecke T., Van Poucke C., De Smet S., Van Royen G. Protein oxidation and proteolysis during storage and in vitro digestion of pork and beef patties. Food Chem. 2016;209:177–184. doi: 10.1016/j.foodchem.2016.04.027.
    1. Bhat Z.F., Morton J.D., Bekhit A.E.A., Kumar S., Bhat H.F. Non-thermal processing has an impact on the digestibility of the muscle proteins. Crit. Rev. Food Sci. 2021:1–28. doi: 10.1080/10408398.2021.1918629.
    1. Zhao D., He J., Zou X., Nian Y., Xu X., Zhou G., Li C. Influence of salting process on the structure and in vitro digestibility of actomyosin. J. Food Sci. Technol. 2019;57:1763–1773. doi: 10.1007/s13197-019-04210-w.
    1. Bhat Z.F., Morton J.D., Bekhit A.E.D.A., Kumar S., Bhat H.F. Thermal processing implications on the digestibility of meat, fish and seafood proteins. Comp. Rev. Food Sci. 2021;20:4511–4548. doi: 10.1111/1541-4337.12802.
    1. Bhat Z.F., Morton J.D., Zhang X., Mason S.L., Bekhit A. Sous-vide cooking improves the quality and in-vitro digestibility of Semitendinosus from culled dairy cows. Food Res. Int. 2020;127:108708. doi: 10.1016/j.foodres.2019.108708.
    1. Canfora E.E., Meex R., Venema K., Blaak E.E. Gut microbial metabolites in obesity, NAFLD and T2DM. Nat. Rev. Endocrinol. 2019;15:261–273. doi: 10.1038/s41574-019-0156-z.
    1. Magne F., Gotteland M., Gauthier L., Zazueta A., Pesoa S., Navarrete P., Balamurugan R. The Firmicutes/Bacteroidetes ratio: A relevant marker of gut dysbiosis in obese patients? Nutrients. 2020;12:1474. doi: 10.3390/nu12051474.
    1. Kaur U.S., Shet A., Rajnala N., Gopalan B.P., Moar P., Himanshu D., Singh B.P., Chaturvedi R., Tandon R. High abundance of genus Prevotella in the gut of perinatally HIV-infected children is associated with IP-10 levels despite therapy. Sci. Rep. 2018;8:17679. doi: 10.1038/s41598-018-35877-4.
    1. Fan P., Liu P., Song P., Chen X., Ma X. Moderate dietary protein restriction alters the composition of gut microbiota and improves ileal barrier function in adult pig model. Sci. Rep. 2017;7:43412. doi: 10.1038/srep43412.
    1. He J., Zhou G., Bai Y., Wang C., Zhu S., Xu X., Li C. The effect of meat processing methods on changes in disulfide bonding and alteration of protein structures: Impact on protein digestion products. RSC Adv. 2018;8:17595–17605. doi: 10.1039/C8RA02310G.
    1. Collado L., Figueras M.J. Taxonomy, epidemiology, and clinical relevance of the genus Arcobacter. Clin. Microbiol. Rev. 2011;24:174–192. doi: 10.1128/CMR.00034-10.
    1. Polansky O., Sekelova Z., Faldynova M., Sebkova A., Sisak F., Rychlik I. Important metabolic pathways and biological processes expressed by chicken cecal microbiota. Appl. Environ. Microbiol. 2015;82:1569–1576. doi: 10.1128/AEM.03473-15.
    1. Liu M., Bayjanov J.R., Renckens B., Nauta A., Siezen R.J. The proteolytic system of lactic acid bacteria revisited: A genomic comparison. BMC Genom. 2010;11:36. doi: 10.1186/1471-2164-11-36.
    1. Binda C., Lopetuso L.R., Rizzatti G., Gibiino G., Cennamo V., Gasbarrini A. Actinobacteria: A relevant minority for the maintenance of gut homeostasis. Digest. Liver Dis. 2018;50:421–428. doi: 10.1016/j.dld.2018.02.012.
    1. Naito Y., Uchiyama K., Takagi T. A next-generation beneficial microbe: Akkermansia muciniphila. J. Clin. Biochem. Nutr. 2018;63:33–35. doi: 10.3164/jcbn.18-57.
    1. Geerlings S.Y., Kostopoulos I., de Vos W.M., Belzer C. Akkermansia muciniphila in the Human Gastrointestinal Tract: When, Where, and How? Microorganisms. 2018;6:75. doi: 10.3390/microorganisms6030075.
    1. Berardo A., Devreese B., De Maere H., Stavropoulou D.A., Van Royen G., Leroy F., De Smet S. Actin proteolysis during ripening of dry fermented sausages at different pH values. Food Chem. 2017;221:1322–1332. doi: 10.1016/j.foodchem.2016.11.023.
