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Selective breeding of cold-tolerant black soldier fly (Hermetia illucens) larvae: Gut microbial shifts and transcriptional patterns
•Three commercial BSF colonies were identified in China.•Enterococcus and Vagococcus are dominant genera in cold-tolerant BSFL bred at 16℃.•A series of gene pathways are associated with the development of cold tolerance. The larvae of black soldier fly (BSFL) convert organic waste into insect protei...
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Published in: | Waste management (Elmsford) 2024-04, Vol.177, p.252-265 |
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description | •Three commercial BSF colonies were identified in China.•Enterococcus and Vagococcus are dominant genera in cold-tolerant BSFL bred at 16℃.•A series of gene pathways are associated with the development of cold tolerance.
The larvae of black soldier fly (BSFL) convert organic waste into insect proteins used as feedstuff for livestock and aquaculture. BSFL production performance is considerably reduced during winter season. Herein, the intraspecific diversity of ten commercial BSF colonies collected in China was evaluated. The Bioforte colony was subjected to selective breeding at 12 °C and 16 °C to develop cold-tolerant BSF with improved production performance. After breeding for nine generations, the weight of larvae, survival rate, and the dry matter conversion rate significantly increased. Subsequently, intestinal microbiota in the cold-tolerant strain showed that bacteria belonging to Morganella, Dysgonomonas, Salmonella, Pseudochrobactrum, and Klebsiella genera were highly represented in the 12 °C bred, while those of Acinetobacter, Pseudochrobactrum, Enterococcus, Comamonas, and Leucobacter genera were significantly represented in the 16 °C bred group. Metagenomic revealed that several animal probiotics of the Enterococcus and Vagococcus genera were greatly enriched in the gut of larvae bred at 16 °C. Moreover, bacterial metabolic pathways including carbohydrate, lipid, amino acids, and cofactors and vitamins, were significantly increased, while organismal systems and human diseases was decreased in the 16 °C bred group. Transcriptomic analysis revealed that the upregulated differentially expressed genes in the 16 °C bred groups mainly participated in Autophagy-animal, AMPK signaling pathway, mTOR signaling pathway, Wnt signaling pathway, FoxO signaling pathway, Hippo signaling pathway at day 34 under 16 °C conditions, suggesting their significant role in the survival of BSFL. Taken together, these results shed lights on the role of intestinal microflora and gene pathways in the adaptation of BSF larvae to cold stress. |
doi_str_mv | 10.1016/j.wasman.2024.02.007 |
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The larvae of black soldier fly (BSFL) convert organic waste into insect proteins used as feedstuff for livestock and aquaculture. BSFL production performance is considerably reduced during winter season. Herein, the intraspecific diversity of ten commercial BSF colonies collected in China was evaluated. The Bioforte colony was subjected to selective breeding at 12 °C and 16 °C to develop cold-tolerant BSF with improved production performance. After breeding for nine generations, the weight of larvae, survival rate, and the dry matter conversion rate significantly increased. Subsequently, intestinal microbiota in the cold-tolerant strain showed that bacteria belonging to Morganella, Dysgonomonas, Salmonella, Pseudochrobactrum, and Klebsiella genera were highly represented in the 12 °C bred, while those of Acinetobacter, Pseudochrobactrum, Enterococcus, Comamonas, and Leucobacter genera were significantly represented in the 16 °C bred group. Metagenomic