Insights in the Global Genetics and Gut Microbiome of Black Soldier Fly, Hermetia illucens: Implications for Animal Feed Safety Control

The utilization of the black soldier fly (BSF) Hermetia illucens L. for recycling organic waste into high-quality protein and fat biomass for animal feeds has gained momentum worldwide. However, information on the genetic diversity and environmental implications on safety of the larvae is limited. T...

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Main Authors: Fathiya M. Khamis, Fidelis L. O. Ombura, Komivi S. Akutse, Sevgan Subramanian, Samira A. Mohamed, Komi K. M. Fiaboe, Weerachai Saijuntha, Joop J. A. Van Loon, Marcel Dicke, Thomas Dubois, Sunday Ekesi, Chrysantus M. Tanga
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-07-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fmicb.2020.01538/full
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author Fathiya M. Khamis
Fidelis L. O. Ombura
Komivi S. Akutse
Sevgan Subramanian
Samira A. Mohamed
Komi K. M. Fiaboe
Komi K. M. Fiaboe
Weerachai Saijuntha
Joop J. A. Van Loon
Marcel Dicke
Thomas Dubois
Sunday Ekesi
Chrysantus M. Tanga
spellingShingle Fathiya M. Khamis
Fidelis L. O. Ombura
Komivi S. Akutse
Sevgan Subramanian
Samira A. Mohamed
Komi K. M. Fiaboe
Komi K. M. Fiaboe
Weerachai Saijuntha
Joop J. A. Van Loon
Marcel Dicke
Thomas Dubois
Sunday Ekesi
Chrysantus M. Tanga
Insights in the Global Genetics and Gut Microbiome of Black Soldier Fly, Hermetia illucens: Implications for Animal Feed Safety Control
Frontiers in Microbiology
genetic diversity
gut microbiome
Hermetia illucens
mitochondrial COI gene
16S-metagenomics
author_facet Fathiya M. Khamis
Fidelis L. O. Ombura
Komivi S. Akutse
Sevgan Subramanian
Samira A. Mohamed
Komi K. M. Fiaboe
Komi K. M. Fiaboe
Weerachai Saijuntha
Joop J. A. Van Loon
Marcel Dicke
Thomas Dubois
Sunday Ekesi
Chrysantus M. Tanga
author_sort Fathiya M. Khamis
title Insights in the Global Genetics and Gut Microbiome of Black Soldier Fly, Hermetia illucens: Implications for Animal Feed Safety Control
title_short Insights in the Global Genetics and Gut Microbiome of Black Soldier Fly, Hermetia illucens: Implications for Animal Feed Safety Control
title_full Insights in the Global Genetics and Gut Microbiome of Black Soldier Fly, Hermetia illucens: Implications for Animal Feed Safety Control
title_fullStr Insights in the Global Genetics and Gut Microbiome of Black Soldier Fly, Hermetia illucens: Implications for Animal Feed Safety Control
title_full_unstemmed Insights in the Global Genetics and Gut Microbiome of Black Soldier Fly, Hermetia illucens: Implications for Animal Feed Safety Control
title_sort insights in the global genetics and gut microbiome of black soldier fly, hermetia illucens: implications for animal feed safety control
publisher Frontiers Media S.A.
series Frontiers in Microbiology
issn 1664-302X
publishDate 2020-07-01
description The utilization of the black soldier fly (BSF) Hermetia illucens L. for recycling organic waste into high-quality protein and fat biomass for animal feeds has gained momentum worldwide. However, information on the genetic diversity and environmental implications on safety of the larvae is limited. This study delineates genetic variability and unravels gut microbiome complex of wild-collected and domesticated BSF populations from six continents using mitochondrial COI gene and 16S metagenomics. All sequences generated from the study linked to H. illucens accessions KM967419.1, FJ794355.1, FJ794361.1, FJ794367.1, KC192965.1, and KY817115.1 from GenBank. Phylogenetic analyses of the sequences generated from the study and rooted by GenBank accessions of Hermetia albitarsis Fabricius and Hermetia sexmaculata Macquart separated all samples into three branches, with H. illucens and H. sexmaculata being closely related. Genetic distances between H. illucens samples from the study and GenBank accessions of H. illucens ranged between 0.0091 and 0.0407 while H. sexmaculata and H. albitarsis samples clearly separated from all H. illucens by distances of 0.1745 and 0.1903, respectively. Genetic distance matrix was used to generate a principal coordinate plot that further confirmed the phylogenetic clustering. Haplotype network map demonstrated that Australia, United States 1 (Rhode Island), United States 2 (Colorado), Kenya, and China shared a haplotype, while Uganda shared a haplotype with GenBank accession KC192965 BSF from United States. All other samples analyzed had individual haplotypes. Out of 481,695 reads analyzed from 16S metagenomics, four bacterial families (Enterobactereaceae, Dysgonomonadaceae, Wohlfahrtiimonadaceae, and Enterococcaceae) were most abundant in the BSF samples. Alpha-diversity, as assessed by Shannon index, showed that the Kenyan and Thailand populations had the highest and lowest microbe diversity, respectively; while microbial diversity assessed through Bray Curtis distance showed United States 3 (Maysville) and Netherlands populations to be the most dissimilar. Our findings on genetic diversity revealed slight phylogeographic variation between BSF populations across the globe. The 16S data depicted larval gut bacterial families with economically important genera that might pose health risks to both animals and humans. This study recommends pre-treatment of feedstocks and postharvest measures of the harvested BSF larvae to minimize risk of pathogen contamination along the insect-based feed value chain.
