The Prebiotic Effect of an Organic Acid Mixture on Faecalibacterium prausnitzii Metabolism and Its Anti-Pathogenic Role against Vibrio parahaemolyticus in Shrimp
Abstract
:Simple Summary
Abstract
1. Introduction
2. Materials and Methods
2.1. F. prausnitzii Growth Performance in the Presence of AuraAqua
2.2. In Vitro Shrimp Gut Models
2.3. Quantification of F. prausnitzii in the Shrimp Gut Model by RT-PCR and by Viable Counts
2.4. Butyrate Measurement during F. prausnitzii Growth in the Presence of AuraAqua
2.5. In Vitro Butyrate Production in the Presence of a Cellulose Substrate
2.6. Infection of Shrimp Primary Cells (SGP) with V. parahaemolyticus in the Presence F. prausnitzii
2.7. RT-PCR for Butyryl-CoA Transferase Quantification
2.8. Statistical Analysis
3. Results
3.1. The In Vitro Effect of AuraAqua (Aq) on F. prausnitzii Growth in Minimal Media
3.2. F. prausnitzii Growth and Butyrate Prodyction in a Shrimp Gut Model and an Irradiated Spiked Faeces Gut Model in the Presence of Aq
3.3. F. prausnitzii In Vitro Growth, Butyrate Production and Substrate Digestion
3.4. The Impact of Aq Grown F. prausnitzii on V. parahaeomolyticus A3 Infection of Primary Shrimp Gut Epithelial Cells (SGP)
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Butt, U.D.; Lin, N.; Akhter, N.; Siddiqui, T.; Li, S.; Wu, B. Overview of the latest developments in the role of probiotics, prebiotics and synbiotics in shrimp aquaculture. Fish Shellfish. Immunol. 2021, 114, 263–281. [Google Scholar] [CrossRef] [PubMed]
- Huang, H.T.; Chang, J.J.; Lin, Y.R.; Chen, Y.Y.; Wu Chang, Y.H.; Chen, B.Y.; Nan, F.H. Synergistic effects of dietary oxolinic acid combined with oxytetracycline on nonspecific immune responses and resistance against Vibrio parahaemolyticus infection of white shrimp (Penaeus vannamei). Fish Shellfish. Immunol. 2022, 127, 740–747. [Google Scholar] [CrossRef] [PubMed]
- Ninawe, A.S.; Selvin, J. Probiotics in shrimp aquaculture: Avenues and challenges. Crit. Rev. Microbiol. 2009, 35, 43–66. [Google Scholar] [CrossRef] [PubMed]
- Kanrar, S.; Dhar, A.K. Complete Genome Sequence of a Novel Mutant Strain of Vibrio parahaemolyticus from Pacific White Shrimp (Penaeus vannamei). Genome Announc. 2018, 6, e00497-18. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Pinkerton, L.; Linton, M.; Kelly, C.; Ward, P.; Gradisteanu Pircalabioru, G.; Pet, I.; Stef, L.; Sima, F.; Adamov, T.; Gundogdu, O.; et al. Attenuation of Vibrio parahaemolyticus Virulence Factors by a Mixture of Natural Antimicrobials. Microorganisms 2019, 7, 679. [Google Scholar] [CrossRef] [Green Version]
- Rui, W.; Xiao, J.; Wang, Q.; Zhao, W.; Liu, X.; Liu, Y.; Fu, S. Genomic analysis of a new type VI secretion system in Vibrio parahaemolyticus and its implication for environmental adaptation in shrimp ponds. Can. J. Microbiol. 2022. [Google Scholar] [CrossRef]
- Sathitkowitchai, W.; Sathapondecha, P.; Angthong, P.; Srimarut, Y.; Malila, Y.; Nakkongkam, W.; Chaiyapechara, S.; Karoonuthaisiri, N.; Keawsompong, S.; Rungrassamee, W. Isolation and Characterization of Mannanase-Producing Bacteria for Potential Synbiotic Application in Shrimp Farming. Animals 2022, 12, 2583. [Google Scholar] [CrossRef]
- Fernandez-Arguelles, E.L.; Rodriguez-Mansilla, J.; Antunez, L.E.; Garrido-Ardila, E.M.; Munoz, R.P. Effects of dancing on the risk of falling related factors of healthy older adults: A systematic review. Arch. Gerontol. Geriatr. 2015, 60, 1–8. [Google Scholar] [CrossRef]
