{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,26]],"date-time":"2026-10-26T22:50:30Z","timestamp":1793055030709,"version":"4.5.0"},"reference-count":59,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2022,10,19]],"date-time":"2022-10-19T00:00:00Z","timestamp":1666137600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Nutr."],"abstract":"<jats:p>The intestinal dysfunction induced by high plant protein diets is frequently observed in farmed fish, and probiotics of <jats:italic>Bacillus<\/jats:italic> genus were documented to benefit the intestinal health through the modulation of intestinal microbiota without clearness in its underlying mechanism yet. Fusobacteria, Proteobacteria, and Firmicutes were observed to be the dominate phyla, but their proportion differentiated in the intestinal bacterial community of Pengze crucian carp (<jats:italic>Carassius auratus<\/jats:italic> var. Pengze) fed different diets in this study. Dietary supplementation of <jats:italic>B. cereus and B. subtilis<\/jats:italic> could reshape the intestinal bacterial community altered by high plant protein diets through a notable reduction in opportunistic pathogen <jats:italic>Aeromonas<\/jats:italic> together with an increase in <jats:italic>Romboutsia<\/jats:italic> and\/or <jats:italic>Clostridium_sensu_stricto<\/jats:italic> from Firmicutes. Due to the alteration in the composition of bacterial community, Pengze crucian carp exhibited characteristic ecological networks dominated by cooperative interactions. Nevertheless, the increase in <jats:italic>Aeromonas<\/jats:italic> intensified the competition within bacterial communities and reduced the number of specialists within ecological network, contributing to the microbial dysbiosis induced by high plant protein diets. Two probiotics diets promoted the cooperation within the intestinal bacterial community and increased the number of specialists preferred to module hubs, and then further improved the homeostasis of the intestinal microbiota. Microbial dysbiosis lead to microbial dysfunction, and microbial lipopolysaccharide biosynthesis was observed to be elevated in high plant protein diets due to the increase in <jats:italic>Aeromonas<\/jats:italic>, gram-negative microbe. Probiotics <jats:italic>B. cereus and B. subtilis<\/jats:italic> restored the microbial function by elevating their amino acid and carbohydrate metabolism together with the promotion in the synthesis of primary and secondary bile acids. These results suggested that dietary supplementation of probiotics <jats:italic>B. cereus and B. subtilis<\/jats:italic> could restore the homeostasis and functions of intestinal microbiota in Pengze crucian carp fed high plant protein diets.<\/jats:p>","DOI":"10.3389\/fnut.2022.1027641","type":"journal-article","created":{"date-parts":[[2022,10,19]],"date-time":"2022-10-19T17:46:10Z","timestamp":1666201570000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":16,"title":["Probiotics Bacillus cereus and B. subtilis reshape the intestinal microbiota of Pengze crucian carp (Carassius auratus var. Pengze) fed with high plant protein diets"],"prefix":"10.3389","volume":"9","author":[{"given":"Jiamin","family":"Li","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Peng","family":"Fang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xinwen","family":"Yi","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Vikas","family":"Kumar","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mo","family":"Peng","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2022,10,19]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","first-page":"112271","DOI":"10.1016\/j.jenvman.2021.112271","article-title":"Aquaculture industry: supply and demand, best practices, effluent and its current issues and treatment technology","volume":"287","author":"Ahmad","year":"2021","journal-title":"J Environ Manage."},{"key":"B2","doi-asserted-by":"publisher","first-page":"83","DOI":"10.1016\/j.copbio.2020.11.014","article-title":"Contemporary aquaculture: implications for human nutrition","volume":"70","author":"Fiorella","year":"2021","journal-title":"Curr Opin Biotechnol."},{"key":"B3","doi-asserted-by":"publisher","first-page":"703","DOI":"10.1111\/raq.12347","article-title":"Risk assessment of the use of alternative animal and plant raw material resources in aquaculture feeds","volume":"12","author":"Glencross","year":"2020","journal-title":"Rev Aquacult."