Abstract
This study investigated the compound probiotics and heat-killed compound probiotics on antioxidants, plasma biochemical parameters, intestinal histopathology, and microbiome of koi fish, Cyprinus carpio haematopterus. Koi fish (15.9 ± 0.63 g) were fed with five different diets: C (control, basal diet without probiotics), D3 (3% compound probiotics), D6 (6% compound probiotics), lnaD3 (3% heat-killed compound probiotics), and lnaD6 (6% heat-killed compound probiotics). After 28 days of the feeding trial, results showed that the activities of acid phosphatase (ACP), alkaline phosphatase (AKP), catalase (CAT), and total superoxide dismutase (T-SOD) were significantly improved in koi fish fed with heat-killed compound probiotics compared to the control group (P < 0.05). Interestingly, total activities of glutamyl oxaloacetic transaminase (GOT), total protein (TP), albumin (TA), globulin (GLB), and triglyceride (TG) were significantly improved in koi fish fed with compound probiotics compared to the control group (P < 0.05). The intestinal muscular and intestinal villi height of lnaD3 was significantly higher than other groups (P < 0.05). In addition, compound probiotics and heat-killed compound probiotics increased the diversity of intestinal microbes. Therefore, dietary supplementation with heat-killed compound probiotics can be an effective measure for improving nonspecific immune response, intestinal morphology, and the flora of koi fish.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
All data, models, and code generated or used during the study appear in the submitted article.
References
Abd El-Rhman AM, Khattab YA, Shalaby AM (2009) Micrococcus luteus and Pseudomonas species as probiotics for promoting the growth performance and health of Nile tilapia. Oreochromis Niloticus Shellfish Immunol 27(2):175–180. https://doi.org/10.1016/j.fsi.2009.03.020
Aberoum A, Jooyandeh H (2010) A review on occurrence and characterization of the Aeromonas species from marine fishes. World J Fish Mar Sci 2(6):519–523. https://doi.org/10.1016/s0025-326x(02)00143-1
Aly SM, Ahmed YA-G, Ghareeb AA-A, Mohamed MF (2008) Studies on Bacillus subtilis and Lactobacillus acidophilus, as potential probiotics, on the immune response and resistance of Tilapia nilotica (Oreochromis niloticus) to challenge infections. Fish Shellfish Immunol 25(1–2):128–136. https://doi.org/10.1016/j.fsi.2008.03.013
Amenyogbe E, Chen G, Wang Z, Huang J, Huang B, Li H (2020) The exploitation of probiotics, prebiotics and synbiotics in aquaculture: present study, limitations and future directions: a review. Aquac Int 28(3):1017–1041. https://doi.org/10.1007/s10499-020-00509-0
Balcázar JL, De Blas I, Ruiz-Zarzuela I, Vendrell D, Gironés O, Muzquiz JL (2007) Enhancement of the immune response and protection induced by probiotic lactic acid bacteria against furunculosis in rainbow trout (Oncorhynchus mykiss). FEMS Immunol Med Microbiol 51(1):185–193. https://doi.org/10.1111/j.1574-695X.2007.00294.x
Biswas G, Korenaga H, Nagamine R, Takayama H, Kawahara S, Takeda S, Kikuchi Y, Dashnyam B, Kono T, Sakai M (2013) Cytokine responses in the Japanese pufferfish (Takifugu rubripes) head kidney cells induced with heat-killed probiotics isolated from the Mongolian dairy products. Fish Shellfish Immunol 34(5):1170–1177. https://doi.org/10.1016/j.fsi.2013.01.024
Cardona E, Gueguen Y, Magré K, Lorgeoux B, Piquemal D, Pierrat F, Noguier F, Saulnier D (2016) Bacterial community characterization of water and intestine of the shrimp Litopenaeus stylirostris in a biofloc system. BMC Microbiol 16(1):1–9. https://doi.org/10.1186/s12866-016-0770-z