    1. Traore S., Aubry L., Gatellier P., Przybylski W., Jaworska D., Kajak-Siemaszko K., Sante-Lhoutellier V. Higher drip loss is associated with protein oxidation. Meat Sci. 2012;90:917–924. doi: 10.1016/j.meatsci.2011.11.033.
    1. Sante-Lhoutellier V., Aubry L., Gatellier P. Effect of oxidation on in vitro digestibility of skeletal muscle myofibrillar proteins. J Agric. Food Chem. 2007;55:5343–5348. doi: 10.1021/jf070252k.
    1. Cabanillas B., Novak N. Effects of daily food processing on allergenicity. Crit. Rev. Food Sci. 2019;59:31–42. doi: 10.1080/10408398.2017.1356264.
    1. Zhu Y., Vanga S.K., Wang J., Raghavan V. Effects of ultrasonic and microwave processing on Avidin assay and secondary structures of egg white protein. Food Bioprocess Technol. 2018;11:1974–1984. doi: 10.1007/s11947-018-2158-6.
    1. Wang X.B.N.A., Chi Y.J.N.A. Microwave-assisted phosphorylation of soybean protein isolates and their physicochemical properties. Czech J. Food Sci. 2012;30:99–107. doi: 10.17221/91/2011-CJFS.
    1. Morzel M., Gatellier P., Sayd T., Renerre M., Laville E. Chemical oxidation decreases proteolytic susceptibility of skeletal muscle myofibrillar proteins. Meat Sci. 2006;73:536–543. doi: 10.1016/j.meatsci.2006.02.005.
    1. Gratz M., Schottroff F., Gall L., Zejma B., Simon F., Jaeger H. Advantages of ohmic cooking in the kilohertz-range-part I: Impact of conductivity and frequency on the heating uniformity of potatoes. Innov. Food Sci. Emerg. 2021;67:102595. doi: 10.1016/j.ifset.2020.102595.
    1. Rodrigues R.M., Pereira R.N., Vicente A.A., Cavaco-Paulo A., Ribeiro A. Ohmic heating as a new tool for protein scaffold engineering. Mat. Sci. Eng. C. 2021;120:111784. doi: 10.1016/j.msec.2020.111784.
    1. Moreira T., Pereira R.N., Vicente A.A., Da C.R. Effect of Ohmic heating on functionality of sodium caseinate—A relationship with protein gelation. Food Res. Int. 2019;116:628–636. doi: 10.1016/j.foodres.2018.08.087.
    1. Alizadeh O., Aliakbarlu J. Effects of ultrasound and ohmic heating pretreatments on hydrolysis, antioxidant and antibacterial activities of whey protein concentrate and its fractions. Food Sci. Technol. 2020;131:109913. doi: 10.1016/j.lwt.2020.109913.
    1. Jaeger H., Janositz A., Knorr D. The Maillard reaction and its control during food processing. The potential of emerging technologies. Pathol. Biol. 2010;58:207–213. doi: 10.1016/j.patbio.2009.09.016.
    1. Nooshkam M., Varidi M., Verma D.K. Functional and biological properties of Maillard conjugates and their potential application in medical and food: A review. Food Res. Int. 2020;131:109003. doi: 10.1016/j.foodres.2020.109003.
    1. Han K., Yao Y., Dong S., Jin S., Xiao H., Wu H., Zeng M. Chemical characterization of the glycated myofibrillar proteins from grass carp (Ctenopharyngodon idella) and their impacts on the human gut microbiota in vitro fermentation. Food Funct. 2017;8:1184–1194. doi: 10.1039/C6FO01632D.
    1. Yang M., Liu J., Yang X., Li S., Li C., Liu B., Ma S., Liu X., Du Z., Zhang T., et al. Effect of glycation degree on the in vitro simulated gastrointestinal digestion: A promising formulation for egg white gel with controlled digestibility. Food Chem. 2021;349:129096. doi: 10.1016/j.foodchem.2021.129096.
    1. Jiménez-Saiz R., Belloque J., Molina E., López-Fandinño R. Human immunoglobulin E (IgE) binding to heated and glycated ovalbumin and ovomucoid before and after in vitro digestion. J. Agric. Food Chem. 2011;59:10044–10051. doi: 10.1021/jf2014638.
    1. Hellwig M. Analysis of protein oxidation in food and feed products. J. Agric. Food Chem. 2020;68:12870–12885. doi: 10.1021/acs.jafc.0c00711.