},{"key":"B4","doi-asserted-by":"publisher","first-page":"642","DOI":"10.1111\/raq.12492","article-title":"Nutritional immunity of fish intestines: Important insights for sustainable aquaculture","volume":"13","author":"Dawood","year":"2021","journal-title":"Rev Aquacult."},{"key":"B5","doi-asserted-by":"publisher","first-page":"644","DOI":"10.1111\/anu.12532","article-title":"Dietary effects of soybean products on gut microbiota and immunity of aquatic animals: a review","volume":"24","author":"Zhou","year":"2018","journal-title":"Aquacult Nutr."},{"key":"B6","doi-asserted-by":"publisher","first-page":"63","DOI":"10.1097\/MOG.0b013e32834d61e9","article-title":"The intestinal microbiota in health and disease","volume":"28","author":"Young","year":"2012","journal-title":"Curr Opin Gastroen."},{"key":"B7","doi-asserted-by":"publisher","first-page":"177","DOI":"10.1017\/S0029665118002719","article-title":"Gut microbiota and health: connecting actors across the metabolic system","volume":"78","author":"Fava","year":"2019","journal-title":"Proc Nutr Soc."},{"key":"B8","doi-asserted-by":"publisher","first-page":"36","DOI":"10.1016\/j.fsi.2021.07.007","article-title":"The functionality of probiotics in aquaculture: an overview","volume":"117","author":"El-Saadony","year":"2021","journal-title":"Fish Shellfish Immunol."},{"key":"B9","doi-asserted-by":"publisher","first-page":"820","DOI":"10.1016\/j.fsi.2019.02.010","article-title":"review on the application of Bacillus as probiotics in aquaculture","volume":"87","author":"Kuebutornye","year":"2019","journal-title":"Fish Shellfish Immunol."},{"key":"B10","doi-asserted-by":"publisher","first-page":"453","DOI":"10.1007\/978-3-030-85465-2_20","article-title":"Mechanisms of the beneficial effects of probiotic Bacillus spp. in aquaculture","author":"Kawser","year":"2022","journal-title":"Bacilli Agrobiotechnol."},{"key":"B11","doi-asserted-by":"publisher","first-page":"8","DOI":"10.1016\/j.fsi.2020.06.061","article-title":"Bacillus subtilis H2 modulates immune response, fat metabolism and bacterial flora in the gut of grass carp (Ctenopharyngodon idellus)","volume":"106","author":"Shi","year":"2020","journal-title":"Fish Shellfish Immunol."},{"key":"B12","doi-asserted-by":"publisher","first-page":"737625","DOI":"10.1016\/j.aquaculture.2021.737625","article-title":"Relationship between immune performance and the dominant intestinal microflora of turbot fed with different Bacillus species","volume":"549","author":"Ma","year":"2022","journal-title":"Aquaculture."},{"key":"B13","doi-asserted-by":"publisher","first-page":"1343","DOI":"10.1007\/s10499-021-00701-w","article-title":"Effects of dietary Bacillus licheniformis on growth performance, intestinal morphology, intestinal microbiome, and disease resistance in common carp (Cyprinus carpio L)","volume":"29","author":"Zhang","year":"2021","journal-title":"Aquacult Internat."},{"key":"B14","doi-asserted-by":"publisher","first-page":"244","DOI":"10.1111\/jwas.12724","article-title":"Potential of indigenous Bacillus spp. as probiotic feed supplements in an extruded low-fish-meal diet for juvenile olive flounder, Paralichthys olivaceus","volume":"52","author":"Niu","year":"2021","journal-title":"J World Aquacult Soc"},{"key":"B15","doi-asserted-by":"publisher","first-page":"2494","DOI":"10.3390\/microorganisms9122494","article-title":"Probiotic Bacillus safensis NPUST1 administration improves growth performance, gut microbiota, and innate immunity against Streptococcus iniae in Nile tilapia (Oreochromis niloticus)","volume":"9","author":"Wu","year":"2021","journal-title":"Microorganisms."},{"key":"B16","doi-asserted-by":"publisher","first-page":"735798","DOI":"10.1016\/j.aquaculture.2020.735798","article-title":"Dietary cinnamaldehyde and Bacillus subtilis improve growth performance, digestive enzyme activity, and antioxidant capability and shape intestinal microbiota in tongue sole, Cynoglossus semilaevis","volume":"531","author":"Wang","year":"2021","journal-title":"Aquaculture"},{"key":"B17","doi-asserted-by":"publisher","first-page":"663","DOI":"10.1126\/science.aad2602","article-title":"The ecology of the microbiome: networks, competition, and stability","volume":"350","author":"Coyte","year":"2015","journal-title":"Science."