Carnevali O, Maradonna F, Gioacchini G (2017) Integrated control of fish metabolism, wellbeing and reproduction: the role of probiotic. Aquaculture 472:144–155. https://doi.org/10.1016/j.aquaculture.2016.03.037
Chiu S-T, Chu T-W, Simangunsong T, Ballantyne R, Chiu C-S, Liu C-H (2021) Probiotic, Lactobacillus pentosus BD6 boost the growth and health status of white shrimp, Litopenaeus vannamei via oral administration. Fish Shellfish Immunol 117:124–135. https://doi.org/10.1016/j.fsi.2021.07.024
Čížek A, Dolejská M, Sochorová R, Strachotová K, Piačková V, Veselý T (2010) Antimicrobial resistance and its genetic determinants in aeromonads isolated in ornamental (koi) carp (Cyprinus carpio koi) and common carp (Cyprinus carpio). Vet Microbiol 142(3–4):435–439. https://doi.org/10.1016/j.vetmic.2009.10.001
Dawood MA, Koshio S, Ishikawa M, Yokoyama S (2015) Effects of heat killed Lactobacillus plantarum (LP20) supplemental diets on growth performance, stress resistance and immune response of red sea bream, Pagrus major. Aquaculture 442:29–36. https://doi.org/10.1016/j.aquaculture.2015.02.005
Dawood MA, Magouz FI, Salem MF, Abdel-Daim HA (2019) Modulation of digestive enzyme activity, blood health, oxidative responses and growth-related gene expression in GIFT by heat-killed Lactobacillus plantarum (L-137). Aquaculture 505:127–136. https://doi.org/10.1016/j.aquaculture.2019.02.053
Demirci B, Terzi F, Kesbic OS, Acar U, Yilmaz S, Kesbic FI (2021) Does dietary incorporation level of pea protein isolate influence the digestive system morphology in rainbow trout ( Oncorhynchus mykiss )? Anat Histol Embryol 50(6):956–964. https://doi.org/10.1111/ahe.12740
Díaz-Rosales P, Salinas I, Rodríguez A, Cuesta A, Chabrillón M, Balebona MC, Moriñigo MÁ, Esteban MÁ, Meseguer J (2006) Gilthead seabream (Sparus aurata L.) innate immune response after dietary administration of heat-inactivated potential probiotics. Fish Shellfish Immunol 20(4):482–492. https://doi.org/10.1016/j.fsi.2005.06.007
Díaz-Rosales P, Arijo S, Chabrillón M, Alarcón F, Tapia-Paniagua S, Martínez-Manzanares E, Balebona M, Moriñigo M (2009) Effects of two closely related probiotics on respiratory burst activity of Senegalese sole (Solea senegalensis, Kaup) phagocytes, and protection against Photobacterium damselae subsp. piscicida. Aquaculture 293(1–2):16–21. https://doi.org/10.1016/j.aquaculture.2009.03.050
Dowidar M, Abd ElAzeem S, Khater A, Awad Somayah M, Metwally S (2018) Improvement of growth performance, immunity and disease resistance in Nile tilapia, Oreochromis niloticus, by using dietary probiotics supplementation. J AnimSci Vet Med 3(2):35–46. https://doi.org/10.31248/JASVM2018.076
Duc PM, Myo HN, Hoa TTT, Liem PT, Onoda S, Hien TTT (2020) Effects of heat killed Lactobacillus plantarum (HK L-137) supplemental diets on growth, survival and health of juvenile striped catfish, Pangasianodon hypophthalmus. Int J Sci Res Publ 10(3):761–767. https://doi.org/10.29322/ijsrp.10.03.2020.p9993
El-Saadony MT, Alagawany M, Patra AK, Kar I, Tiwari R, Dawood MA, Dhama K, Abdel-Latif HM (2021) The functionality of probiotics in aquaculture: an overview. Fish Shellfish Immunol 117:36–52. https://doi.org/10.1016/j.fsi.2021.07.007
Elsabagh M, Mohamed R, Moustafa EM, Hamza A, Farrag F, Decamp O, Dawood MA, Eltholth M (2018) Assessing the impact of Bacillus strains mixture probiotic on water quality, growth performance, blood profile and intestinal morphology of Nile tilapia. Oreochromis Niloticus Aquac Nutr 24(6):1613–1622. https://doi.org/10.1111/anu.12797
Falcinelli S, Picchietti S, Rodiles A, Cossignani L, Merrifield DL, Taddei AR, Maradonna F, Olivotto I, Gioacchini G, Carnevali O (2015) Lactobacillus rhamnosus lowers zebrafish lipid content by changing gut microbiota and host transcription of genes involved in lipid metabolism. Sci Rep 5(1):1–11. https://doi.org/10.1038/srep09336