- Du, Y.; Xu, W.; Wu, T.; Li, H.; Hu, X.; Chen, J. Enhancement of growth, survival, immunity and disease resistance in Litopenaeus vannamei, by the probiotic, Lactobacillus plantarum Ep-M17. Fish Shellfish. Immunol. 2022, 129, 36–51. [Google Scholar] [CrossRef]
- Auger, S.; Mournetas, V.; Chiapello, H.; Loux, V.; Langella, P.; Chatel, J.M. Gene co-expression network analysis of the human gut commensal bacterium Faecalibacterium prausnitzii in R-Shiny. PLoS ONE 2022, 17, e0271847. [Google Scholar] [CrossRef]
- Cornejo-Granados, F.; Lopez-Zavala, A.A.; Gallardo-Becerra, L.; Mendoza-Vargas, A.; Sanchez, F.; Vichido, R.; Brieba, L.G.; Viana, M.T.; Sotelo-Mundo, R.R.; Ochoa-Leyva, A. Microbiome of Pacific Whiteleg shrimp reveals differential bacterial community composition between Wild, Aquacultured and AHPND/EMS outbreak conditions. Sci. Rep. 2017, 7, 11783. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hankel, J.; Chuppava, B.; Wilke, V.; Hartung, C.B.; Muthukumarasamy, U.; Strowig, T.; Bach Knudsen, K.E.; Kamphues, J.; Visscher, C. High Dietary Intake of Rye Affects Porcine Gut Microbiota in a Salmonella Typhimurium Infection Study. Plants 2022, 11, 2232. [Google Scholar] [CrossRef] [PubMed]
- Zhang, X.; Song, M.; Lv, P.; Hao, G.; Sun, S. Effects of Clostridium butyricum on intestinal environment and gut microbiome under Salmonella infection. Poult. Sci. 2022, 101, 102077. [Google Scholar] [CrossRef] [PubMed]
- Balta, I.; Stef, L.; Butucel, E.; Gradisteanu Pircalabioru, G.; Venig, A.; Ward, P.; Deshaies, M.; Pet, I.; Stef, D.; Koyun, O.Y.; et al. The Antioxidant Effect of Natural Antimicrobials in Shrimp Primary Intestinal Cells Infected with Nematopsis messor. Antioxidants 2022, 11, 974. [Google Scholar] [CrossRef] [PubMed]
- Sima, F.; Stratakos, A.C.; Ward, P.; Linton, M.; Kelly, C.; Pinkerton, L.; Stef, L.; Gundogdu, O.; Lazar, V.; Corcionivoschi, N. A Novel Natural Antimicrobial Can Reduce the in vitro and in vivo Pathogenicity of T6SS Positive Campylobacter jejuni and Campylobacter coli Chicken Isolates. Front. Microbiol. 2018, 9, 2139. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Balta, I.; Marcu, A.; Linton, M.; Kelly, C.; Stef, L.; Pet, I.; Ward, P.; Pircalabioru, G.G.; Chifiriuc, C.; Gundogdu, O.; et al. The in vitro and in vivo anti-virulent effect of organic acid mixtures against Eimeria tenella and Eimeria bovis. Sci. Rep. 2021, 11, 16202. [Google Scholar] [CrossRef]
- Balta, I.; Stef, L.; Pet, I.; Ward, P.; Callaway, T.; Ricke, S.C. Antiviral activity of a novel mixture of natural antimicrobials, in vitro, and in a chicken infection model in vivo. Sci. Rep. 2020, 10, 16631. [Google Scholar] [CrossRef]
- Balta, I.; Pet, I.; Ward, P.; Venig, A.; Callaway, T.; Corcionivoschi, N.; Stef, L. Reducing Nematopsis spp Infection of Panaeus Vannamei Shrimps Post Larvae by Using a Mixture of Natural Antimicrobials. Bull. Univ. Agric. Sci. Vet. Med. Cluj-Napoca-Food Sci. Technol. 2022, 79. [Google Scholar] [CrossRef]
- Kelly, C.; Gundogdu, O.; Pircalabioru, G.; Cean, A.; Scates, P.; Linton, M.; Pinkerton, L.; Magowan, E.; Stef, L.; Simiz, E.; et al. The In Vitro and In Vivo Effect of Carvacrol in Preventing Campylobacter Infection, Colonization and in Improving Productivity of Chicken Broilers. Foodborne Pathog. Dis. 2017, 14, 341–349. [Google Scholar] [CrossRef]
