Gut microbiome of mealworms (Tenebrio molitor Larvae) show similar responses to polystyrene and corn straw diets
Abstract Background Some insects can degrade both natural and synthetic plastic polymers, their host and gut microbes play crucial roles in this process. However, there is still a scientific gap in understanding how the insect adapted to the polystyrene (PS) diet from natural feed. In this study, we...
| Main Authors: | , , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
BMC
2023-05-01
|
| Series: | Microbiome |
| Subjects: | |
| Online Access: | https://doi.org/10.1186/s40168-023-01550-w |
| _version_ | 1797831969750384640 |
|---|---|
| author | Tursunay Mamtimin Huawen Han Aman Khan Pengya Feng Qing Zhang Xiaobiao Ma Yitian Fang Pu Liu Saurabh Kulshrestha Toshiro Shigaki Xiangkai Li |
| author_facet | Tursunay Mamtimin Huawen Han Aman Khan Pengya Feng Qing Zhang Xiaobiao Ma Yitian Fang Pu Liu Saurabh Kulshrestha Toshiro Shigaki Xiangkai Li |
| author_sort | Tursunay Mamtimin |
| collection | DOAJ |
| description | Abstract Background Some insects can degrade both natural and synthetic plastic polymers, their host and gut microbes play crucial roles in this process. However, there is still a scientific gap in understanding how the insect adapted to the polystyrene (PS) diet from natural feed. In this study, we analyzed diet consumption, gut microbiota responses, and metabolic pathways of Tenebrio molitor larvae exposed to PS and corn straw (CS). Results T. molitor larvae were incubated under controlled conditions (25 ± 1 °C, 75 ± 5% humidity) for 30 days by using PS foam with weight-, number-, and size-average molecular weight (Mw, Mn, and Mz) of 120.0, 73.2, and 150.7 kDa as a diet, respectively. The larvae exhibited lower PS consumption (32.5%) than CS (52.0%), and these diets had no adverse effects on their survival. The gut microbiota structures, metabolic pathways, and enzymatic profiles of PS- and CS-fed larvae showed similar responses. The gut microbiota of larvae analysis indicated Serratia sp., Staphylococcus sp., and Rhodococcus sp. were associated with both PS and CS diets. Metatranscriptomic analysis revealed that xenobiotics, aromatic compounds, and fatty acid degradation pathways were enriched in PS- and CS-fed groups; laccase-like multicopper oxidases, cytochrome P450, monooxygenase, superoxidase, and dehydrogenase were involved in lignin and PS degradation. Furthermore, the upregulated gene lac640 in both PS- and CS-fed groups was overexpressed in E. coli and exhibited PS and lignin degradation ability. Conclusions The high similarity of gut microbiomes adapted to biodegradation of PS and CS indicated the plastics-degrading ability of the T. molitor larvae originated through an ancient mechanism that degrades the natural lignocellulose. Video Abstract Graphical Abstract |
| first_indexed | 2024-04-09T14:01:18Z |
| format | Article |
| id | doaj.art-9de14a30c0584719b72afceb813ec522 |
| institution | Directory Open Access Journal |
| issn | 2049-2618 |
| language | English |
| last_indexed | 2024-04-09T14:01:18Z |
| publishDate | 2023-05-01 |
| publisher | BMC |
| record_format | Article |
| series | Microbiome |
| spelling | doaj.art-9de14a30c0584719b72afceb813ec5222023-05-07T11:18:34ZengBMCMicrobiome2049-26182023-05-0111112010.1186/s40168-023-01550-wGut microbiome of mealworms (Tenebrio molitor Larvae) show similar responses to polystyrene and corn straw dietsTursunay Mamtimin0Huawen Han1Aman Khan2Pengya Feng3Qing Zhang4Xiaobiao Ma5Yitian Fang6Pu Liu7Saurabh Kulshrestha8Toshiro Shigaki9Xiangkai Li10Ministry of Education Key Laboratory of Cell Activities and Stress Adaptations, School of Life Science, Lanzhou UniversityMinistry of Education Key Laboratory of Cell Activities and Stress Adaptations, School of Life Science, Lanzhou UniversityMinistry of Education Key Laboratory of Cell Activities and Stress Adaptations, School of Life Science, Lanzhou UniversityMinistry of Education Key Laboratory of Cell Activities and Stress Adaptations, School of Life Science, Lanzhou UniversityMinistry of Education Key Laboratory of Cell Activities and Stress Adaptations, School of Life Science, Lanzhou UniversityMinistry of Education Key Laboratory of Cell Activities and Stress Adaptations, School of Life Science, Lanzhou UniversityState Key Laboratory of Microbial Metabolism, School of Life Sciences and Biotechnology, Shanghai Jiao Tong UniversityMinistry of Education Key Laboratory of Cell Activities and Stress Adaptations, School of Life Science, Lanzhou UniversityFaculty of Applied Sciences and Biotechnology, Shoolini UniversityGraduate School of Agricultural