Feng Z, Song X, Zhao L, Zhu W (2020) Isolation of probiotics and their effects on growth, antioxidant and non-specific immunity of sea cucumber Apostichopus japonicus. Fish Shellfish Immunol 106:1087–1094. https://doi.org/10.1016/j.fsi.2020.08.049
Frouël S, Le Bihan E, Serpentini A, Lebel J, Koueta N, Nicolas J (2008) Preliminary study of the effects of commercial lactobacilli preparations on digestive metabolism of juvenile sea bass (Dicentrarchus labrax). Microbial Physiol 14(1–3):100–106. https://doi.org/10.1159/000106088
Gayed MA, Elabd H, Tageldin M, Abbass A (2021) Probiotic Zado®(Ruminococcus Flavefaciens) boosts hematology, immune, serum proteins, and growth profiles in Nile tilapia (Oreochromis niloticus). Fish Shellfish Immunol Rep 2:100021. https://doi.org/10.1016/j.fsirep.2021.100021
Giri SS, Sukumaran V, Sen SS, Vinumonia J, Banu BN, Jena PK (2011) Antagonistic activity of cellular components of potential probiotic bacteria, isolated from the gut of Labeo rohita, against Aeromonas hydrophila. Probiotics Antimicrob Proteins 3(3):214–222. https://doi.org/10.1007/s12602-011-9078-3
Giri SS, Sukumaran V, Oviya M (2013) Potential probiotic Lactobacillus plantarum VSG3 improves the growth, immunity, and disease resistance of tropical freshwater fish. Labeo Rohita Fish Shellfish Immunol 34(2):660–666. https://doi.org/10.1016/j.fsi.2012.12.008
Giri SS, Jun JW, Yun S, Kim HJ, Kim SG, Kim SW, Woo KJ, Han SJ, Oh WT, Kwon J, Sukumaran V, Park SC (2020) Effects of dietary heat-killed Pseudomonas aeruginosa strain VSG2 on immune functions, antioxidant efficacy, and disease resistance in Cyprinus carpio. Aquaculture 514:734489. https://doi.org/10.1016/j.aquaculture.2019.734489
Gomez D, Sunyer JO, Salinas I (2013) The mucosal immune system of fish: the evolution of tolerating commensals while fighting pathogens. Fish Shellfish Immunol 35(6):1729–1739. https://doi.org/10.1016/j.fsi.2013.09.032
Guangxin G, Li K, Zhu Q, Zhao C, Li C, He Z, Hu S, Ren Y (2022) Improvements of immune genes and intestinal microbiota composition of turbot (Scophthalmus maximus) with dietary oregano oil and probiotics. Aquaculture 547:737442. https://doi.org/10.1016/j.aquaculture.2021.737442
Haque MM, Hasan NA, Eltholth MM, Saha P, Mely SS, Rahman T, Murray FJ (2021) Assessing the impacts of in-feed probiotic on the growth performance and health condition of pangasius (Pangasianodon hypophthalmus) in a farm trial. Aquac Rep 20:100699. https://doi.org/10.1016/j.aqrep.2021.100699
Islam SM, Rohani MF, Shahjahan M (2021) Probiotic yeast enhances growth performance of Nile tilapia (Oreochromis niloticus) through morphological modifications of intestine. Aquac Rep 21:100800. https://doi.org/10.1016/j.aqrep.2021.100800
Jahan N, Islam SM, Rohani MF, Hossain MT, Shahjahan M (2021) Probiotic yeast enhances growth performance of rohu (Labeo rohita) through upgrading hematology, and intestinal microbiota and morphology. Aquaculture 545:737243. https://doi.org/10.1016/j.aquaculture.2021.737243
Jiang H-F, Liu X-L, Chang Y-Q, Liu M-T, Wang G-X (2013) Effects of dietary supplementation of probiotic Shewanella colwelliana WA64, Shewanella olleyana WA65 on the innate immunity and disease resistance of abalone, Haliotis discus hannai Ino. Fish Shellfish Immunol 35(1):86–91. https://doi.org/10.1016/j.fsi.2013.04.009
Karlsson FH, Ussery DW, Nielsen J, Nookaew I (2011) A closer look at bacteroides: phylogenetic relationship and genomic implications of a life in the human gut. Microb Ecol 61(3):473–485. https://doi.org/10.1007/s00248-010-9796-1
