A systematic meta-analysis reveals enrichment of Actinobacteria and Firmicutes in the fish gut in response to black soldier fly (Hermetica illucens) meal-based diets

Abdel-Aziz, 2013, Identifying some pathogenic Vibrio/Photobacterium species during mass mortalities of cultured gilthead seabream (Sparus aurata) and European seabass (Dicentrarchus labrax) from some Egyptian coastal provinces, Intl. J. Vet. Sci. Med., 1, 87, 10.1016/j.ijvsm.2013.10.004 Albanese, 2015, MICCA: a complete and accurate software for taxonomic profiling of metagenomic data, Sci. Rep., 5, 1, 10.1038/srep09743 Andersen, 2018, ampvis2: an R package to analyse and visualise 16S rRNA amplicon data, BioRxiv Andreo-Martínez, 2021, A meta-analysis of gut microbiota in children with autism, J. Autism Dev. Disord., 1 Andrews Bano, 2007, Dominance of Mycoplasma in the guts of the long-jawed Mudsucker, Gillichthys mirabilis, from five California salt marshes, Environ. Microbiol., 9, 2636, 10.1111/j.1462-2920.2007.01381.x Barroso, 2014, The potential of various insect species for use as food for fish, Aquaculture., 422, 193, 10.1016/j.aquaculture.2013.12.024 Bisanz, 2019, Meta-analysis reveals reproducible gut microbiome alterations in response to a high-fat diet, Cell Host Microbe, 26 Brown, 2019, Analysis of the gut and gill microbiome of resistant and susceptible lines of rainbow trout (Oncorhynchus mykiss), Fish Shellfish Immunol., 86, 497, 10.1016/j.fsi.2018.11.079 Bruni, 2020, Total replacement of dietary fish meal with black soldier fly (Hermetia illucens) larvae does not impair physical, chemical or volatile composition of farmed Atlantic salmon (Salmo salar L.), J. Sci. Food Agric., 100, 1038, 10.1002/jsfa.10108 Bruno, 2019, The intestinal microbiota of Hermetia illucens larvae is affected by diet and shows a diverse composition in the different midgut regions, Appl. Environ. Microbiol., 85, 10.1128/AEM.01864-18 Bullock, 1975, Fluorescent antibody identification and detection of the Corynebacterium causing kidney disease of salmonids, J. Fish. Board Canada., 32, 2224, 10.1139/f75-263 Butt, 2019, Gut microbiota and energy homeostasis in fish, Front. Endocrinol. (Lausanne), 10, 9, 10.3389/fendo.2019.00009 Caimi, 2021, Dietary inclusion of a partially defatted black soldier fly (Hermetia illucens) larva meal in low fishmeal-based diets for rainbow trout (Oncorhynchus mykiss), J. Anim. Sci. Biotechnol., 12, 1, 10.1186/s40104-021-00575-1 Calle, 2011, AUC-RF: a new strategy for genomic profiling with random forest, Hum. Hered., 72, 121, 10.1159/000330778 Chaklader, 2019, Insect larvae, Hermetia illucens in poultry by-product meal for barramundi, Lates calcarifer modulates histomorphology, immunity and resistance to Vibrio harveyi, Sci. Rep., 9, 1, 10.1038/s41598-019-53018-3 Chaklader, 2021, Supplementation of tuna hydrolysate and insect larvae improves fishmeal replacement efficacy of poultry by-product in Lates calcarifer (Bloch, 1790) juveniles, Sci. Rep., 11, 1, 10.1038/s41598-021-84660-5 Champely, 2017 Cheaib, 2020, Unpicking the mysterious symbiosis of Mycoplasma in salmonids, bioRxiv Ciric, 2018, Characterisation of gut microbiota of farmed Chinook salmon using metabarcoding, bioRxiv Cohen, 2013 Cummins, 2017, Evaluation of black soldier fly (Hermetia illucens) larvae meal as partial or total replacement of marine fish meal in practical diets for Pacific white shrimp (Litopenaeus vannamei), Aquaculture., 473, 337, 10.1016/j.aquaculture.2017.02.022 DeLong, 1988, Comparing the areas under two or more correlated receiver operating characteristic curves: a nonparametric approach, Biometrics, 837, 10.2307/2531595 Dixon, 2003, VEGAN, a package of R functions for community ecology, J. Veg. Sci., 14, 927, 10.1111/j.1654-1103.2003.tb02228.x Egerton, 2018, The gut microbiota of marine fish, Front. Microbiol., 9, 873, 10.3389/fmicb.2018.00873 Ewels, 2016, MultiQC: summarize analysis results for multiple tools and samples in a single report, Bioinformatics., 32, 3047, 10.1093/bioinformatics/btw354 Fouz, 