High replacement of fishmeal by Chlorella meal affects intestinal microbiota and the potential metabolic function in largemouth bass (Micropterus salmoides)
Microalgae have beneficial effects on the performance of fish as additives and they are becoming a promising alternative to fishmeal as macronutrient ingredients. However, the impact on the fish intestinal microbiome and the function, caused by microalgae as protein sources in diets, remains unclear...
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Published in | Frontiers in microbiology Vol. 13; p. 1016662 |
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Main Authors | , , , , , , , |
Format | Journal Article |
Language | English |
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23.09.2022
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Abstract | Microalgae have beneficial effects on the performance of fish as additives and they are becoming a promising alternative to fishmeal as macronutrient ingredients. However, the impact on the fish intestinal microbiome and the function, caused by microalgae as protein sources in diets, remains unclear. This study aimed to determine the composition and potential function of the intestinal microbial community of largemouth bass (
Micropterus salmoides
) fed diets at five replacement levels (0, 25, 50, 75 and 100%) of fishmeal by
Chlorella
meal in a basal diet (400 g kg
−1
) after 8 weeks. The results showed significant decreases in unique amplicon sequence variants in the intestine at the higher levels of fishmeal replacement. At 50% of fishmeal replacement, dietary inclusions of
Chlorella
meal had no impact on species richness and Shannon diversity and the community structure of the intestinal microbiota. However, high levels of fishmeal replacement (75 and 100%) significantly induced intestinal community disturbance and diversity loss in largemouth bass. Responding to the high fishmeal replacement level, the dominant genus
Cetobacterium
and
Pleslomonas
sharply increased and several taxa from
Lactobacillus
decreased significantly. Functional data predicted by PICRUSt revealed that nutrition-related metabolism was dominant in the intestinal microbiota of fish fed all the five diets, although some potential functions, particularly amino acid and lipid metabolisms, and energy metabolism, were upregulated firstly, and then downregulated in fish fed diets with the increase of dietary
Chlorella
meal. Meanwhile, certain pathways were not enriched in intestinal microbiome until up to 75% of fishmeal replacement, such as carbohydrate metabolism, and cofactors and vitamins metabolism. To conclude, this study reveals that fishmeal replacement (50%) by
Chlorella
meal at the level of 237 g kg
−1
in diets is feasible for largemouth bass without impairing the microbiome structure and the metabolism function, providing an alternative strategy for evaluating the possibility of fishmeal replacement by microalgae in aquafeeds. |
---|---|
AbstractList | Microalgae have beneficial effects on the performance of fish as additives and they are becoming a promising alternative to fishmeal as macronutrient ingredients. However, the impact on the fish intestinal microbiome and the function, caused by microalgae as protein sources in diets, remains unclear. This study aimed to determine the composition and potential function of the intestinal microbial community of largemouth bass (
Micropterus salmoides
) fed diets at five replacement levels (0, 25, 50, 75 and 100%) of fishmeal by
Chlorella
meal in a basal diet (400 g kg
−1
) after 8 weeks. The results showed significant decreases in unique amplicon sequence variants in the intestine at the higher levels of fishmeal replacement. At 50% of fishmeal replacement, dietary inclusions of