Kesbiç OS, Yiğit M, Acar Ü (2016) Effects of tank color on growth performance and nitrogen excretion of European seabass (Dicentrarchus labrax) juveniles. Proc National Acad Sci, India Section b: Biol Sci 86(1):205–210. https://doi.org/10.1007/s40011-014-0441-5
Kesbiç OS, Acar Ü, Yilmaz S, Aydin ÖD (2020) Effects of bergamot (Citrus bergamia) peel oil-supplemented diets on growth performance, haematology and serum biochemical parameters of Nile tilapia (Oreochromis niloticus). Fish Physiol Biochem 46(1):103–110. https://doi.org/10.1007/s10695-019-00700-y
Khalafalla MM, Ibrahim SA, Zayed MM, Awad MN, Mohamed RA (2020) Effect of a dietary mixture of beneficial bacteria on growth performance, health condition, chemical composition, and water quality of Nile Tilapia, Oreochromis niloticus fingerlings. J Aquat Food Prod Technol 29(8):823–835. https://doi.org/10.1080/10498850.2020.1764685
Khojasteh B (2012) The morphology of the post-gastric alimentary canal in teleost fishes: A brief review. Int J Aquat Sci 3:71–88
Kuebutornye FK, Tang J, Cai J, Yu H, Wang Z, Abarike ED, Lu Y, Li Y, Afriyie G (2020) In vivo assessment of the probiotic potentials of three host-associated Bacillus species on growth performance, health status and disease resistance of Oreochromis niloticus against Streptococcus agalactiae. Aquaculture 527:735440. https://doi.org/10.1016/j.aquaculture.2020.735440
Lee S, Katya K, Park Y, Won S, Seong M, Hamidoghli A, Bai SC (2017) Comparative evaluation of dietary probiotics Bacillus subtilis WB60 and Lactobacillus plantarum KCTC3928 on the growth performance, immunological parameters, gut morphology and disease resistance in Japanese eel, Anguilla japonica. Fish Shellfish Immunol 61:201–210. https://doi.org/10.1016/j.fsi.2016.12.035
Lemaire P, Drai P, Mathieu A, Lemaire S, Carriere S, Giudicelli J, Lafaurie M (1991) Changes with different diets in plasma enzymes (GOT, GPT, LDH, ALP) and plasma lipids (cholesterol, triglycerides) of sea-bass (Dicentrarchus labrax). Aquaculture 93(1):63–75. https://doi.org/10.1016/0044-8486(91)90205-L
Li J, Wu Z-B, Zhang Z, Zha J-W, Qu S-Y, Qi X-Z, Wang G-X, Ling F (2019) Effects of potential probiotic Bacillusvelezensis K2 on growth, immunity and resistance to Vibrio harveyi infection of hybrid grouper (Epinephelus lanceolatus♂×E. fuscoguttatus♀. us Fish Shellfish Immunol 93:1047–1055
Makridis P, Martins S, Reis J, Dinis MT (2008) Use of probiotic bacteria in the rearing of Senegalese sole (Solea senegalensis) larvae. Aquac Res 39(6):627–634. https://doi.org/10.1111/j.1365-2109.2008.01933.x
Maynard CL, Elson CO, Hatton RD, Weaver CT (2012) Reciprocal interactions of the intestinal microbiota and immune system. Nature 489(7415):231–241. https://doi.org/10.1038/nature11551
Megarani DV, Hardian AB, Arifianto D, Santosa CM, Salasia SI (2020) Comparative morphology and morphometry of blood cells in zebrafish (Danio rerio), common carp (Cyprinus carpio carpio), and tilapia (Oreochromis niloticus). J Am Assoc Lab Anim Sci 59(6):673–680. https://doi.org/10.30802/aalas-jaalas-20-000013
Mohammadian T, Monjezi N, Peyghan R, Mohammadian B (2022) Effects of dietary probiotic supplements on growth, digestive enzymes activity, intestinal histomorphology and innate immunity of common carp (Cyprinus carpio): a field study. Aquaculture 549:737787. https://doi.org/10.1016/j.aquaculture.2021.737787
Munoz-Atienza E, Araújo C, Lluch N, Hernández PE, Herranz C, Cintas LM, Magadán S (2015) Different impact of heat-inactivated and viable lactic acid bacteria of aquatic origin on turbot (Scophthalmus maximus L.) head-kidney leucocytes. Fish Shellfish Immunol 44(1):214–223. https://doi.org/10.1016/j.fsi.2015.02.021