- Moreno-Indias, I.; Sanchez-Alcoholado, L.; Perez-Martinez, P.; Andres-Lacueva, C.; Cardona, F.; Tinahones, F.; Queipo-Ortuno, M.I. Red wine polyphenols modulate fecal microbiota and reduce markers of the metabolic syndrome in obese patients. Food Funct. 2016, 7, 1775–1787. [Google Scholar] [CrossRef]
- Toschi, A.; Rossi, B.; Tugnoli, B.; Piva, A.; Grilli, E. Nature-identical compounds and organic acids ameliorate and prevent the damages induced by an inflammatory challenge in Caco-2 cell culture. Molecules 2020, 25, 4296. [Google Scholar] [CrossRef] [PubMed]
- Heinken, A.; Khan, M.T.; Paglia, G.; Rodionov, D.A.; Harmsen, H.J.; Thiele, I. Functional metabolic map of Faecalibacterium prausnitzii, a beneficial human gut microbe. J. Bacteriol. 2014, 196, 3289–3302. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Suhaimi, N.S.M.; Yin, Y.S.; Nazari, T.F.; Halim, M.A.; Daud, F.; Ibrahim, D.; Zarkasi, K.Z. The potential use of prodigiosin as a shrimp feed additive and its dynamic influence on the shrimp gut microbial community—An in vitro gut model. Malays. J. Microbiol. 2019, 15, 10. [Google Scholar]
- Sezgin, E.; Terlemez, G.; Bozkurt, B.; Bengi, G.; Akpinar, H.; Buyuktorun, I. Quantitative real-time PCR analysis of bacterial biomarkers enable fast and accurate monitoring in inflammatory bowel disease. PeerJ 2022, 10, e14217. [Google Scholar] [CrossRef]
- Fujimoto, T.; Imaeda, H.; Takahashi, K.; Kasumi, E.; Bamba, S.; Fujiyama, Y.; Andoh, A. Decreased abundance of Faecalibacterium prausnitzii in the gut microbiota of Crohn’s disease. J. Gastroenterol. Hepatol. 2013, 28, 613–619. [Google Scholar] [CrossRef]
- Ramirez-Farias, C.; Slezak, K.; Fuller, Z.; Duncan, A.; Holtrop, G.; Louis, P. Effect of inulin on the human gut microbiota: Stimulation of Bifidobacterium adolescentis and Faecalibacterium prausnitzii. Br. J. Nutr. 2009, 101, 541–550. [Google Scholar] [CrossRef] [Green Version]
- Wang, W.; Chen, L.; Zhou, R.; Wang, X.; Song, L.; Huang, S.; Wang, G.; Xia, B. Increased proportions of Bifidobacterium and the Lactobacillus group and loss of butyrate-producing bacteria in inflammatory bowel disease. J. Clin. Microbiol. 2014, 52, 398–406. [Google Scholar] [CrossRef] [Green Version]
- Fagundes, R.R.; Bourgonje, A.R.; Saeed, A.; Vich Vila, A.; Plomp, N.; Blokzijl, T.; Sadaghian Sadabad, M.; von Martels, J.Z.H.; van Leeuwen, S.S.; Weersma, R.K.; et al. Inulin-grown Faecalibacterium prausnitzii cross-feeds fructose to the human intestinal epithelium. Gut Microbes 2021, 13, 1993582. [Google Scholar] [CrossRef]
- Godínez-Méndez, L.A.; Gurrola-Díaz, C.M.; Zepeda-Nuño, J.S.; Vega-Magaña, N.; Lopez-Roa, R.I.; Íñiguez-Gutiérrez, L.; García-López, P.M.; Fafutis-Morris, M.; Delgado-Rizo, V. In Vivo Healthy Benefits of Galacto-Oligosaccharides from Lupinus albus (LA-GOS) in Butyrate Production through Intestinal Microbiota. Biomolecules 2021, 11, 1658. [Google Scholar] [CrossRef]
- Louis, P.; Flint, H.J. Development of a semiquantitative degenerate real-time pcr-based assay for estimation of numbers of butyryl-coenzyme A (CoA) CoA transferase genes in complex bacterial samples. Appl. Environ. Microbiol. 2007, 73, 2009–2012. [Google Scholar] [CrossRef] [Green Version]
- Won, S.; Hamidoghli, A.; Choi, W.; Bae, J.; Jang, W.J.; Lee, S.; Bai, S.C. Evaluation of Potential Probiotics Bacillus subtilis WB60, Pediococcus pentosaceus, and Lactococcus lactis on Growth Performance, Immune Response, Gut Histology and Immune-Related Genes in Whiteleg Shrimp, Litopenaeus vannamei. Microorganisms 2020, 8, 281. [Google Scholar] [CrossRef] [PubMed]