Chlorella
meal had no impact on species richness and Shannon diversity and the community structure of the intestinal microbiota. However, high levels of fishmeal replacement (75 and 100%) significantly induced intestinal community disturbance and diversity loss in largemouth bass. Responding to the high fishmeal replacement level, the dominant genus
Cetobacterium
and
Pleslomonas
sharply increased and several taxa from
Lactobacillus
decreased significantly. Functional data predicted by PICRUSt revealed that nutrition-related metabolism was dominant in the intestinal microbiota of fish fed all the five diets, although some potential functions, particularly amino acid and lipid metabolisms, and energy metabolism, were upregulated firstly, and then downregulated in fish fed diets with the increase of dietary
Chlorella
meal. Meanwhile, certain pathways were not enriched in intestinal microbiome until up to 75% of fishmeal replacement, such as carbohydrate metabolism, and cofactors and vitamins metabolism. To conclude, this study reveals that fishmeal replacement (50%) by
Chlorella
meal at the level of 237 g kg
−1
in diets is feasible for largemouth bass without impairing the microbiome structure and the metabolism function, providing an alternative strategy for evaluating the possibility of fishmeal replacement by microalgae in aquafeeds. Microalgae have beneficial effects on the performance of fish as additives and they are becoming a promising alternative to fishmeal as macronutrient ingredients. However, the impact on the fish intestinal microbiome and the function, caused by microalgae as protein sources in diets, remains unclear. This study aimed to determine the composition and potential function of the intestinal microbial community of largemouth bass (Micropterus salmoides) fed diets at five replacement levels (0, 25, 50, 75 and 100%) of fishmeal by Chlorella meal in a basal diet (400 g kg−1) after 8 weeks. The results showed significant decreases in unique amplicon sequence variants in the intestine at the higher levels of fishmeal replacement. At 50% of fishmeal replacement, dietary inclusions of Chlorella meal had no impact on species richness and Shannon diversity and the community structure of the intestinal microbiota. However, high levels of fishmeal replacement (75 and 100%) significantly induced intestinal community disturbance and diversity loss in largemouth bass. Responding to the high fishmeal replacement level, the dominant genus Cetobacterium and Pleslomonas sharply increased and several taxa from Lactobacillus decreased significantly. Functional data predicted by PICRUSt revealed that nutrition-related metabolism was dominant in the intestinal microbiota of fish fed all the five diets, although some potential functions, particularly amino acid and lipid metabolisms, and energy metabolism, were upregulated firstly, and then downregulated in fish fed diets with the increase of dietary Chlorella meal. Meanwhile, certain pathways were not enriched in intestinal microbiome until up to 75% of fishmeal replacement, such as carbohydrate metabolism, and cofactors and vitamins metabolism. To conclude, this study reveals that fishmeal replacement (50%) by Chlorella meal at the level of 237 g kg−1 in diets is feasible for largemouth bass without impairing the microbiome structure and the metabolism function, providing an alternative strategy for evaluating the possibility of fishmeal replacement by microalgae in aquafeeds. |
Author | Zhang, Zhimin Yang, Yunxia Liu, Haokun Zhu, Xiaoming Han, Dong Xie, Shouqi Xi, Longwei Jin, Junyan |