Nayak SK (2010) Probiotics and immunity: a fish perspective. Fish Shellfish Immunol 29(1):2–14. https://doi.org/10.1016/j.fsi.2010.02.017
Nofouzi K, Sheikhzadeh N, Varshoie H, Sharabyani SK, Jafarnezhad M, Shabanzadeh S, Ahmadifar E, Stanford J, Shahbazfar AA (2019) Beneficial effects of killed Tsukamurella inchonensis on rainbow trout (Oncorhynchus mykiss) growth, intestinal histology, immunological, and biochemical parameters. Fish Physiol Biochem 45(1):209–217. https://doi.org/10.1007/s10695-018-0555-4
Pan X, Wu T, Song Z, Tang H, Zhao Z (2008) Immune responses and enhanced disease resistance in Chinese drum, Miichthys miiuy (Basilewsky), after oral administration of live or dead cells of Clostridium butyrium CB2. J Fish Dis 31(9):679–686. https://doi.org/10.1111/j.1365-2761.2008.00955.x
Patriche T, Patriche N, Tenciu M (2009) Cyprinids total blood proteins determination. Lucrări Ştiinţifice Zootehnie Şi Biotechnologii 42(2):95–101
Peng Z, Yan L, Wei L, Gao X, Shi L, Ren T, Han Y (2022) Effect of dietary chicken gut meal levels on growth performance, plasma biochemical parameters, digestive ability and fillet quality of Cyprinus carpio. Aquac Rep 24:101183. https://doi.org/10.1016/j.aqrep.2022.101183
Putri FP, Dewi NN (2019) Growth monitoring of koi fish (Cypri nus carpio) in natural hatchery techniques in Umbulan, Pasuruan, East Java. IOP Conf Series: Earth Environ Sci 236(1):012016–012018. https://doi.org/10.1088/1755-1315/236/1/012016
Ramos MA, Gonçalves JFM, Batista S, Costas B, Pires MA, Rema P, Ozório ROA (2015) Growth, immune responses and intestinal morphology of rainbow trout (Oncorhynchus mykiss) supplemented with commercial probiotics. Fish Shellfish Immunol 45(1):19–26. https://doi.org/10.1016/j.fsi.2015.04.001
Ramos MA, Batista S, Pires MA, Silva AP, Pereira LF, Saavedra MJ, Ozório ROA, Rema P (2017) Dietary probiotic supplementation improves growth and the intestinal morphology of Nile tilapia. Animal 11(8):1259–1269. https://doi.org/10.1017/S1751731116002792
Rekecki A, Dierckens K, Laureau S, Boon N, Bossier P, Van den Broeck W (2009) Effect of germ-free rearing environment on gut development of larval sea bass (Dicentrarchus labrax L.). Aquaculture 293(1):8–15. https://doi.org/10.1016/j.aquaculture.2009.04.001
Salinas I, Abelli L, Bertoni F, Picchietti S, Roque A, Furones D, Cuesta A, Meseguer J, Esteban MÁ (2008) Monospecies and multispecies probiotic formulations produce different systemic and local immunostimulatory effects in the gilthead seabream (Sparus aurata L.). Fish Shellfish Immunol 25(1):114–123. https://doi.org/10.1016/j.fsi.2008.03.011
Santos L, Ramos F (2016) Analytical strategies for the detection and quantification of antibiotic residues in aquaculture fishes: a review. Trends Food Sci Technol 52:16–30. https://doi.org/10.1016/j.tifs.2016.03.015
Saputra F, Shiu Y-L, Chen Y-C, Puspitasari AW, Danata RH, Liu C-H, Hu S-Y (2016) Dietary supplementation with xylanase-expressing B. áamyloliquefaciens R8 improves growth performance and enhances immunity against Aeromonas hydrophila in Nile tilapia (Oreochromis niloticus). Fish Shellfish Immunol 58:397–405. https://doi.org/10.1016/j.fsi.2016.09.046
Saravanan K, Sivaramakrishnan T, Praveenraj J, Kiruba-Sankar R, Haridas H, Kumar S, Varghese B (2021) Effects of single and multi-strain probiotics on the growth, hemato-immunological, enzymatic activity, gut morphology and disease resistance in Rohu Labeo rohita. Aquaculture 540:736749. https://doi.org/10.1016/j.aquaculture.2021.736749
Segawa S, Nakakita Y, Takata Y, Wakita Y, Kaneko T, Kaneda H, Watari J, Yasui H (2008) Effect of oral administration of heat-killed Lactobacillus brevis SBC8803 on total and ovalbumin-specific immunoglobulin E production through the improvement of Th1/Th2 balance. Int J Food Microbiol 121(1):1–10. https://doi.org/10.1016/j.ijfoodmicro.2007.10.004