and Life Sciences, The University of TokyoMinistry of Education Key Laboratory of Cell Activities and Stress Adaptations, School of Life Science, Lanzhou UniversityAbstract Background Some insects can degrade both natural and synthetic plastic polymers, their host and gut microbes play crucial roles in this process. However, there is still a scientific gap in understanding how the insect adapted to the polystyrene (PS) diet from natural feed. In this study, we analyzed diet consumption, gut microbiota responses, and metabolic pathways of Tenebrio molitor larvae exposed to PS and corn straw (CS). Results T. molitor larvae were incubated under controlled conditions (25 ± 1 °C, 75 ± 5% humidity) for 30 days by using PS foam with weight-, number-, and size-average molecular weight (Mw, Mn, and Mz) of 120.0, 73.2, and 150.7 kDa as a diet, respectively. The larvae exhibited lower PS consumption (32.5%) than CS (52.0%), and these diets had no adverse effects on their survival. The gut microbiota structures, metabolic pathways, and enzymatic profiles of PS- and CS-fed larvae showed similar responses. The gut microbiota of larvae analysis indicated Serratia sp., Staphylococcus sp., and Rhodococcus sp. were associated with both PS and CS diets. Metatranscriptomic analysis revealed that xenobiotics, aromatic compounds, and fatty acid degradation pathways were enriched in PS- and CS-fed groups; laccase-like multicopper oxidases, cytochrome P450, monooxygenase, superoxidase, and dehydrogenase were involved in lignin and PS degradation. Furthermore, the upregulated gene lac640 in both PS- and CS-fed groups was overexpressed in E. coli and exhibited PS and lignin degradation ability. Conclusions The high similarity of gut microbiomes adapted to biodegradation of PS and CS indicated the plastics-degrading ability of the T. molitor larvae originated through an ancient mechanism that degrades the natural lignocellulose. Video Abstract Graphical Abstracthttps://doi.org/10.1186/s40168-023-01550-wTenebrio molitorPolystyreneCorn strawMicrobial communityMetabolic pathwayBiodegradation |
| spellingShingle | Tursunay Mamtimin Huawen Han Aman Khan Pengya Feng Qing Zhang Xiaobiao Ma Yitian Fang Pu Liu Saurabh Kulshrestha Toshiro Shigaki Xiangkai Li Gut microbiome of mealworms (Tenebrio molitor Larvae) show similar responses to polystyrene and corn straw diets Microbiome Tenebrio molitor Polystyrene Corn straw Microbial community Metabolic pathway Biodegradation |
| title | Gut microbiome of mealworms (Tenebrio molitor Larvae) show similar responses to polystyrene and corn straw diets |
| title_full | Gut microbiome of mealworms (Tenebrio molitor Larvae) show similar responses to polystyrene and corn straw diets |
| title_fullStr | Gut microbiome of mealworms (Tenebrio molitor Larvae) show similar responses to polystyrene and corn straw diets |
| title_full_unstemmed | Gut microbiome of mealworms (Tenebrio molitor Larvae) show similar responses to polystyrene and corn straw diets |
| title_short | Gut microbiome of mealworms (Tenebrio molitor Larvae) show similar responses to polystyrene and corn straw diets |
| title_sort | gut microbiome of mealworms tenebrio molitor larvae show similar responses to polystyrene and corn straw diets |
| topic | Tenebrio molitor Polystyrene Corn straw Microbial community Metabolic pathway Biodegradation |
| url | https://doi.org/10.1186/s40168-023-01550-w |
| work_keys_str_mv | AT tursunaymamtimin gutmicrobiomeofmealwormstenebriomolitorlarvaeshowsimilarresponsestopolystyreneandcornstrawdiets AT huawenhan gutmicrobiomeofmealwormstenebriomolitorlarvaeshowsimilarresponsestopolystyreneandcornstrawdiets AT amankhan gutmicrobiomeofmealwormstenebriomolitorlarvaeshowsimilarresponsestopolystyreneandcornstrawdiets AT pengyafeng gutmicrobiomeofmealwormstenebriomolitorlarvaeshowsimilarresponsestopolystyreneandcornstrawdiets AT qingzhang gutmicrobiomeofmealwormstenebriomolitorlarvaeshowsimilarresponsestopolystyreneandcornstrawdiets AT xiaobiaoma gutmicrobiomeofmealwormstenebriomolitorlarvaeshowsimilarresponsestopolystyreneandcornstrawdiets AT yitianfang gutmicrobiomeofmealwormstenebriomolitorlarvaeshowsimilarresponsestopolystyreneandcornstrawdiets AT puliu gutmicrobiomeofmealwormstenebriomolitorlarvaeshowsimilarresponsestopolystyreneandcornstrawdiets AT saurabhkulshrestha gutmicrobiomeofmealwormstenebriomolitorlarvaeshowsimilarresponsestopolystyreneandcornstrawdiets AT toshiroshigaki gutmicrobiomeofmealwormstenebriomolitorlarvaeshowsimilarresponsestopolystyreneandcornstrawdiets AT xiangkaili gutmicrobiomeofmealwormstenebriomolitorlarvaeshowsimilarresponsestopolystyreneandcornstrawdiets |