AuthorAffiliation | 1 State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of Sciences , Wuhan , China 3 Hubei Engineering Research Center for Aquatic Animal Nutrition and Feed , Wuhan , China 2 College of Advanced Agricultural Sciences, University of Chinese Academy of Sciences , Beijing , China 4 The Innovative Academy of Seed Design, Chinese Academy of Sciences , Wuhan , China |
AuthorAffiliation_xml | – name: 1 State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of Sciences , Wuhan , China – name: 4 The Innovative Academy of Seed Design, Chinese Academy of Sciences , Wuhan , China – name: 2 College of Advanced Agricultural Sciences, University of Chinese Academy of Sciences , Beijing , China – name: 3 Hubei Engineering Research Center for Aquatic Animal Nutrition and Feed , Wuhan , China |
Author_xml | – sequence: 1 givenname: Zhimin surname: Zhang fullname: Zhang, Zhimin – sequence: 2 givenname: Longwei surname: Xi fullname: Xi, Longwei – sequence: 3 givenname: Haokun surname: Liu fullname: Liu, Haokun – sequence: 4 givenname: Junyan surname: Jin fullname: Jin, Junyan – sequence: 5 givenname: Yunxia surname: Yang fullname: Yang, Yunxia – sequence: 6 givenname: Xiaoming surname: Zhu fullname: Zhu, Xiaoming – sequence: 7 givenname: Dong surname: Han fullname: Han, Dong – sequence: 8 givenname: Shouqi surname: Xie fullname: Xie, Shouqi |
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CitedBy_id | crossref_primary_10_1111_ijfs_16471 crossref_primary_10_3390_cimb46010049 crossref_primary_10_1016_j_aqrep_2023_101645 crossref_primary_10_1155_2024_6337005 crossref_primary_10_3389_fimmu_2023_1110696 crossref_primary_10_1111_raq_12865 crossref_primary_10_7717_peerj_17520 |
Cites_doi | 10.1007/s00726-020-02920-6 10.1016/j.aquaculture.2020.735741 10.1016/S0044-8486(01)00526-9 10.1016/j.aquaculture.2020.736261 10.1016/j.aqrep.2020.100557 10.1046/j.1355-557x.2001.00008.x 10.1007/s10499-019-00341-1 10.3390/biology9060119 10.1016/j.aquaculture.2008.08.015 10.1111/anu.13297 10.1016/j.rvsc.2018.05.013 10.1016/j.aquaculture.2021.737225 10.1016/j.aquaculture.2020.736117 10.1111/anu.12594 10.1038/s42003-021-01820-z 10.1016/j.aquaculture.2020.736185 10.1016/j.fsi.2015.02.024 10.1038/s41587-019-0209-9 10.22358/jafs/66164/2011 10.1111/are.13080 10.1016/j.aquaculture.2019.04.011 10.1016/j.aquaculture.2019.03.075 10.1007/s10068-020-00811-w 10.1016/j.fsi.2018.05.022 10.1093/femsle/fnab071 10.1007/s10811-017-1234-z 10.1128/JB.01175-08 10.1016/j.aquaculture.2021.736943 10.3389/fmicb.2019.02576 10.1111/j.1472-765X.2007.02258.x 10.1038/nature16504 10.3389/fmicb.2017.01531 10.1111/anu.13064 10.1007/s00726-008-0171-1 10.1016/j.aquaculture.2020.735236 10.1111/raq.12416 10.1007/s00394-017-1445-8 10.1111/j.1365-294X.2012.05552.x 10.1016/j.aquaculture.2021.736841 10.1111/are.13797 10.1111/jwas.12320 10.1371/journal.pone.0187696 10.1111/are.14626 10.1093/bioinformatics/btr507 10.3390/su13168726 10.1111/j.1749-7345.2002.tb00021.x 10.1111/jam.15269 10.1016/B978-0-08-100506-4.00008-8 10.1016/j.aquaculture.2016.08.006 10.1111/j.1365-2109.2009.02174.x 10.1038/nmeth.3869 10.1111/anu.12959 10.1016/j.vetmic.2013.05.009 10.1016/j.aquaculture.2021.737369 10.1016/j.aquaculture.2021.737551 10.1016/j.aquaculture.2013.11.011 10.1111/j.1365-2095.2007.00533.x 10.1533/9781845694920.2.300 |
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References | Green (ref15) 2013; 166 Liu (ref27) 2021; 27 (ref49) 2015 Zhou (ref61) 2021; 534 Pakravan (ref34) 2018; 24 Jorge (ref17) 2019; 25 Alagawany (ref2) 2021; 542 Bai (ref5) 2001; 32 Xu (ref54) 2022; 548 Xi (ref52) 2022 Sonnenburg (ref45) 2016; 529 Sampaio-Oliveira (ref42) 2008; 14 Perez-Velazquez (ref35) 2019; 507 Kaushik (ref19) 2010; 41 Kazakov (ref20) 2009; 191 Oliva-Teles (ref33) 2015 Abdel-Latif (ref1) 2022; 547 Tsuchiya (ref48) 2008; 46 Bravo-Tello (ref7) 2017; 12 Sagaram (ref41) 2021; 368 Luo (ref28) 2018; 49 Anderson (ref3) 2016; 464 Ye (ref56) 2019; 506 Rosenau (ref39) 2021; 13 Kononova (ref22) 2019; 27 Sullam (ref46) 2012; 21 Zhao (ref60) 2021; 19 Skrede (ref44) 2011; 20 Xie (ref53) 2021; 543 Francis (ref13) 2001; 199 Rowland (ref40) 2018; 57 Van Vo (ref50) 2020; 529 Shah (ref43) 2018; 30 Tacon (ref47) 2008; 285 Nayak (ref32) 2020; 9 Cao (ref9) 2018; 79 Li (ref26); 53 (ref12) 2021 Zhang (ref58) 2017; 8 Gatesoupe (ref14) 2014 Li (ref25) 2009; 37 Zhang (ref59) 2019; 10 Li (ref24); 533 Lyons (ref29) 2017; 48 Rackerby (ref36) 2020; 29 Callahan (ref8) 2016; 13 Larios-Soriano (ref23) 2022; 132 Wang (ref51) 2020; 524 Rahimnejad (ref37) 2017; 48 Yamamoto (ref55) 2021; 545 Yukgehnaish (ref57) 2020; 12 Bolyen (ref6) 2019; 37 Raji (ref38) 2018; 119 Arteaga Quico (ref4) 2021; 533 Ding (ref11) 2015; 44 Kim (ref21) 2002; 33 Mims (ref31) 2021; 4 Chen (ref10) 2020; 51 Magoc (ref30) 2021; 27 He (ref16) 2020; 26 Kaushik (ref18) 2008 |
References_xml | – volume: 53 start-page: 33 ident: ref26 article-title: Use of alternative protein sources for fishmeal replacement in the diet of largemouth bass (Micropterus salmoides). Part I: effects of poultry by-product meal and soybean meal on growth, feed utilization, and health publication-title: Amino Acids doi: 10.1007/s00726-020-02920-6 contributor: fullname: Li – volume: 529 start-page: 735741 year: 2020 ident: ref50 article-title: Progressive replacement of fishmeal by raw and enzyme-treated alga, Spirulina platensis influences growth, intestinal micromorphology and stress response in juvenile barramundi, Lates calcarifer publication-title: Aquaculture doi: 10.1016/j.aquaculture.2020.735741 contributor: fullname: Van Vo – volume: 199 start-page: 197 year: 2001 ident: ref13 article-title: Antinutritional factors present in plant-derived alternate fish feed ingredients and their effects in fish publication-title: Aquaculture doi: 10.1016/S0044-8486(01)00526-9 contributor: fullname: Francis – volume: 534 start-page: 736261 year: 2021 ident: ref61 article-title: High dietary starch impairs intestinal health and microbiota of largemouth bass, Micropterus salmoides publication-title: Aquaculture doi: 10.1016/j.aquaculture.2020.736261 contributor: fullname: Zhou – volume: 19 start-page: 100557 year: 2021 ident: ref60 article-title: Growth performance, intestinal histomorphology, body composition, hematological and antioxidant parameters of Oncorhynchus mykiss were not detrimentally affected by replacement of fish meal with concentrated dephenolization cottonseed protein publication-title: Aquacult. Rep. doi: 10.1016/j.aqrep.2020.100557 contributor: fullname: Zhao – volume: 32 start-page: 92 year: 2001 ident: ref5 article-title: Effects of Chlorella powder as a feed additive on growth performance in juvenile Korean rockfish, Sebastes schlegeli (Hilgendorf) publication-title: Aquac. Res. doi: 10.1046/j.1355-557x.2001.00008.x contributor: fullname: Bai – volume: 27 start-page: 475 year: 2019 ident: ref22 article-title: Intestinal microbiota of salmonids and its changes upon introduction of soy proteins to fish feed publication-title: Aquacult. Int. doi: 10.1007/s10499-019-00341-1 contributor: fullname: Kononova – volume: 9 start-page: 119 year: 2020 ident: ref32 article-title: Dietary supplementation with omega-6 LC-PUFA-rich microalgae regulates mucosal immune response and promotes microbial diversity in the zebrafish gut publication-title: Biology (Basel). doi: 10.3390/biology9060119 contributor: fullname: Nayak – volume: 285 start-page: 146 year: 2008 ident: ref47 article-title: Global overview on the use of fish meal and fish oil in industrially compounded aquafeeds: trends and future prospects publication-title: Aquaculture doi: 10.1016/j.aquaculture.2008.08.015 contributor: fullname: Tacon – volume: 27 start-page: 1569 year: 2021 ident: ref27 article-title: Substitution of fish meal