Shelby RA, Lim C, Yildirim-Aksoy M, Delaney MA (2006) Effects of probiotic diet supplements on disease resistance and immune response of young Nile tilapia, Oreochromis niloticus. J Appl Aquac 18(2):23–34. https://doi.org/10.1300/j028v18n02_02
Tan X, Sun Z, Chen S, Chen S, Huang Z, Zhou C, Zou C, Liu Q, Ye H, Lin H, Ye C, Wang A (2017) Effects of dietary dandelion extracts on growth performance, body composition, plasma biochemical parameters, immune responses and disease resistance of juvenile golden pompano Trachinotus ovatus. Fish Shellfish Immunol 66:198–206. https://doi.org/10.1016/j.fsi.2017.05.028
Taverniti V, Guglielmetti S (2011) The immunomodulatory properties of probiotic microorganisms beyond their viability (ghost probiotics: proposal of paraprobiotic concept). Genes Nutr 6(3):261–274. https://doi.org/10.1007/s12263-011-0218-x
Van Doan H, Hoseinifar SH, Naraballobh W, Jaturasitha S, Tongsiri S, Chitmanat C, Ringø E (2019) Dietary inclusion of orange peels derived pectin and Lactobacillus plantarum for Nile tilapia (Oreochromis niloticus) cultured under indoor biofloc systems. Aquaculture 508:98–105. https://doi.org/10.1016/j.aquaculture.2019.03.067
Van Nguyen N, Onoda S, Van Khanh T, Hai PD, Trung NT, Hoang L, Koshio S (2019) Evaluation of dietary heat-killed Lactobacillus plantarum strain L-137 supplementation on growth performance, immunity and stress resistance of Nile tilapia (Oreochromis niloticus). Aquaculture 498:371–379. https://doi.org/10.1016/j.aquaculture.2018.08.081
Wang Y, Wu Y, Wang Y, Xu H, Mei X, Yu D, Wang Y, Li W (2017) Antioxidant properties of probiotic bacteria. Nutrients 9(5):521. https://doi.org/10.3390/nu9050521
Wang J, Yang HL, **a HQ, Ye JD, Lu KL, Hu X, Feng Y, Ruan L, Sun YZ (2018) Supplementation of heat-inactivated Bacillus clausii DE 5 in diets for grouper, Epinephelus coioides, improves feed utilization, intestinal and systemic immune responses and not growth performance. Aquac Nutr 24(2):821–831. https://doi.org/10.1111/anu.12611
Wang J, Feng J, Liu S, Cai Z, Song D, Yang L, Nie G (2021) The probiotic properties of different preparations using Lactococcus lactis Z-2 on intestinal tract, blood and hepatopancreas in Cyprinus carpio. Aquaculture 543:736911. https://doi.org/10.1016/j.aquaculture.2021.736911
Wang J, Zhang D, Wang Y, Liu Z, Liu L, Shi C (2021b) Probiotic effects of the Bacillus velezensis GY65 strain in the mandarin fish Siniperca Chuatsi. Aquac Rep 21:100902
Wang Z, Zheng N, Liang J, Wang Q, Zu X, Wang H, Yuan H, Zhang R, Guo S, Liu Y, Zhou J (2021) Emodin resists to Cyprinid herpesvirus 3 replication via the pathways of Nrf2/Keap1-ARE and NF-κB in the ornamental koi carp (Cyprinus carpio haematopterus). Comp Biochem Physiol Part C: Toxicol Pharmacol 246:109023. https://doi.org/10.1016/j.cbpc.2021.109023
Wu S, Wang G, Angert ER, Wang W, Li W, Zou H (2012) Composition, diversity, and origin of the bacterial community in grass carp intestine. Plos One 7(2):e30440. https://doi.org/10.1371/journal.pone.0030440
Wu X, Teame T, Hao Q, Ding Q, Liu H, Ran C, Yang Y, Zhang Y, Zhou Z, Duan M (2020) Use of a paraprobiotic and postbiotic feed supplement (HWF™) improves the growth performance, composition and function of gut microbiota in hybrid sturgeon (Acipenser baerii x Acipenser schrenckii). Fish Shellfish Immunol 104:36–45. https://doi.org/10.1016/j.fsi.2020.05.054