},{"key":"B18","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1186\/s12916-016-0629-z","article-title":"Probiotics and microbiota composition","volume":"14","author":"Sanders","year":"2016","journal-title":"BMC Med."},{"key":"B19","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1038\/srep09336","article-title":"Lactobacillus rhamnosus lowers zebrafish lipid content by changing gut microbiota and host transcription of genes involved in lipid metabolism","volume":"5","author":"Falcinelli","year":"2015","journal-title":"Sci Rep."},{"key":"B20","doi-asserted-by":"publisher","first-page":"259","DOI":"10.1038\/nature04927","article-title":"Ecological networks and their fragility","volume":"442","author":"Montoya","year":"2006","journal-title":"Nature."},{"key":"B21","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1038\/s41598-017-05312-1","article-title":"Molecular ecological network analysis reveals the effects of probiotics and florfenicol on intestinal microbiota homeostasis: an example of sea cucumber","volume":"7","author":"Yang","year":"2017","journal-title":"Sci Rep."},{"key":"B22","doi-asserted-by":"publisher","first-page":"718","DOI":"10.1007\/s13238-010-0093-z","article-title":"Human gut microbiome: the second genome of human body","volume":"1","author":"Zhu","year":"2010","journal-title":"Protein Cell."},{"key":"B23","doi-asserted-by":"publisher","first-page":"573","DOI":"10.1053\/j.gastro.2020.10.057","article-title":"Metabolism and metabolic disorders and the microbiome: the intestinal microbiota associated with obesity, lipid metabolism, and metabolic health\u2014pathophysiology and therapeutic strategies","volume":"160","author":"Aron-Wisnewsky","year":"2021","journal-title":"Gastroenterology."},{"key":"B24","doi-asserted-by":"publisher","first-page":"1105","DOI":"10.3390\/ijms23031105","article-title":"Gut microbiota and short chain fatty acids: implications in glucose homeostasis","volume":"23","author":"Portincasa","year":"2022","journal-title":"Int J Mol Sci."},{"key":"B25","doi-asserted-by":"publisher","first-page":"2083","DOI":"10.1007\/s00726-017-2493-3","article-title":"review of the relationship between the gut microbiota and amino acid metabolism","volume":"49","author":"Lin","year":"2017","journal-title":"Amino Acids."},{"key":"B26","doi-asserted-by":"publisher","first-page":"1525","DOI":"10.1053\/j.gastro.2014.02.008","article-title":"Role of the microbiome in energy regulation and metabolism","volume":"146","author":"Nieuwdorp","year":"2014","journal-title":"Gastroenterology."},{"key":"B27","doi-asserted-by":"publisher","first-page":"723","DOI":"10.1093\/icb\/icx020","article-title":"Beyond fermentation: other important services provided to endothermic herbivores by their gut microbiota","volume":"57","author":"Dearing","year":"2017","journal-title":"Integr Comp Biol."},{"key":"B28","doi-asserted-by":"publisher","first-page":"151","DOI":"10.1016\/j.aquaculture.2018.08.062","article-title":"Changes in microbiota along the intestine of grass carp (Ctenopharyngodon idella): community, interspecific interactions, and functions","volume":"498","author":"Yang","year":"2019","journal-title":"Aquaculture."},{"key":"B29","doi-asserted-by":"publisher","first-page":"100828","DOI":"10.1016\/j.aqrep.2021.100828","article-title":"Effects of dietary sodium butyrate on growth performance, antioxidant capacity, intestinal histomorphology and immune response in juvenile Pengze crucian carp (Carassius auratus Pengze)","volume":"21","author":"Fang","year":"2021","journal-title":"Aquacult Rep."},{"key":"B30","doi-asserted-by":"publisher","first-page":"100435","DOI":"10.1016\/j.aqrep.2020.100435","article-title":"The effects of substituting fish meal with soy protein concentrate on growth performance, antioxidant capacity and intestinal histology in juvenile golden crucian carp, Cyprinus carpio \u00d7 Carassius auratus","volume":"18","author":"Zhu","year":"2020","journal-title":"Aquacult Rep"},{"key":"B31","doi-asserted-by":"publisher","first-page":"18","DOI":"10.3390\/fishes7010018","article-title":"Effects of dietary Enterococcus faecalis YFI-G720 on the growth, immunity, serum biochemical, intestinal morphology, intestinal microbiota, and disease resistance of crucian carp (Carassius auratus)","volume":"7","author":"Xu","year":"2022","journal-title":"Fishes."