    1. Soladoye O.P., Juárez M.L., Aalhus J.L., Shand P., Estévez M. Protein oxidation in processed meat: Mechanisms and potential implications on human health. Comp. Rev. Food Sci. 2015;14:106–122. doi: 10.1111/1541-4337.12127.
    1. Bax M., Buffière C., Hafnaoui N., Gaudichon C., Savary-Auzeloux I., Dardevet D., Santé-Lhoutellier V., Rémond D., Blachier F. Effects of meat cooking, and of ingested amount, on protein digestion speed and entry of residual proteins into the colon: A study in minipigs. PLoS ONE. 2013;8:e61252. doi: 10.1371/journal.pone.0061252.
    1. Gong X., Morton J.D., Bhat Z.F., Mason S.L., Bekhit A.E.D.A. Comparative efficacy of actinidin from green and gold kiwi fruit extract on in vitro simulated protein digestion of beef Semitendinosus and its myofibrillar protein fraction. Int. J. Food Sci. Technol. 2020;55:742–750. doi: 10.1111/ijfs.14345.
    1. Du X., Sun Y., Pan D., Wang Y., Ou C., Cao J. Change of the structure and the digestibility of myofibrillar proteins in Nanjing dry-cured duck during processing. J. Sci. Food Agric. 2018;98:3140–3147. doi: 10.1002/jsfa.8815.
    1. Kaur L., Maudens E., Haisman D.R., Boland M.J., Singh H. Microstructure and protein digestibility of beef: The effect of cooking conditions as used in stews and curries. Food Sci. Technol. 2014;55:612–620. doi: 10.1016/j.lwt.2013.09.023.
    1. Wei T., Dang Y., Cao J., Wu Z., He J., Sun Y., Pan D., Tian Z. Different duck products protein on rat physiology and gut microbiota. J. Proteom. 2019;206:103436. doi: 10.1016/j.jprot.2019.103436.
    1. Cao C., Tang M., Zhao N., Dong S., Wu H. Effects of fish protein with glycation extent on gut microbiota and colonic barrier function in mice fed a high-fat diet. J. Funct. Foods. 2021;85:104636. doi: 10.1016/j.jff.2021.104636.
    1. Kanauchi O., Fujiyama Y., Mitsuyama K., Araki Y., Ishii T., Nakamura T., Hitomi Y., Agata K., Saiki T., Andoh A., et al. Increased growth of Bifidobacterium and Eubacterium by germinated barley foodstuff, accompanied by enhanced butyrate production in healthy volunteers. Int. J. Mol. Med. 1999;3:175. doi: 10.3892/ijmm.3.2.175.
    1. Santiago-López L., Hernández-Mendoza A., Vallejo-Cordoba B., Wall-Medrano A., González-Córdova A.F. Th17 immune response in inflammatory bowel disease: Future roles and opportunities for lactic acid bacteria and bioactive compounds released in fermented milk. Trends Food Sci. Technol. 2021;112:109–117. doi: 10.1016/j.tifs.2021.03.051.
    1. Bermingham E.N., Maclean P., Thomas D.G., Cave N.J., Young W. Key bacterial families (Clostridiaceae, Erysipelotrichaceae and Bacteroidaceae) are related to the digestion of protein and energy in dogs. PeerJ. 2017;5:e3019. doi: 10.7717/peerj.3019.
    1. Muniz P.D., Chen J., Hillmann B., Jeraldo P., Al-Ghalith G., Taneja V., Davis J.M., Knights D., Nelson H., Faubion W.A., et al. An increased abundance of Clostridiaceae characterizes Arthritis in inflammatory bowel disease and rheumatoid arthritis: A Cross-sectional study. Inflamm. Bowel Dis. 2019;25:902–913. doi: 10.1093/ibd/izy318.
    1. Krzyściak W., Pluskwa K.K., Jurczak A., Kościelniak D. The pathogenicity of the Streptococcus genus. Eur. J. Clin. Microbiol. 2013;32:1361–1376. doi: 10.1007/s10096-013-1914-9.
    1. Goertz S., de Menezes A.B., Birtles R.J., Fenn J., Lowe A.E., MacColl A.D.C., Poulin B., Young S., Bradley J.E., Taylor C.H. Geographical location influences the composition of the gut microbiota in wild house mice (Mus musculus domesticus) at a fine spatial scale. PLoS ONE. 2019;14:e222501. doi: 10.1371/journal.pone.0222501.
    1. Goodrich J.K., Waters J.L., Poole A.C., Sutter J.L., Koren O., Blekhman R., Beaumont M., Van Treuren W., Knight R., Bell J.T., et al. Human genetics shape the gut microbiome. Cell. 2014;159:789–799. doi: 10.1016/j.cell.2014.09.053.

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