with enzyme-treated soybean in diets for juvenile largemouth bass (Micropterus salmoides) publication-title: Aquac. Nutr. doi: 10.1111/anu.13297 contributor: fullname: Liu – volume: 119 start-page: 67 year: 2018 ident: ref38 article-title: Fishmeal replacement with spirulina platensis and Chlorella vulgaris in African catfish (Clarias gariepinus) diet: effect on antioxidant enzyme activities and haematological parameters publication-title: Res. Vet. Sci. doi: 10.1016/j.rvsc.2018.05.013 contributor: fullname: Raji – volume: 545 start-page: 737225 year: 2021 ident: ref55 article-title: Effects of butyrate, propionate, and their combination in vitro, and the impacts of their supplementation in high-plant-protein diets to the production performance, innate immune responses, and intestinal microbiota of red drum (Sciaenops ocellatus) publication-title: Aquaculture doi: 10.1016/j.aquaculture.2021.737225 contributor: fullname: Yamamoto – volume: 533 start-page: 736117 year: 2021 ident: ref4 article-title: Dietary supplementation with Chlorella peruviana improve the growth and innate immune response of rainbow trout Oncorhynchus mykiss fingerlings publication-title: Aquaculture doi: 10.1016/j.aquaculture.2020.736117 contributor: fullname: Arteaga Quico – volume: 24 start-page: 594 year: 2018 ident: ref34 article-title: Chlorella vulgaris meal improved growth performance, digestive enzyme activities, fatty acid composition and tolerance of hypoxia and ammonia stress in juvenile Pacific white shrimp Litopenaeus vannamei publication-title: Aquac. Nutr. doi: 10.1111/anu.12594 contributor: fullname: Pakravan – volume: 4 start-page: 281 year: 2021 ident: ref31 article-title: The gut mycobiome of healthy mice is shaped by the environment and correlates with metabolic outcomes in response to diet publication-title: Commun. Biol. doi: 10.1038/s42003-021-01820-z contributor: fullname: Mims – volume: 533 start-page: 736185 ident: ref24 article-title: Effects of fishmeal replacement with composite mixture of shrimp hydrolysate and plant proteins on growth performance, feed utilization, and target of rapamycin pathway in largemouth bass, Micropterus salmoides publication-title: Aquaculture doi: 10.1016/j.aquaculture.2020.736185 contributor: fullname: Li – volume: 44 start-page: 295 year: 2015 ident: ref11 article-title: An evaluation of replacing fish meal with fermented soybean meal in the diet of Macrobrachium nipponense: growth, nonspecific immunity, and resistance to Aeromonas hydrophila publication-title: Fish Shellfish. Immun. doi: 10.1016/j.fsi.2015.02.024 contributor: fullname: Ding – volume: 37 start-page: 852 year: 2019 ident: ref6 article-title: Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2 publication-title: Nat. Biotechnol. doi: 10.1038/s41587-019-0209-9 contributor: fullname: Bolyen – volume: 20 start-page: 131 year: 2011 ident: ref44 article-title: Evaluation of microalgae as sources of digestible nutrients for monogastric animals publication-title: J. Anim. Feed Sci. doi: 10.22358/jafs/66164/2011 contributor: fullname: Skrede – volume-title: China Fisheries Statistical Yearbook 2021 year: 2021 ident: ref12 – volume: 48 start-page: 2438 year: 2017 ident: ref29 article-title: Effects of low-level dietary microalgae supplementation on the distal intestinal microbiome of farmed rainbow trout Oncorhynchus mykiss (Walbaum) publication-title: Aquac. Res. doi: 10.1111/are.13080 contributor: fullname: Lyons – volume: 507 start-page: 83 year: 2019 ident: ref35 article-title: Effect of fishmeal and fish oil replacement by algal meals on biological performance and fatty acid profile of hybrid striped bass (Morone crhysops ♀ × M. saxatilis ♂) publication-title: Aquaculture doi: 10.1016/j.aquaculture.2019.04.011 contributor: fullname: Perez-Velazquez – volume: 506 start-page: 437 year: 2019 ident: ref56 article-title: Effects of dietary plant protein sources influencing hepatic lipid metabolism and hepatocyte apoptosis in hybrid grouper (Epinephelus lanceolatu♂ × Epinephelus fuscoguttatus♀) publication-title: Aquaculture doi: 10.1016/j.aquaculture.2019.03.075 contributor: fullname: Ye – volume: 29 start-page: 1463 year: 2020 ident: ref36 article-title: Understanding the effects of dietary components on the gut microbiome and human health publication-title: Food Sci. Biotechnol. doi: 10.1007/s10068-020-00811-w contributor: fullname: Rackerby – volume: 79 start-page: 265 year: 2018 ident: ref9 article-title: Replacement of fishmeal by spirulina Arthrospira platensis affects growth, immune related-gene expression in gibel carp (Carassius auratus gibelio var. CAS III), and its challenge against Aeromonas hydrophila infection publication-title: Fish. Shellfish. Immun. doi: 10.1016/j.fsi.2018.05.022 contributor: fullname: Cao – start-page: 26 volume-title: Effects of fish meal replacement with Chlorella meal on growth performance, pigmentation, and liver health of largemouth bass ( year: 2022 ident: ref52 contributor: fullname: Xi – volume: 368 start-page: fnab071 year: 2021 ident: ref41 article-title: Microalgae as feed ingredients: recent developments on their role in immunomodulation and gut microbiota of aquaculture species publication-title: FEMS Microbiol. Lett. doi: 10.1093/femsle/fnab071 contributor: fullname: Sagaram – volume: 30 start-page: 197 year: 2018 ident: ref43 article-title: Microalgae in aquafeeds for a sustainable aquaculture industry publication-title: J. Appl. Phycol. doi: 10.1007/s10811-017-1234-z contributor: fullname: Shah – volume: 191 start-page: 52 year: 2009 ident: ref20 article-title: Comparative genomics of regulation of fatty acid and branched-chain amino acid utilization in Proteobacteria publication-title: J. Bacteriol. doi: 10.1128/JB.01175-08 contributor: fullname: Kazakov – volume: 543 start-page: 736943 year: 2021 ident: ref53 article-title: Effects of Cetobacterium somerae fermentation product on gut and liver health of common carp (Cyprinus carpio) fed diet supplemented with ultra-micro ground mixed plant proteins publication-title: Aquaculture doi: 10.1016/j.aquaculture.2021.736943 contributor: fullname: Xie – volume: 10 start-page: 2576 year: 2019 ident: ref59 article-title: Microbiome of co-cultured fish exhibits host selection and niche differentiation at the organ scale publication-title: Front. Microbiol. doi: 10.3389/fmicb.2019.02576 contributor: fullname: Zhang – volume: 46 start-page: 43 year: 2008 ident: ref48 article-title: Novel ecological niche of Cetobacterium somerae, an anaerobic bacterium in the intestinal tracts of freshwater fish publication-title: Lett. Appl. Microbiol. doi: 10.1111/j.1472-765X.2007.02258.x contributor: fullname: Tsuchiya – volume: 529 start-page: 212 year: 2016 ident: ref45 article-title: Diet-induced extinctions in the gut microbiota compound over generations publication-title: Nature doi: 10.1038/nature16504 contributor: fullname: Sonnenburg – volume: 8 start-page: 1531 year: 2017 ident: ref58 article-title: High spatial and temporal variations of microbial community along the southern catfish gastrointestinal tract: insights into dynamic food digestion publication-title: Front. Microbiol. doi: 10.3389/fmicb.2017.01531 contributor: fullname: Zhang – volume: 26 start-page: 1058 year: 2020 ident: ref16 article-title: Effects of fish meal replaced by fermented soybean meal on growth performance, intestinal histology and microbiota of largemouth bass (Micropterus salmoides) publication-title: Aquac. Nutr. doi: 10.1111/anu.13064 contributor: fullname: He – volume: 37 start-page: 43 year: 2009 