Transcriptome analysis and immune gene expression of channel catfish (Ictalurus punctatus) fed diets with inclusion of frass from black soldier fly larvae

The larval waste, exoskeleton shedding, and leftover feed components of the black soldier fly and its larvae make up the by-product known as frass. In this study, we subjected channel catfish (Ictalurus punctatus) to a 10-week feeding trial to assess how different dietary amounts of frass inclusion...

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Main Authors: Nithin Muliya Sankappa, Miles D. Lange, Mediha Yildirim-Aksoy, Rashida Eljack, Huseyin Kucuktas, Benjamin H. Beck, Jason W. Abernathy
Format: Article
Language:English
Published: Frontiers Media S.A. 2024-01-01
Series:Frontiers in Physiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fphys.2023.1330368/full
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author Nithin Muliya Sankappa
Nithin Muliya Sankappa
Miles D. Lange
Mediha Yildirim-Aksoy
Rashida Eljack
Huseyin Kucuktas
Benjamin H. Beck
Jason W. Abernathy
author_facet Nithin Muliya Sankappa
Nithin Muliya Sankappa
Miles D. Lange
Mediha Yildirim-Aksoy
Rashida Eljack
Huseyin Kucuktas
Benjamin H. Beck
Jason W. Abernathy
author_sort Nithin Muliya Sankappa
collection DOAJ
description The larval waste, exoskeleton shedding, and leftover feed components of the black soldier fly and its larvae make up the by-product known as frass. In this study, we subjected channel catfish (Ictalurus punctatus) to a 10-week feeding trial to assess how different dietary amounts of frass inclusion would affect both systemic and mucosal tissue gene expression, especially in regard to growth and immune-related genes. Fish were divided in quadruplicate aquaria, and five experimental diets comprising 0, 50, 100, 200, and 300 g of frass per kilogram of feed were fed twice daily. At the end of the trial, liver, head kidney, gill, and intestine samples were collected for gene expression analyses. First, liver and intestine samples from fish fed with a no frass inclusion diet (control), low-frass (50 g/kg) inclusion diet, or a high-frass (300 g/kg) inclusion diet were subjected to Illumina RNA sequencing to determine global differential gene expression among diet groups. Differentially expressed genes (DEGs) included the upregulation of growth-related genes such as glucose-6-phosphatase and myostatin, as well as innate immune receptors and effector molecules such as toll-like receptor 5, apolipoprotein A1, C-type lectin, and lysozyme. Based on the initial screenings of low/high frass using RNA sequencing, a more thorough evaluation of immune gene expression of all tissues sampled, and all levels of frass inclusion, was further conducted. Using targeted quantitative PCR panels for both innate and adaptive immune genes from channel catfish, differential expression of genes was identified, which included innate receptors (TLR1, TLR5, TLR9, and TLR20A), proinflammatory cytokines (IL-1β type a, IL-1β type b, IL-17, IFN-γ, and TNFα), chemokines (CFC3 and CFD), and hepcidin in both systemic (liver and head kidney) and mucosal (gill and intestine) tissues. Overall, frass from black soldier fly larvae inclusion in formulated diets was found to alter global gene expression and activate innate and adaptive immunity in channel catfish, which has the potential to support disease resistance in this species in addition to demonstrated growth benefits.