- Markowiak-Kopeć, P.; Śliżewska, K. The Effect of Probiotics on the Production of Short-Chain Fatty Acids by Human Intestinal Microbiome. Nutrients 2020, 12, 1107. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhu, W.; Gao, J.; Liu, H.; Liu, J.; Jin, T.; Qin, N.; Ren, X.; Xia, X. Antibiofilm effect of sodium butyrate against Vibrio parahaemolyticus. Food Control 2022, 131, 108422. [Google Scholar] [CrossRef]
- Tan, J.; McKenzie, C.; Potamitis, M.; Thorburn, A.N.; Mackay, C.R.; Macia, L. The role of short-chain fatty acids in health and disease. Adv. Immunol. 2014, 121, 91–119. [Google Scholar] [CrossRef] [PubMed]
- Zhou, L.; Zhang, M.; Wang, Y.; Dorfman, R.G.; Liu, H.; Yu, T.; Chen, X.; Tang, D.; Xu, L.; Yin, Y.; et al. Faecalibacterium prausnitzii Produces Butyrate to Maintain Th17/Treg Balance and to Ameliorate Colorectal Colitis by Inhibiting Histone Deacetylase 1. Inflamm. Bowel Dis. 2018, 24, 1926–1940. [Google Scholar] [CrossRef] [Green Version]
- Lopez-Siles, M.; Khan, T.M.; Duncan, S.H.; Harmsen, H.J.; Garcia-Gil, L.J.; Flint, H.J. Cultured representatives of two major phylogroups of human colonic Faecalibacterium prausnitzii can utilize pectin, uronic acids, and host-derived substrates for growth. Appl. Environ. Microbiol. 2012, 78, 420–428. [Google Scholar] [CrossRef] [Green Version]
- Martin, R.; Miquel, S.; Benevides, L.; Bridonneau, C.; Robert, V.; Hudault, S.; Chain, F.; Berteau, O.; Azevedo, V.; Chatel, J.M.; et al. Functional Characterization of Novel Faecalibacterium prausnitzii Strains Isolated from Healthy Volunteers: A Step Forward in the Use of F. prausnitzii as a Next-Generation Probiotic. Front. Microbiol. 2017, 8, 1226. [Google Scholar] [CrossRef] [Green Version]
- Chen, M.; Chen, X.Q.; Tian, L.X.; Liu, Y.J.; Niu, J. Improvement of growth, intestinal short-chain fatty acids, non-specific immunity and ammonia resistance in Pacific white shrimp (Litopenaeus vannamei) fed dietary water-soluble chitosan and mixed probiotics. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 2020, 236, 108791. [Google Scholar] [CrossRef]
- Silva, B.C.; Jesus, G.F.A.; Seiffert, W.Q.; Vieira, F.N.; Mouriño, J.L.P.; Jatobá, A.; Nolasco-Soria, H. The effects of dietary supplementation with butyrate and polyhydroxybutyrate on the digestive capacity and intestinal morphology of Pacific White Shrimp (Litopenaeus vannamei). Mar. Freshw. Behav. Physiol. 2016, 49, 447–458. [Google Scholar] [CrossRef]
- Olano-Martin, E.; Mountzouris, K.C.; Gibson, G.R.; Rastall, R.A. In vitro fermentability of dextran, oligodextran and maltodextrin by human gut bacteria. Br. J. Nutr. 2000, 83, 247–255. [Google Scholar] [CrossRef] [Green Version]
- Murakami, R.; Hashikura, N.; Yoshida, K.; Xiao, J.Z.; Odamaki, T. Growth-promoting effect of alginate on Faecalibacterium prausnitzii through cross-feeding with Bacteroides. Food Res. Int. 2021, 144, 110326. [Google Scholar] [CrossRef]
- Precup, G.; Teleky, B.E.; Ranga, F.; Vodnar, D.C. Assessment of Physicochemical and Rheological Properties of Xylo-Oligosaccharides and Glucose-Enriched Doughs Fermented with BB-12. Biology 2022, 11, 553. [Google Scholar] [CrossRef] [PubMed]
- Lensu, S.; Pariyani, R.; Makinen, E.; Yang, B.; Saleem, W.; Munukka, E.; Lehti, M.; Driuchina, A.; Linden, J.; Tiirola, M.; et al. Prebiotic Xylo-Oligosaccharides Ameliorate High-Fat-Diet-Induced Hepatic Steatosis in Rats. Nutrients 2020, 12, 3225. [Google Scholar] [CrossRef] [PubMed]