ident: ref25 article-title: New developments in fish amino acid nutrition: towards functional and environmentally oriented aquafeeds publication-title: Amino Acids doi: 10.1007/s00726-008-0171-1 contributor: fullname: Li – volume: 524 start-page: 735236 year: 2020 ident: ref51 article-title: Total replacement of fish meal with soybean meal in diets for bullfrog (Lithobates catesbeianus): effects on growth performance and gut microbial composition publication-title: Aquaculture doi: 10.1016/j.aquaculture.2020.735236 contributor: fullname: Wang – volume: 12 start-page: 1903 year: 2020 ident: ref57 article-title: Gut microbiota metagenomics in aquaculture: factors influencing gut microbiome and its physiological role in fish publication-title: Rev. Aquacult. doi: 10.1111/raq.12416 contributor: fullname: Yukgehnaish – volume: 57 start-page: 1 year: 2018 ident: ref40 article-title: Gut microbiota functions: metabolism of nutrients and other food components publication-title: Eur. J. Nutr. doi: 10.1007/s00394-017-1445-8 contributor: fullname: Rowland – volume: 21 start-page: 3363 year: 2012 ident: ref46 article-title: Environmental and ecological factors that shape the gut bacterial communities of fish: a meta-analysis publication-title: Mol. Ecol. doi: 10.1111/j.1365-294X.2012.05552.x contributor: fullname: Sullam – volume: 542 start-page: 736841 year: 2021 ident: ref2 article-title: Nutritional applications of species of Spirulina and Chlorella in farmed fish: A review publication-title: Aquaculture doi: 10.1016/j.aquaculture.2021.736841 contributor: fullname: Alagawany – volume: 49 start-page: 3329 year: 2018 ident: ref28 article-title: Chlorella additive increased growth performance, improved appetite and immune response of juvenile crucian carp Carassius auratus publication-title: Aquac. Res. doi: 10.1111/are.13797 contributor: fullname: Luo – volume: 48 start-page: 103 year: 2017 ident: ref37 article-title: Effects of dietary inclusion of Chlorella vulgaris on growth, blood biochemical parameters, and antioxidant enzyme activity in olive flounder, Paralichthys olivaceus publication-title: J. World Aquacult. Soc. doi: 10.1111/jwas.12320 contributor: fullname: Rahimnejad – volume: 12 start-page: e0187696 year: 2017 ident: ref7 article-title: Effect of microalgae on intestinal inflammation triggered by soybean meal and bacterial infection in zebrafish publication-title: PLoS One doi: 10.1371/journal.pone.0187696 contributor: fullname: Bravo-Tello – volume: 51 start-page: 2870 year: 2020 ident: ref10 article-title: Effects of fishmeal replacement with cottonseed protein concentrate on growth, digestive proteinase, intestinal morphology and microflora in pearl gentian grouper (♀Epinephelus fuscoguttatus × ♂Epinephelus lanceolatu) publication-title: Aquac. Res. doi: 10.1111/are.14626 contributor: fullname: Chen – volume: 27 start-page: 2957 year: 2021 ident: ref30 article-title: FLASH: fast length adjustment of short reads to improve genome assemblies publication-title: Bioinformatics doi: 10.1093/bioinformatics/btr507 contributor: fullname: Magoc – volume-title: Transforming Our World: The 2030 Agenda for Sustainable Development year: 2015 ident: ref49 – volume: 13 start-page: 8726 year: 2021 ident: ref39 article-title: Total replacement of fishmeal by spirulina (Arthrospira platensis) and its effect on growth performance and product quality of African catfish (Clarias gariepinus) publication-title: Sustainability. doi: 10.3390/su13168726 contributor: fullname: Rosenau – volume: 33 start-page: 425 year: 2002 ident: ref21 article-title: Effects of dietary Chlorella ellipsoidea supplementation on growth, blood characteristics, and whole-body composition in juvenile Japanese flounder Paralichthys olivaceus publication-title: J. World