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spelling doaj.art-9ef3655c504e47b1936258273c2c31882024-01-09T04:40:46ZengFrontiers Media S.A.Frontiers in Physiology1664-042X2024-01-011410.3389/fphys.2023.13303681330368Transcriptome analysis and immune gene expression of channel catfish (Ictalurus punctatus) fed diets with inclusion of frass from black soldier fly larvaeNithin Muliya Sankappa0Nithin Muliya Sankappa1Miles D. Lange2Mediha Yildirim-Aksoy3Rashida Eljack4Huseyin Kucuktas5Benjamin H. Beck6Jason W. Abernathy7Oak Ridge Institute for Science and Education (ORISE), ARS Research Participation Program, Oak Ridge, TN, United StatesUnited States Department of Agriculture, Agricultural Research Service, Aquatic Animal Health Research Unit (AAHRU), Auburn, AL, United StatesUnited States Department of Agriculture, Agricultural Research Service, Aquatic Animal Health Research Unit (AAHRU), Auburn, AL, United StatesUnited States Department of Agriculture, Agricultural Research Service, Aquatic Animal Health Research Unit (AAHRU), Auburn, AL, United StatesUnited States Department of Agriculture, Agricultural Research Service, Aquatic Animal Health Research Unit (AAHRU), Auburn, AL, United StatesU.S. Fish and Wildlife Service, Southwestern Native Aquatic Resources and Recovery Center, Aquatic Animal Health Unit, Dexter, NM, United StatesUnited States Department of Agriculture, Agricultural Research Service, Aquatic Animal Health Research Unit (AAHRU), Auburn, AL, United StatesUnited States Department of Agriculture, Agricultural Research Service, Aquatic Animal Health Research Unit (AAHRU), Auburn, AL, United StatesThe larval waste, exoskeleton shedding, and leftover feed components of the black soldier fly and its larvae make up the by-product known as frass. In this study, we subjected channel catfish (Ictalurus punctatus) to a 10-week feeding trial to assess how different dietary amounts of frass inclusion would affect both systemic and mucosal tissue gene expression, especially in regard to growth and immune-related genes. Fish were divided in quadruplicate aquaria, and five experimental diets comprising 0, 50, 100, 200, and 300 g of frass per kilogram of feed were fed twice daily. At the end of the trial, liver, head kidney, gill, and intestine samples were collected for gene expression analyses. First, liver and intestine samples from fish fed with a no frass inclusion diet (control), low-frass (50 g/kg) inclusion diet, or a high-frass (300 g/kg) inclusion diet were subjected to Illumina RNA sequencing to determine global differential gene expression among diet groups. Differentially expressed genes (DEGs) included the upregulation of growth-related genes such as glucose-6-phosphatase and myostatin, as well as innate immune receptors and effector molecules such as toll-like receptor 5, apolipoprotein A1, C-type lectin, and lysozyme. Based on the initial screenings of low/high frass using RNA sequencing, a more thorough evaluation of immune gene expression of all tissues sampled, and all levels of frass inclusion, was further conducted. Using targeted quantitative PCR panels for both innate and adaptive immune genes from channel catfish, differential expression of genes was identified, which included innate receptors (TLR1, TLR5, TLR9, and TLR20A), proinflammatory cytokines (IL-1β type a, IL-1β type b, IL-17, IFN-γ, and TNFα), chemokines (CFC3 and CFD), and hepcidin in both systemic (liver and head kidney) and mucosal (gill and intestine) tissues. Overall, frass from black soldier fly larvae inclusion in formulated diets was found to alter global gene expression and activate innate and adaptive immunity in channel catfish, which has the potential to support disease resistance in this species in addition to demonstrated growth benefits.https://www.frontiersin.org/articles/10.3389/fphys.2023.1330368/fullchannel catfishfrassalternative dietsfeed additivesRNA-seqinnate immunity
spellingShingle Nithin Muliya Sankappa
Nithin Muliya Sankappa
Miles D. Lange
Mediha Yildirim-Aksoy
Rashida Eljack
Huseyin Kucuktas
Benjamin H. Beck
Jason W. Abernathy
Transcriptome analysis and immune gene expression of channel catfish (Ictalurus punctatus) fed diets with inclusion of frass from black soldier fly larvae
Frontiers in Physiology
channel catfish
frass
alternative diets
feed additives
RNA-seq
innate immunity
title Transcriptome analysis and immune gene expression of channel catfish (Ictalurus punctatus) fed diets with inclusion of frass from black soldier fly larvae
title_full Transcriptome analysis and immune gene expression of channel catfish (Ictalurus punctatus) fed diets with inclusion of frass from black soldier fly larvae
title_fullStr Transcriptome analysis and immune gene expression of channel catfish (Ictalurus punctatus) fed diets with inclusion of frass from black soldier fly larvae
title_full_unstemmed Transcriptome analysis and immune gene expression of channel catfish (Ictalurus punctatus) fed diets with inclusion of frass from black soldier fly larvae
title_short Transcriptome analysis and immune gene expression of channel catfish (Ictalurus punctatus) fed diets with inclusion of frass from black soldier fly larvae
title_sort transcriptome analysis and immune gene expression of channel catfish ictalurus punctatus fed diets with inclusion of frass from black soldier fly larvae
topic channel catfish
frass
alternative diets
feed additives
RNA-seq
innate immunity
url https://www.frontiersin.org/articles/10.3389/fphys.2023.1330368/full
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