2000, Evidence that water transmits the disease caused by the fish pathogen Photobacterium damselae subsp. damselae, J. Appl. Microbiol., 88, 531, 10.1046/j.1365-2672.2000.00992.x Foysal, 2019, Dietary supplementation of black soldier fly (Hermetica illucens) meal modulates gut microbiota, innate immune response and health status of marron (Cherax cainii, Austin 2002) fed poultry-by-product and fishmeal based diets, PeerJ., 7 Foysal, 2020, Meta-omics technologies reveals beneficiary effects of Lactobacillus plantarum as dietary supplements on gut microbiota, immune response and disease resistance of Nile tilapia (Oreochromis niloticus), Aquaculture., 520, 10.1016/j.aquaculture.2020.734974 Gaudioso, 2021, Processed animal proteins from insect and poultry by-products in a fish meal-free diet for rainbow trout: impact on intestinal microbiota and inflammatory markers, Int. J. Mol. Sci., 22, 5454, 10.3390/ijms22115454 Gupta, 2020, Therapies to modulate gut microbiota: past, present and future, World J. Gastroenterol., 26, 777, 10.3748/wjg.v26.i8.777 Hamza, 2016, Virgibacillus proomii and Bacillus mojavensis as probiotics in sea bass (Dicentrarchus labrax) larvae: effects on growth performance and digestive enzyme activities, Fish Physiol. Biochem., 42, 495, 10.1007/s10695-015-0154-6 Han, 2018, A revisit to fishmeal usage and associated consequences in Chinese aquaculture, Rev. Aquac., 10, 493, 10.1111/raq.12183 Harrer, 2019, 9000 Hoffman, 2015, Omics-driven startups challenge healthcare model, Nat. Biotechnol., 33, 887, 10.1038/nbt0915-887 Hua, 2019, The future of aquatic protein: implications for protein sources in aquaculture diets, One Earth., 1, 316, 10.1016/j.oneear.2019.10.018 Huyben, 2019, High-throughput sequencing of gut microbiota in rainbow trout (Oncorhynchus mykiss) fed larval and pre-pupae stages of black soldier fly (Hermetia illucens), Aquaculture., 500, 485, 10.1016/j.aquaculture.2018.10.034 Joshi, 2011 Kenny, 2020, Cholesterol metabolism by uncultured human gut bacteria influences host cholesterol level, Cell Host Microbe, 28 Kim, 2007, Detection of major bacterial and viral pathogens in trash fish used to feed cultured flounder in Korea, Aquaculture., 272, 105, 10.1016/j.aquaculture.2007.09.008 Klammsteiner, 2020, The core gut microbiome of black soldier fly (Hermetia illucens) larvae raised on low-bioburden diets, Front. Microbiol., 11, 993, 10.3389/fmicb.2020.00993 Kossmeier, 2019, 1 Leinonen, 2010, The sequence read archive, Nucleic Acids Res., 39, D19, 10.1093/nar/gkq1019 Li, 2020, Total replacement of fish meal with black soldier fly (Hermetia illucens) larvae meal does not compromise the gut health of Atlantic salmon (Salmo salar), Aquaculture., 520, 10.1016/j.aquaculture.2020.734967 Li, 2021, Differential response of digesta-and mucosa-associated intestinal microbiota to dietary insect meal during the seawater phase of Atlantic salmon, Anim. Microbiome., 3, 1, 10.1186/s42523-020-00071-3 Lyons, 2017, Phylogenetic and functional characterization of the distal intestinal microbiome of rainbow trout Oncorhynchus mykiss from both farm and aquarium settings, J. Appl. Microbiol., 122, 347, 10.1111/jam.13347 Madibana, 2020, Black soldier fly larvae meal as a fishmeal substitute in juvenile dusky kob diets: effect on feed utilization, growth performance, and blood parameters, Sustainability., 12, 9460, 10.3390/su12229460 Majeed, 2019, Evaluation of the in vitro cholesterol-lowering activity of the probiotic strain Bacillus coagulans MTCC 5856, Int. J. Food Sci. Technol., 54, 212, 10.1111/ijfs.13926 McMurdie, 2013, Phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data, PLoS One, 8, 10.1371/journal.pone.0061217 Müller, 2017, The black soldier fly, Hermetia illucens–a promising source for sustainable production of proteins, lipids and bioactive substances, Z. Naturforsch. C, 72, 351, 10.1515/znc-2017-0030 Nataraja, 2014, First complete genome sequencing of the genus Virgibacillus: Virgibacillus sp. MSP4-1, an obligate halophile, ICAR Newsletter, 3 Natnan, 