},{"key":"B32","doi-asserted-by":"publisher","first-page":"322","DOI":"10.1016\/j.fsi.2018.04.055","article-title":"Probiotic potential of Bacillus velezensis JW: antimicrobial activity against fish pathogenic bacteria and immune enhancement effects on Carassius auratus","volume":"78","author":"Yi","year":"2018","journal-title":"Fish Shellfish Immunol"},{"key":"B33","doi-asserted-by":"publisher","first-page":"2663","DOI":"10.3389\/fmicb.2019.02663","article-title":"Effect of Bacillus velezensis on Aeromonas veronii-induced intestinal mucosal barrier function damage and inflammation in crucian carp (Carassius auratus)","volume":"10","author":"Zhang","year":"2019","journal-title":"Front Microbiol."},{"key":"B34","doi-asserted-by":"publisher","first-page":"559","DOI":"10.1007\/s12602-018-9428-5","article-title":"Effect of dietary probiotic Lactobacillus helveticus on growth performance, antioxidant levels, and absorption of essential trace elements in goldfish (Carassius auratus)","volume":"11","author":"Ahire","year":"2019","journal-title":"Probiotics Antimicrob Proteins."},{"key":"B35","doi-asserted-by":"publisher","first-page":"735691","DOI":"10.1016\/j.aquaculture.2020.735691","article-title":"Probiotic (Bacillus cereus) enhanced growth of Pengze crucian carp concurrent with modulating the antioxidant defense response and exerting beneficial impacts on inflammatory response via Nrf2 activation","volume":"529","author":"Yang","year":"2020","journal-title":"Aquaculture."},{"key":"B36","doi-asserted-by":"publisher","first-page":"2207","DOI":"10.1111\/are.14102","article-title":"Dietary supplementation of Bacillus cereus as probiotics in Pengze crucian carp (Carassius auratus var. Pengze): effects on growth performance, fillet quality, serum biochemical parameters and intestinal histology","volume":"50","author":"Yang","year":"2019","journal-title":"Aquacult Res."},{"key":"B37","doi-asserted-by":"publisher","first-page":"106","DOI":"10.1016\/j.aquaculture.2019.04.064","article-title":"Effects of dietary supplementation with \u03b2-glucan and Bacillus subtilis on growth, fillet quality, immune capacity, and antioxidant status of Pengze crucian carp (Carassius auratus var","volume":"508","author":"Cao","year":"2019","journal-title":"Pengze) Aquaculture."},{"key":"B38","doi-asserted-by":"publisher","first-page":"98","DOI":"10.1016\/j.bbrc.2015.01.074","article-title":"Intestinal microbiota and immune related genes in sea cucumber (Apostichopus japonicus) response to dietary \u03b2-glucan supplementation","volume":"458","author":"Yang","year":"2015","journal-title":"Biochem Biophys Res Commun."},{"key":"B39","doi-asserted-by":"publisher","first-page":"e2584","DOI":"10.7717\/peerj.2584","article-title":"a versatile open source tool for metagenomics","volume":"4","author":"Rognes","year":"2016","journal-title":"PeerJ."},{"key":"B40","first-page":"32","volume-title":"Permutational Multivariate Analysis of Variance","author":"Anderson","year":"2005"},{"key":"B41","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1186\/1471-2105-13-113","article-title":"Molecular ecological network analyses","volume":"13","author":"Deng","year":"2012","journal-title":"BMC Bioinf."},{"key":"B42","doi-asserted-by":"publisher","first-page":"685","DOI":"10.1038\/s41587-020-0548-6","article-title":"PICRUSt2 for prediction of metagenome functions","volume":"38","author":"Douglas","year":"2020","journal-title":"Nat Biotechnol."},{"key":"B43","doi-asserted-by":"publisher","first-page":"117","DOI":"10.1111\/j.1442-9993.1993.tb00438.x","article-title":"Non-parametric multivariate analyses of changes in community structure","volume":"18","author":"Clarke","year":"1993","journal-title":"Austral Ecol."},{"key":"B44","doi-asserted-by":"publisher","first-page":"3123","DOI":"10.1093\/bioinformatics\/btu494","article-title":"STAMP statistical analysis of taxonomic and functional profiles","volume":"30","author":"Parks","year":"2014","journal-title":"Bioinformatics."},{"key":"B45","doi-asserted-by":"publisher","first-page":"1077","DOI":"10.1111\/raq.12513","article-title":"Microbiome diversity and dysbiosis in aquaculture","volume":"13","author":"Infante-Villamil","year":"2021","journal-title":"Rev Aquacult."