revealed that several animal probiotics of the Enterococcus and Vagococcus genera were greatly enriched in the gut of larvae bred at 16 °C. Moreover, bacterial metabolic pathways including carbohydrate, lipid, amino acids, and cofactors and vitamins, were significantly increased, while organismal systems and human diseases was decreased in the 16 °C bred group. Transcriptomic analysis revealed that the upregulated differentially expressed genes in the 16 °C bred groups mainly participated in Autophagy-animal, AMPK signaling pathway, mTOR signaling pathway, Wnt signaling pathway, FoxO signaling pathway, Hippo signaling pathway at day 34 under 16 °C conditions, suggesting their significant role in the survival of BSFL. Taken together, these results shed lights on the role of intestinal microflora and gene pathways in the adaptation of BSF larvae to cold stress.</description><identifier>ISSN: 0956-053X</identifier><identifier>EISSN: 1879-2456</identifier><identifier>DOI: 10.1016/j.wasman.2024.02.007</identifier><identifier>PMID: 38354633</identifier><language>eng</language><publisher>United States: Elsevier Ltd</publisher><subject>Amino Acids ; Animals ; Cold tolerance ; Diptera - genetics ; Gastrointestinal Microbiome ; Hermetia illucens L ; Humans ; Intestinal microflora ; Larva - genetics ; Metagenome ; Selective Breeding ; Transcriptome</subject><ispartof>Waste management (Elmsford), 2024-04, Vol.177, p.252-265</ispartof><rights>2024 Elsevier Ltd</rights><rights>Copyright © 2024 Elsevier Ltd. All rights reserved.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c311t-2b57f1cfa34009156331a984652b01af17e2ef0885fc329aea7cff3272a3ff9f3</cites><orcidid>0000-0002-4251-1322 ; 0000-0001-6511-9772 ; 0000-0002-6670-3062 ; 0009-0009-6023-0506</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,780,784,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/38354633$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Ma, Chong</creatorcontrib><creatorcontrib>Huang, Zhijun</creatorcontrib><creatorcontrib>Feng, Xingbao</creatorcontrib><creatorcontrib>Memon, Fareed Uddin</creatorcontrib><creatorcontrib>Cui, Ying</creatorcontrib><creatorcontrib>Duan, Xinyu</creatorcontrib><creatorcontrib>Zhu, Jianfeng</creatorcontrib><creatorcontrib>Tettamanti, Gianluca</creatorcontrib><creatorcontrib>Hu, Wenfeng</creatorcontrib><creatorcontrib>Tian, Ling</creatorcontrib><title>Selective breeding of cold-tolerant black soldier fly (Hermetia illucens) larvae: Gut microbial shifts and transcriptional patterns</title><title>Waste management (Elmsford)</title><addtitle>Waste Manag</addtitle><description>•Three commercial BSF colonies were identified in China.•Enterococcus and Vagococcus are dominant genera in cold-tolerant BSFL bred at 16℃.•A series of gene pathways are associated with the development of cold tolerance.
The larvae of black soldier fly (BSFL) convert organic waste into insect proteins used as feedstuff for livestock and aquaculture. BSFL production performance is considerably reduced during winter season. Herein, the intraspecific diversity of ten commercial BSF colonies collected in China was evaluated. The Bioforte colony was subjected to selective breeding at 12 °C and 16 °C to develop cold-tolerant BSF with improved production performance. After breeding for nine generations, the weight of larvae, survival rate, and the dry matter conversion rate significantly increased. Subsequently, intestinal microbiota in the cold-tolerant strain showed that bacteria belonging to Morganella, Dysgonomonas, Salmonella, Pseudochrobactrum, and Klebsiella genera were highly represented in the 12 °C bred, while those of Acinetobacter, Pseudochrobactrum, Enterococcus, Comamonas, and Leucobacter genera were significantly represented in the 16 °C bred group. Metagenomic