Xue J, Shen K, Hu Y, Hu Y, Kumar V, Yang G, Wen C (2020) Effects of dietary Bacillus cereus, B. subtilis, Paracoccus marcusii, and Lactobacillus plantarum supplementation on the growth, immune response, antioxidant capacity, and intestinal health of juvenile grass carp (Ctenopharyngodon idellus). Aquac Rep 17:100387. https://doi.org/10.1016/j.aqrep.2020.100387
Yang H-L, Sun Y-Z, Hu X, Ye J-D, Lu K-L, Hu L-H, Zhang J-J (2019) Bacillus pumilus SE5 originated PG and LTA tuned the intestinal TLRs/MyD88 signaling and microbiota in grouper (Epinephelus coioides). Fish Shellfish Immunol 88:266–271. https://doi.org/10.1016/j.fsi.2019.03.005
Yang G, Shen K, Yu R, Wu Q, Yan Q, Chen W, Ding L, Kumar V, Wen C, Peng M (2020) 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. Aquaculture 529:735691. https://doi.org/10.1016/j.aquaculture.2020.735691
Yeganeh S, Adel M, Nosratimovafagh A, Dawood MA (2021) The effect of Lactococcus lactis subsp. Lactis PTCC 1403 on the growth performance, digestive enzymes activity, antioxidative status, immune response, and disease resistance of rainbow trout (Oncorhynchus mykiss). Probiotics Antimicrob Proteins 13(6):1723–1733. https://doi.org/10.1007/s12602-021-09787-3
Yi Y, Zhang Z, Zhao F, Liu H, Yu L, Zha J, Wang G (2018) Probiotic potential of Bacillus velezensis JW: antimicrobial activity against fish pathogenic bacteria and immune enhancement effects on Carassius auratus. Fish Shellfish Immunol 78:322–330. https://doi.org/10.1016/j.fsi.2018.04.055
Zadeh SS, Saad CR, Christianus A, Kamarudin MS, Sijam K, Shamsudin MN, Neela VK (2010) Assessment of growth condition for a candidate probiotic, Shewanella algae, isolated from digestive system of a healthy juvenile Penaeus monodon. Aquacult Int 18(6):1017–1026. https://doi.org/10.1007/s10499-010-9319-6
Zhu C-Z, Li D, Chen W-J, Ban S-N, Liu T, Wen H, Jiang M (2021) Effects of dietary host-associated Lactococcus lactis on growth performance, disease resistance, intestinal morphology and intestinal microbiota of mandarin fish (Siniperca chuatsi). Aquaculture 540:736702. https://doi.org/10.1016/j.aquaculture.2021.736702
Hien, T. T. T., Tu, T. L. C., Carris, S. H., Onoda, S., Tuan, T. N., & Duc, P. M. (2021). Dietary supplementation with heat-killed Lactobacillus plantarum L-137 improves growth, immune response, and disease resistance of snakehead (Channa striata). 14(4).
Acknowledgements
Thanks to Dalian Shengtai Biology Science and Technology Co., Ltd for providing the compound probiotics.
Funding
This work was supported by the Development and Demonstration of Efficient Green Production Mode of Important Seawater Fish in Liaoning (grant numbers 2020JH1/10200002) and the Project for Dalian Youth Star of Science and Technology (grant numbers 2019RQ137).
Author information
Authors and Affiliations
Contributions
Lin Wu wrote the manuscript and collected the data. Yuzhe Han revised the manuscript. Tongjun Ren provided funding acquisition and revised the manuscript. Others provided help for this experiment.
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing interests.
Ethics approval
The experimental processes in this research confirmed to the Guidelines of the Care and Use of Laboratory Animals in China, and the study was approved by the ethics committee of Dalian Ocean University.
Conflict of interest
The authors declare no competing interests.
Additional information
Handling editor: Gavin Burnell
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Wu, L., Wang, L., Cui, S. et al. Effects of dietary compound probiotics and heat-killed compound probiotics on antioxidative capacity, plasma biochemical parameters, intestinal morphology, and microbiota of Cyprinus carpio haematopterus. Aquacult Int 31, 2199–2219 (2023). https://doi.org/10.1007/s10499-023-01080-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10499-023-01080-0