},{"key":"B46","doi-asserted-by":"publisher","first-page":"100472","DOI":"10.1016\/j.aqrep.2020.100472","article-title":"Replacement of fishmeal with soybean meal affects the growth performance, digestive enzymes, intestinal microbiota and immunity of Carassius auratus gibelio\u2640 \u00d7 Cyprinus carpio\u2642","volume":"18","author":"Liu","year":"2020","journal-title":"Aquacult Rep."},{"key":"B47","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/j.aquaculture.2016.11.042","article-title":"The use of probiotic bacteria against Aeromonas infections in salmonid aquaculture","volume":"469","author":"Fe\u010dkaninov\u00e1","year":"2017","journal-title":"Aquaculture."},{"key":"B48","doi-asserted-by":"publisher","first-page":"185","DOI":"10.1016\/j.micpath.2017.03.037","article-title":"Pathogenic potentials of Aeromonas species isolated from aquaculture and abattoir environments","volume":"107","author":"Igbinosa","year":"2017","journal-title":"Microb Pathogen."},{"key":"B49","doi-asserted-by":"publisher","first-page":"e00122","DOI":"10.1128\/mBio.00122-11","article-title":"Phylogenetic molecular ecological network of soil microbial communities in response to elevated CO2","volume":"2","author":"Zhou","year":"2011","journal-title":"MBio."},{"key":"B50","volume-title":"The Theory of Island Biogeography","author":"Wilson","year":"1967"},{"key":"B51","doi-asserted-by":"publisher","first-page":"1413","DOI":"10.1038\/ismej.2015.212","article-title":"Privatization of cooperative benefits stabilizes mutualistic cross-feeding interactions in spatially structured environments","volume":"10","author":"Pande","year":"2016","journal-title":"ISME J."},{"key":"B52","doi-asserted-by":"crossref","DOI":"10.23919\/ECC.2019.8796069","article-title":"Cooperation enhances robustness of coexistence in spatially structured consortia","volume-title":"2019 18th European Control Conference (ECC)","author":"Ren","year":"2019"},{"key":"B53","doi-asserted-by":"publisher","first-page":"19891","DOI":"10.1073\/pnas.0706375104","article-title":"The modularity of pollination networks","volume":"104","author":"Olesen","year":"2007","journal-title":"PNAS."},{"key":"B54","doi-asserted-by":"publisher","first-page":"90","DOI":"10.5217\/ir.2014.12.2.90","article-title":"Lipopolysaccharide: basic biochemistry, intracellular signaling, and physiological impacts in the gut","volume":"12","author":"Rhee","year":"2014","journal-title":"Intestinal Res."},{"key":"B55","doi-asserted-by":"publisher","first-page":"137","DOI":"10.1007\/BF00446812","article-title":"Amino acid utilization patterns in clostridial taxonomy","volume":"123","author":"Elsden","year":"1979","journal-title":"Arch Microbiol."},{"key":"B56","doi-asserted-by":"publisher","first-page":"1768","DOI":"10.2741\/3820","article-title":"Amino acid metabolism in intestinal bacteria: links between gut ecology and host health","volume":"16","author":"Dai","year":"2011","journal-title":"Front Biosci-Landmark."},{"key":"B57","doi-asserted-by":"publisher","first-page":"31","DOI":"10.1016\/S0065-2911(08)60015-6","article-title":"Physiology of carbohydrate to solvent conversion by clostridia","volume":"39","author":"Mitchell","year":"1997","journal-title":"Adv Microb Physiol."},{"key":"B58","doi-asserted-by":"publisher","first-page":"148","DOI":"10.1016\/j.copbio.2012.11.007","article-title":"Microbe\u2013microbe interactions in mixed culture food fermentations","volume":"24","author":"Smid","year":"2013","journal-title":"Curr Opin Biotechnol."},{"key":"B59","doi-asserted-by":"publisher","first-page":"1700300","DOI":"10.1002\/mnfr.201700300","article-title":"Consumption of two healthy dietary patterns restored microbiota dysbiosis in obese patients with metabolic dysfunction","volume":"61","author":"Haro","year":"2017","journal-title":"Mol Nutr Food Res."}],"container-title":["Frontiers in Nutrition"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fnut.2022.1027641\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,10,19]],"date-time":"2022-10-19T17:46:12Z","timestamp":1666201572000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fnut.2022.1027641\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,10,19]]},"references-count":59,"alternative-id":["10.3389\/fnut.2022.1027641"],"URL":"https:\/\/doi.org\/10.3389\/fnut.2022.1027641","relation":{},"ISSN":["2296-861X"],"issn-type":[{"value":"2296-861X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,10,19]]},"article-number":"1027641"}}