topic genetic diversity
gut microbiome
Hermetia illucens
mitochondrial COI gene
16S-metagenomics
url https://www.frontiersin.org/article/10.3389/fmicb.2020.01538/full
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spelling doaj-b24be550bf2d460dac67a53e8348f1282020-11-25T03:49:53ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2020-07-011110.3389/fmicb.2020.01538548711Insights in the Global Genetics and Gut Microbiome of Black Soldier Fly, Hermetia illucens: Implications for Animal Feed Safety ControlFathiya M. Khamis0Fidelis L. O. Ombura1Komivi S. Akutse2Sevgan Subramanian3Samira A. Mohamed4Komi K. M. Fiaboe5Komi K. M. Fiaboe6Weerachai Saijuntha7Joop J. A. Van Loon8Marcel Dicke9Thomas Dubois10Sunday Ekesi11Chrysantus M. Tanga12Plant Health Theme, International Centre of Insect Physiology and Ecology, Nairobi, KenyaPlant Health Theme, International Centre of Insect Physiology and Ecology, Nairobi, KenyaPlant Health Theme, International Centre of Insect Physiology and Ecology, Nairobi, KenyaPlant Health Theme, International Centre of Insect Physiology and Ecology, Nairobi, KenyaPlant Health Theme, International Centre of Insect Physiology and Ecology, Nairobi, KenyaPlant Health Theme, International Centre of Insect Physiology and Ecology, Nairobi, KenyaDepartment of Integrated Pest Management, International Institute of Tropical Agriculture, Yaounde, CameroonWalai Rukhavej Botanical Research Institute (WRBRI), Biodiversity and Conservation Research Unit, Mahasarakham University, Maha Sarakham, ThailandLaboratory of Entomology, Plant Sciences Group, Wageningen University, Wageningen, NetherlandsLaboratory of Entomology, Plant Sciences Group, Wageningen University, Wageningen, NetherlandsPlant Health Theme, International Centre of Insect Physiology and Ecology, Nairobi, KenyaPlant Health Theme, International Centre of Insect Physiology and Ecology, Nairobi, KenyaPlant Health Theme, International Centre of Insect Physiology and Ecology, Nairobi, KenyaThe utilization of the black soldier fly (BSF) Hermetia illucens L. for recycling organic waste into high-quality protein and fat biomass for animal feeds has gained momentum worldwide. However, information on the genetic diversity and environmental implications on safety of the larvae is limited. This study delineates genetic variability and unravels gut microbiome complex of wild-collected and domesticated BSF populations from six continents using mitochondrial COI gene and 16S metagenomics. All sequences generated from the study linked to H. illucens accessions KM967419.1, FJ794355.1, FJ794361.1, FJ794367.1, KC192965.1, and KY817115.1 from GenBank. Phylogenetic analyses of the sequences generated from the study and rooted by GenBank accessions of Hermetia albitarsis Fabricius and Hermetia sexmaculata Macquart separated all samples into three branches, with H. illucens and H. sexmaculata being closely related. Genetic distances between H. illucens samples from the study and GenBank accessions of H. illucens ranged between 0.0091 and 0.0407 while H. sexmaculata and H. albitarsis samples clearly separated from all H. illucens by distances of 0.1745 and 0.1903, respectively. Genetic distance matrix was used to generate a principal coordinate plot that further confirmed the phylogenetic clustering. Haplotype network map demonstrated that Australia, United States 1 (Rhode Island), United States 2 (Colorado), Kenya, and China shared a haplotype, while Uganda shared a haplotype with GenBank accession KC192965 BSF from United States. All other samples analyzed had individual haplotypes. Out of 481,695 reads analyzed from 16S metagenomics, four bacterial families (Enterobactereaceae, Dysgonomonadaceae, Wohlfahrtiimonadaceae, and Enterococcaceae) were most abundant in the BSF samples. Alpha-diversity, as assessed by Shannon index, showed that the Kenyan and Thailand populations had the highest and lowest microbe diversity, respectively; while microbial diversity assessed through Bray Curtis distance showed United States 3 (Maysville) and Netherlands populations to be the most dissimilar. Our findings on genetic diversity revealed slight phylogeographic variation between BSF populations across the globe. The 16S data depicted larval gut bacterial families with economically important genera that might pose health risks to both animals and humans. This study recommends pre-treatment of feedstocks and postharvest measures of the harvested BSF larvae to minimize risk of pathogen contamination along the insect-based feed value chain.https://www.frontiersin.org/article/10.3389/fmicb.2020.01538/fullgenetic diversitygut microbiomeHermetia illucensmitochondrial COI gene16S-metagenomics