Microbial dynamics and vertical transmission of Escherichia coli across consecutive life stages of the black soldier fly (Hermetia illucens).

IF 4.9 Q1 MICROBIOLOGY
Noor Van Looveren, Freek IJdema, Niels van der Heijden, Mik Van Der Borght, Dries Vandeweyer
{"title":"Microbial dynamics and vertical transmission of Escherichia coli across consecutive life stages of the black soldier fly (Hermetia illucens).","authors":"Noor Van Looveren, Freek IJdema, Niels van der Heijden, Mik Van Der Borght, Dries Vandeweyer","doi":"10.1186/s42523-024-00317-4","DOIUrl":null,"url":null,"abstract":"<p><strong>Background: </strong>The black soldier fly (BSF, Hermetia illucens L.) is one of the most promising insects for bioconversion of organic waste, which often carry a high microbial load with potential foodborne pathogens. Although horizontal transmission (from rearing substrate to larvae) has been extensively studied, less is known about vertical transmission of microorganisms, and particularly of foodborne pathogens, across different BSF life stages.</p><p><strong>Results: </strong>This study investigated the microbial dynamics and vertical transmission of Escherichia coli across different life stages (larvae, prepupae, pupae and adults) of one BSF life cycle and its associated substrate (chicken feed) and frass, based on a combination of general microbial counts (based on culture-dependent techniques) and the bacterial community composition (based on 16S rRNA gene sequencing). Multiple interactions between the microbiota of the substrate, frass and BSF larvae were affirmed. The larvae showed relative consistency among both the microbial counts and bacterial community composition. Diversification of the bacterial communities started during the pupal stage, while most notable changes of the microbial counts and bacterial community compositions occurred during metamorphosis to adults. Furthermore, vertical transmission of E. coli was investigated after substrate inoculation with approximately 7.0 log cfu/g of kanamycin-resistant E. coli, and monitoring E. coli counts from larval to adult stage. Although the frass still contained substantial levels of E. coli (> 4.5 log cfu/g) and E. coli was taken up by the larvae, limited vertical transmission of E. coli was observed with a decreasing trend until the prepupal stage. E. coli counts were below the detection limit (1.0 log cfu/g) for all BSF samples from the end of the pupal stage and the adult stage. Additionally, substrate inoculation of E. coli did not have a substantial impact on the bacterial community composition of the substrate, frass or different BSF life stages.</p><p><strong>Conclusions: </strong>The fluctuating microbial counts and bacterial community composition underscored the dynamic character of the microbiota of BSF life stages. Additionally, vertical transmission throughout one BSF life cycle was not observed for E. coli. Hence, these findings paved the way for future case studies on vertical transmission of foodborne pathogens across consecutive BSF life stages or other insect species.</p>","PeriodicalId":72201,"journal":{"name":"Animal microbiome","volume":null,"pages":null},"PeriodicalIF":4.9000,"publicationDate":"2024-05-26","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11129375/pdf/","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Animal microbiome","FirstCategoryId":"1085","ListUrlMain":"https://doi.org/10.1186/s42523-024-00317-4","RegionNum":0,"RegionCategory":null,"ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"MICROBIOLOGY","Score":null,"Total":0}
引用次数: 0

Abstract

Background: The black soldier fly (BSF, Hermetia illucens L.) is one of the most promising insects for bioconversion of organic waste, which often carry a high microbial load with potential foodborne pathogens. Although horizontal transmission (from rearing substrate to larvae) has been extensively studied, less is known about vertical transmission of microorganisms, and particularly of foodborne pathogens, across different BSF life stages.