2021, Integration of Omics tools for understanding the fish immune response due to microbial challenge, Front. Mar. Sci., 8, 751, 10.3389/fmars.2021.668771 Nyholm, 2000, Establishment of an animal–bacterial association: recruiting symbiotic vibrios from the environment, Proc. Natl. Acad. Sci., 97, 10231, 10.1073/pnas.97.18.10231 Olsen, 2012, A limited supply of fishmeal: impact on future increases in global aquaculture production, Trends Food Sci. Technol., 27, 120, 10.1016/j.tifs.2012.06.003 Osimani, 2019, Hermetia illucens in diets for zebrafish (Danio rerio): a study of bacterial diversity by using PCR-DGGE and metagenomic sequencing, PLoS One, 14, 10.1371/journal.pone.0225956 Parikh, 2016, MeFiT: merging and filtering tool for illumina paired-end reads for 16S rRNA amplicon sequencing, BMC Bioinform., 17, 1, 10.1186/s12859-016-1358-1 Price, 2010, FastTree 2–approximately maximum-likelihood trees for large alignments, PLoS One, 5, 10.1371/journal.pone.0009490 Quast, 2012, The SILVA ribosomal RNA gene database project: improved data processing and web-based tools, Nucleic Acids Res., 41, D590, 10.1093/nar/gks1219 R Core Team, 2013 Ransom, 2008 Rimoldi, 2019, The effects of dietary insect meal from Hermetia illucens prepupae on autochthonous gut microbiota of rainbow trout (Oncorhynchus mykiss), Animals., 9, 143, 10.3390/ani9040143 Rimoldi, 2021, Intestinal microbial communities of rainbow trout (Oncorhynchus mykiss) may be improved by feeding a Hermetia illucens meal/low-fishmeal diet, Fish Physiol. Biochem., 47, 365, 10.1007/s10695-020-00918-1 Robin, 2011, pROC: an open-source package for R and S+ to analyze and compare ROC curves, BMC Bioinform., 12, 1, 10.1186/1471-2105-12-77 Ruettinger, 1981, Epoxidation of unsaturated fatty acids by a soluble cytochrome P-450-dependent system from Bacillus megaterium, J. Biol. Chem., 256, 5728, 10.1016/S0021-9258(19)69267-7 Samanta, 2017, Manipulation of host cholesterol by obligate intracellular bacteria, Front. Cell. Infect. Microbiol., 7, 165, 10.3389/fcimb.2017.00165 Sherry, 2012, Ncbi sra toolkit technology for next generation sequence data Sievers, 2014, 105 Tacon, 2015, Feed matters: satisfying the feed demand of aquaculture, Rev. Fish. Sci. Aquac., 23, 1, 10.1080/23308249.2014.987209 Tegtmeier, 2021, Culture-independent and culture-dependent characterization of the black soldier fly gut microbiome reveals a large proportion of culturable bacteria with potential for industrial applications, Microorganisms., 9, 1642, 10.3390/microorganisms9081642 Terova, 2019, Rainbow trout (Oncorhynchus mykiss) gut microbiota is modulated by insect meal from Hermetia illucens prepupae in the diet, Rev. Fish Biol. Fish., 29, 465, 10.1007/s11160-019-09558-y Tippayadara, 2021, Replacement of fish meal by black soldier fly (Hermetia illucens) larvae meal: effects on growth, haematology, and skin mucus immunity of Nile Tilapia, Oreochromis Niloticus Anim., 11, 193 Torchiano, 2020 Viechtbauer, 2010, Conducting meta-analyses in R with the metafor package, J. Stat. Softw., 36, 1, 10.18637/jss.v036.i03 Weththasinghe, 2021, Dietary inclusion of black soldier fly (Hermetia Illucens) larvae meal and paste improved gut health but had minor effects on skin mucus proteome and immune response in Atlantic salmon (Salmo Salar), Front. Immunol., 12, 114, 10.3389/fimmu.2021.599530 Yang, 2021, Starvation alters gut microbiome in black soldier fly (Diptera: Stratiomyidae) larvae, Front. Microbiol., 12, 160 Yildirim-Aksoy, 2020, Use of dietary frass from black soldier fly larvae, Hermetia illucens, in hybrid tilapia (Nile x Mozambique, Oreocromis niloticus x O. mozambique) diets improves growth and resistance to bacterial diseases, Aquac. Rep., 17 Zarantoniello, 2019, A six-months study on black soldier fly (Hermetia illucens) based diets in zebrafish, Sci. Rep., 9, 1, 10.1038/s41598-019-45172-5 Zhineng, 2021, Intestinal microbiota and functional characteristics of black soldier fly larvae (Hermetia illucens), Ann. Microbiol., 71, 1, 10.1186/s13213-021-01626-8