revealed that several animal probiotics of the Enterococcus and Vagococcus genera were greatly enriched in the gut of larvae bred at 16 °C. Moreover, bacterial metabolic pathways including carbohydrate, lipid, amino acids, and cofactors and vitamins, were significantly increased, while organismal systems and human diseases was decreased in the 16 °C bred group. Transcriptomic analysis revealed that the upregulated differentially expressed genes in the 16 °C bred groups mainly participated in Autophagy-animal, AMPK signaling pathway, mTOR signaling pathway, Wnt signaling pathway, FoxO signaling pathway, Hippo signaling pathway at day 34 under 16 °C conditions, suggesting their significant role in the survival of BSFL. Taken together, these results shed lights on the role of intestinal microflora and gene pathways in the adaptation of BSF larvae to cold stress.</description><subject>Amino Acids</subject><subject>Animals</subject><subject>Cold tolerance</subject><subject>Diptera - genetics</subject><subject>Gastrointestinal Microbiome</subject><subject>Hermetia illucens L</subject><subject>Humans</subject><subject>Intestinal microflora</subject><subject>Larva - genetics</subject><subject>Metagenome</subject><subject>Selective Breeding</subject><subject>Transcriptome</subject><issn>0956-053X</issn><issn>1879-2456</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><recordid>eNp9kUuLFDEQgIMo7rj6D0RyXA_dVpJ-ehBk0V1hwYMK3kJ1uqIZ0-kxSY_s2T9ullk9egpUvnp9xdhzAbUA0b3a178wLRhqCbKpQdYA_QO2E0M_VrJpu4dsB2PbVdCqr2fsSUp7ANEMAh6zMzWotumU2rHfn8iTye5IfIpEswvf-Gq5Wf1c5dVTxJD55NH84KnEHEVu_S2_uKa4UHbInfeboZBeco_xiPSaX22ZL87EdXLoefrubE4cw8xzKZZMdIfs1lC-DpgzxZCeskcWfaJn9-85-_L-3efL6-rm49WHy7c3lVFC5EpObW-FsagagFG0ZX6B49B0rZxAoBU9SbIwDK01So5I2BtrlewlKmtHq87ZxanuIa4_N0pZLy4Z8h4DrVvSciwsjD2ogjYntKyRUiSrD9EtGG-1AH2nX-_1Sb--069B6qK_pL2477BNC83_kv76LsCbE0Blz2OxqZNxFEwRH8sZ9Ly6_3f4Awqkmq8</recordid><startdate>20240401</startdate><enddate>20240401</enddate><creator>Ma, Chong</creator><creator>Huang, Zhijun</creator><creator>Feng, Xingbao</creator><creator>Memon, Fareed Uddin</creator><creator>Cui, Ying</creator><creator>Duan, Xinyu</creator><creator>Zhu, Jianfeng</creator><creator>Tettamanti, Gianluca</creator><creator>Hu, Wenfeng</creator><creator>Tian, Ling</creator><general>Elsevier Ltd</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0002-4251-1322</orcidid><orcidid>https://orcid.org/0000-0001-6511-9772</orcidid><orcidid>https://orcid.org/0000-0002-6670-3062</orcidid><orcidid>https://orcid.org/0009-0009-6023-0506</orcidid></search><sort><creationdate>20240401</creationdate><title>Selective breeding of cold-tolerant black soldier fly (Hermetia illucens) larvae: Gut microbial shifts and transcriptional patterns</title><author>Ma, Chong ; Huang, Zhijun ; Feng, Xingbao ; Memon, Fareed Uddin ; Cui, Ying ; Duan, Xinyu ; Zhu, Jianfeng ; Tettamanti, Gianluca ; Hu, Wenfeng ; Tian, Ling</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c311t-2b57f1cfa34009156331a984652b01af17e2ef0885fc329aea7cff3272a3ff9f3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>Amino Acids</topic><topic>Animals</topic><topic>Cold tolerance</topic><topic>Diptera - genetics</topic><topic>Gastrointestinal Microbiome</topic><topic>Hermetia illucens L</topic><topic>Humans</topic><topic>Intestinal microflora</topic><topic>Larva - genetics</topic><topic>Metagenome</topic><topic>Selective Breeding</topic><topic>Transcriptome</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Ma, Chong</creatorcontrib><creatorcontrib>Huang, Zhijun</creatorcontrib><creatorcontrib>Feng, Xingbao</creatorcontrib><creatorcontrib>Memon, Fareed