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 inFrontiers in microbiology Vol. 13; p. 1016662
Main Authors Zhang, Zhimin, Xi, Longwei, Liu, Haokun, Jin, Junyan, Yang, Yunxia, Zhu, Xiaoming, Han, Dong, Xie, Shouqi
Format Journal Article
LanguageEnglish
Published Frontiers Media S.A 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
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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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Reviewed by: Xing Ren, Ministry of Natural Resources, China; Aldi Nel, University of Fort Hare, South Africa; Jingjing Tian, Chinese Academy of Fishery Sciences, China
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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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Snippet Microalgae have beneficial effects on the performance of fish as additives and they are becoming a promising alternative to fishmeal as macronutrient...
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SubjectTerms bacterial community
fishmeal replacement
microalgae
microbial function
Microbiology
plant protein source
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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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