- Fu, X.; Liu, Z.; Zhu, C.; Mou, H.; Kong, Q. Nondigestible carbohydrates, butyrate, and butyrate-producing bacteria. Crit. Rev. Food Sci. Nutr. 2019, 59, S130–S152. [Google Scholar] [CrossRef]
- Zhou, Y.; Xu, H.; Xu, J.; Guo, X.; Zhao, H.; Chen, Y.; Zhou, Y.; Nie, Y.F. prausnitzii and its supernatant increase SCFAs-producing bacteria to restore gut dysbiosis in TNBS-induced colitis. AMB Express 2021, 11, 33. [Google Scholar] [CrossRef] [PubMed]
- De, D.; Ananda Raja, R.; Ghoshal, T.K.; Mukherjee, S.; Vijayan, K.K. Evaluation of growth, feed utilization efficiency and immune parameters in tiger shrimp (Penaeus monodon) fed diets supplemented with or diet fermented with gut bacterium Bacillus sp. DDKRC1. isolated from gut of Asian seabass (Lates calcarifer). Aquac. Res. 2018, 49, 2147–2155. [Google Scholar] [CrossRef]
- Lindstad, L.J.; Lo, G.; Leivers, S.; Lu, Z.; Michalak, L.; Pereira, G.V.; Rohr, A.K.; Martens, E.C.; McKee, L.S.; Louis, P.; et al. Human Gut Faecalibacterium prausnitzii Deploys a Highly Efficient Conserved System To Cross-Feed on beta-Mannan-Derived Oligosaccharides. mBio 2021, 12, e0362820. [Google Scholar] [CrossRef]
- Balta, I.; Linton, M.; Pinkerton, L.; Kelly, C.; Stef, L.; Pet, I.; Stef, D.; Criste, A.; Gundogdu, O.; Corcionivoschi, N. The effect of natural antimicrobials against Campylobacter spp. and its similarities to Salmonella spp., Listeria spp., Escherichia coli, Vibrio spp., Clostridium spp. and Staphylococcus spp. Food Control 2021, 121, 107745. [Google Scholar] [CrossRef]
- Balta, I.; Linton, M.; Pinkerton, L.; Kelly, C.; Ward, P.; Stef, L.; Pet, I.; Horablaga, A.; Gundogdu, O.; Corcionivoschi, N. The effect of natural antimicrobials on the Campylobacter coli T6SS+/- during in vitro infection assays and on their ability to adhere to chicken skin and carcasses. Int. J. Food Microbiol. 2021, 338, 108998. [Google Scholar] [CrossRef]
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Butucel, E.; Balta, I.; McCleery, D.; Marcu, A.; Stef, D.; Pet, I.; Callaway, T.; Stef, L.; Corcionivoschi, N. The Prebiotic Effect of an Organic Acid Mixture on Faecalibacterium prausnitzii Metabolism and Its Anti-Pathogenic Role against Vibrio parahaemolyticus in Shrimp. Biology 2023, 12, 57. https://doi.org/10.3390/biology12010057
Butucel E, Balta I, McCleery D, Marcu A, Stef D, Pet I, Callaway T, Stef L, Corcionivoschi N. The Prebiotic Effect of an Organic Acid Mixture on Faecalibacterium prausnitzii Metabolism and Its Anti-Pathogenic Role against Vibrio parahaemolyticus in Shrimp. Biology. 2023; 12(1):57. https://doi.org/10.3390/biology12010057
Chicago/Turabian StyleButucel, Eugenia, Igori Balta, David McCleery, Adela Marcu, Ducu Stef, Ioan Pet, Todd Callaway, Lavinia Stef, and Nicolae Corcionivoschi. 2023. "The Prebiotic Effect of an Organic Acid Mixture on Faecalibacterium prausnitzii Metabolism and Its Anti-Pathogenic Role against Vibrio parahaemolyticus in Shrimp" Biology 12, no. 1: 57. https://doi.org/10.3390/biology12010057
APA StyleButucel, E., Balta, I., McCleery, D., Marcu, A., Stef, D., Pet, I., Callaway, T., Stef, L., & Corcionivoschi, N. (2023). The Prebiotic Effect of an Organic Acid Mixture on Faecalibacterium prausnitzii Metabolism and Its Anti-Pathogenic Role against Vibrio parahaemolyticus in Shrimp. Biology, 12(1), 57. https://doi.org/10.3390/biology12010057