Uddin</creatorcontrib><creatorcontrib>Cui, Ying</creatorcontrib><creatorcontrib>Duan, Xinyu</creatorcontrib><creatorcontrib>Zhu, Jianfeng</creatorcontrib><creatorcontrib>Tettamanti, Gianluca</creatorcontrib><creatorcontrib>Hu, Wenfeng</creatorcontrib><creatorcontrib>Tian, Ling</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><jtitle>Waste management (Elmsford)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Ma, Chong</au><au>Huang, Zhijun</au><au>Feng, Xingbao</au><au>Memon, Fareed Uddin</au><au>Cui, Ying</au><au>Duan, Xinyu</au><au>Zhu, Jianfeng</au><au>Tettamanti, Gianluca</au><au>Hu, Wenfeng</au><au>Tian, Ling</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Selective breeding of cold-tolerant black soldier fly (Hermetia illucens) larvae: Gut microbial shifts and transcriptional patterns</atitle><jtitle>Waste management (Elmsford)</jtitle><addtitle>Waste Manag</addtitle><date>2024-04-01</date><risdate>2024</risdate><volume>177</volume><spage>252</spage><epage>265</epage><pages>252-265</pages><issn>0956-053X</issn><eissn>1879-2456</eissn><abstract>•Three commercial BSF colonies were identified in China.•Enterococcus and Vagococcus are dominant genera in cold-tolerant BSFL bred at 16℃.•A series of gene pathways are associated with the development of cold tolerance.
The larvae of black soldier fly (BSFL) convert organic waste into insect proteins used as feedstuff for livestock and aquaculture. BSFL production performance is considerably reduced during winter season. Herein, the intraspecific diversity of ten commercial BSF colonies collected in China was evaluated. The Bioforte colony was subjected to selective breeding at 12 °C and 16 °C to develop cold-tolerant BSF with improved production performance. After breeding for nine generations, the weight of larvae, survival rate, and the dry matter conversion rate significantly increased. Subsequently, intestinal microbiota in the cold-tolerant strain showed that bacteria belonging to Morganella, Dysgonomonas, Salmonella, Pseudochrobactrum, and Klebsiella genera were highly represented in the 12 °C bred, while those of Acinetobacter, Pseudochrobactrum, Enterococcus, Comamonas, and Leucobacter genera were significantly represented in the 16 °C bred group. Metagenomic revealed that several animal probiotics of the Enterococcus and Vagococcus genera were greatly enriched in the gut of larvae bred at 16 °C. Moreover, bacterial metabolic pathways including carbohydrate, lipid, amino acids, and cofactors and vitamins, were significantly increased, while organismal systems and human diseases was decreased in the 16 °C bred group. Transcriptomic analysis revealed that the upregulated differentially expressed genes in the 16 °C bred groups mainly participated in Autophagy-animal, AMPK signaling pathway, mTOR signaling pathway, Wnt signaling pathway, FoxO signaling pathway, Hippo signaling pathway at day 34 under 16 °C conditions, suggesting their significant role in the survival of BSFL. Taken together, these results shed lights on the role of intestinal microflora and gene pathways in the adaptation of BSF larvae to cold stress.</abstract><cop>United States</cop><pub>Elsevier Ltd</pub><pmid>38354633</pmid><doi>10.1016/j.wasman.2024.02.007</doi><tpages>14</tpages><orcidid>https://orcid.org/0000-0002-4251-1322</orcidid><orcidid>https://orcid.org/0000-0001-6511-9772</orcidid><orcidid>https://orcid.org/0000-0002-6670-3062</orcidid><orcidid>https://orcid.org/0009-0009-6023-0506</orcidid></addata></record> |
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subjects | Amino Acids Animals Cold tolerance Diptera - genetics Gastrointestinal Microbiome Hermetia illucens L Humans Intestinal microflora Larva - genetics Metagenome Selective Breeding Transcriptome |
title | Selective breeding of cold-tolerant black soldier fly (Hermetia illucens) larvae: Gut microbial shifts and transcriptional patterns |
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