Aquacult. Soc. doi: 10.1111/j.1749-7345.2002.tb00021.x contributor: fullname: Kim – volume: 132 start-page: 1384 year: 2022 ident: ref23 article-title: Soy protein concentrate effects on gut microbiota structure and digestive physiology of Totoaba macdonaldi publication-title: J. Appl. Microbiol. doi: 10.1111/jam.15269 contributor: fullname: Larios-Soriano – start-page: 203 volume-title: Feed and Feeding Practice in Aquaculture year: 2015 ident: ref33 article-title: Replacing fishmeal and fish oil in industrial aquafeeds for carnivorous fish doi: 10.1016/B978-0-08-100506-4.00008-8 contributor: fullname: Oliva-Teles – volume: 464 start-page: 618 year: 2016 ident: ref3 article-title: Full replacement of menhaden fish meal protein by low-gossypol cottonseed flour protein in the diet of juvenile black sea bass Centropristis striata publication-title: Aquaculture doi: 10.1016/j.aquaculture.2016.08.006 contributor: fullname: Anderson – volume: 41 start-page: 322 year: 2010 ident: ref19 article-title: Protein and amino acid nutrition and metabolism in fish: current knowledge and future needs publication-title: Aquac. Res. doi: 10.1111/j.1365-2109.2009.02174.x contributor: fullname: Kaushik – volume: 13 start-page: 581 year: 2016 ident: ref8 article-title: DADA2: high-resolution sample inference from illumina amplicon data publication-title: Nat. Methods doi: 10.1038/nmeth.3869 contributor: fullname: Callahan – volume: 25 start-page: 1388 year: 2019 ident: ref17 article-title: Short-term supplementation of gilthead seabream (Sparus aurata) diets with Nannochloropsis gaditana modulates intestinal microbiota without affecting intestinal morphology and function publication-title: Aquac. Nutr. doi: 10.1111/anu.12959 contributor: fullname: Jorge – volume: 166 start-page: 286 year: 2013 ident: ref15 article-title: Dietary soybean protein concentrate-induced intestinal disorder in marine farmed Atlantic salmon, Salmo salar is associated with alterations in gut microbiota publication-title: Vet. Microbiol. doi: 10.1016/j.vetmic.2013.05.009 contributor: fullname: Green – volume: 547 start-page: 737369 year: 2022 ident: ref1 article-title: Benefits and applications of Moringa oleifera as a plant protein source in aquafeed: A review publication-title: Aquaculture doi: 10.1016/j.aquaculture.2021.737369 contributor: fullname: Abdel-Latif – volume: 548 start-page: 737551 year: 2022 ident: ref54 article-title: Effects of replacing fishmeal with cottonseed protein concentrate on growth performance, flesh quality and gossypol deposition of largemouth bass (Micropterus salmoides) publication-title: Aquaculture doi: 10.1016/j.aquaculture.2021.737551 contributor: fullname: Xu – start-page: 47 year: 2014 ident: ref14 article-title: The effects of dietary carbohydrate sources and forms on metabolic response and intestinal microbiota in sea bass juveniles, Dicentrarchus labrax publication-title: Aquaculture doi: 10.1016/j.aquaculture.2013.11.011 contributor: fullname: Gatesoupe – volume: 14 start-page: 318 year: 2008 ident: ref42 article-title: Digestibility of plant protein-based diets by largemouth bass Micropterus salmoides publication-title: Aquac. Nutr. doi: 10.1111/j.1365-2095.2007.00533.x contributor: fullname: Sampaio-Oliveira – start-page: 300 volume-title: Improving Farmed Fish Quality and Safety year: 2008 ident: ref18 article-title: Plant proteins as alternative sources for fish feed and farmed fish quality doi: 10.1533/9781845694920.2.300 contributor: fullname: Kaushik |
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Title | High replacement of fishmeal by Chlorella meal affects intestinal microbiota and the potential metabolic function in largemouth bass (Micropterus salmoides) |
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