Results: This study investigated the microbial dynamics and vertical transmission of Escherichia coli across different life stages (larvae, prepupae, pupae and adults) of one BSF life cycle and its associated substrate (chicken feed) and frass, based on a combination of general microbial counts (based on culture-dependent techniques) and the bacterial community composition (based on 16S rRNA gene sequencing). Multiple interactions between the microbiota of the substrate, frass and BSF larvae were affirmed. The larvae showed relative consistency among both the microbial counts and bacterial community composition. Diversification of the bacterial communities started during the pupal stage, while most notable changes of the microbial counts and bacterial community compositions occurred during metamorphosis to adults. Furthermore, vertical transmission of E. coli was investigated after substrate inoculation with approximately 7.0 log cfu/g of kanamycin-resistant E. coli, and monitoring E. coli counts from larval to adult stage. Although the frass still contained substantial levels of E. coli (> 4.5 log cfu/g) and E. coli was taken up by the larvae, limited vertical transmission of E. coli was observed with a decreasing trend until the prepupal stage. E. coli counts were below the detection limit (1.0 log cfu/g) for all BSF samples from the end of the pupal stage and the adult stage. Additionally, substrate inoculation of E. coli did not have a substantial impact on the bacterial community composition of the substrate, frass or different BSF life stages.

Conclusions: The fluctuating microbial counts and bacterial community composition underscored the dynamic character of the microbiota of BSF life stages. Additionally, vertical transmission throughout one BSF life cycle was not observed for E. coli. Hence, these findings paved the way for future case studies on vertical transmission of foodborne pathogens across consecutive BSF life stages or other insect species.

大肠埃希氏菌在黑兵蝇(Hermetia illucens)连续生命阶段中的微生物动态和垂直传播。
背景:黑兵蝇(BSF,Hermetia illucens L.)是最有希望对有机废物进行生物转化的昆虫之一,而有机废物中往往含有大量微生物和潜在的食源性病原体。虽然对横向传播(从饲养基质到幼虫)进行了广泛研究,但对微生物,特别是食源性病原体在 BSF 不同生命阶段的纵向传播了解较少:本研究根据一般微生物计数(基于依赖培养的技术)和细菌群落组成(基于 16S rRNA 基因测序),调查了大肠埃希氏菌在一个 BSF 生命周期的不同生命阶段(幼虫、蛹、蛹和成虫)及其相关基质(鸡饲料)和粪便中的微生物动态和垂直传播。基质、粪便和 BSF 幼虫的微生物群落之间存在多种相互作用。幼虫在微生物数量和细菌群落组成方面表现出相对的一致性。细菌群落的多样化始于蛹期,而微生物数量和细菌群落组成的最显著变化则发生在成虫蜕变期。此外,在基质中接种约 7.0 log cfu/g 的耐卡那霉素大肠杆菌,并监测从幼虫到成虫阶段的大肠杆菌数量后,研究了大肠杆菌的垂直传播。尽管虫粪中仍含有大量大肠杆菌(> 4.5 log cfu/g),而且幼虫也吸收了大肠杆菌,但观察到大肠杆菌的垂直传播有限,且呈下降趋势,直至成虫期。在蛹末期和成虫期的所有 BSF 样品中,大肠杆菌计数均低于检测限(1.0 log cfu/g)。此外,在基质中接种大肠杆菌对基质、虫粪或 BSF 不同生命阶段的细菌群落组成没有实质性影响:微生物数量和细菌群落组成的波动凸显了 BSF 生命阶段微生物群落的动态特征。此外,在 BSF 的一个生命周期中没有观察到大肠杆菌的垂直传播。因此,这些发现为今后开展有关食源性病原体在连续的 BSF 生命阶段或其他昆虫物种之间垂直传播的案例研究铺平了道路。
本文章由计算机程序翻译,如有差异,请以英文原文为准。
求助全文
约1分钟内获得全文 求助全文
来源期刊
CiteScore
7.20
自引率
0.00%
发文量
0
审稿时长
13 weeks
×
引用
GB/T 7714-2015
复制
MLA
复制
APA
复制
导出至
BibTeX EndNote RefMan NoteFirst NoteExpress
×
提示
您的信息不完整,为了账户安全,请先补充。
现在去补充
×
提示
您因"违规操作"
具体请查看互助需知
我知道了
×
提示
确定
请完成安全验证×
copy
已复制链接
快去分享给好友吧!
我知道了
右上角分享
点击右上角分享
0
联系我们:info@booksci.cn Book学术提供免费学术资源搜索服务,方便国内外学者检索中英文文献。致力于提供最便捷和优质的服务体验。 Copyright © 2023 布克学术 All rights reserved.
京ICP备2023020795号-1
ghs 京公网安备 11010802042870号
Book学术文献互助
Book学术文献互助群
群 号:481959085
Book学术官方微信