Cargando…

Gut microbiome of mealworms (Tenebrio molitor Larvae) show similar responses to polystyrene and corn straw diets

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 analyze...

Descripción completa

Detalles Bibliográficos
Autores principales: Mamtimin, Tursunay, Han, Huawen, Khan, Aman, Feng, Pengya, Zhang, Qing, Ma, Xiaobiao, Fang, Yitian, Liu, Pu, Kulshrestha, Saurabh, Shigaki, Toshiro, Li, Xiangkai
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10161430/
https://www.ncbi.nlm.nih.gov/pubmed/37147715
http://dx.doi.org/10.1186/s40168-023-01550-w
_version_ 1785037491920699392
author Mamtimin, Tursunay
Han, Huawen
Khan, Aman
Feng, Pengya
Zhang, Qing
Ma, Xiaobiao
Fang, Yitian
Liu, Pu
Kulshrestha, Saurabh
Shigaki, Toshiro
Li, Xiangkai
author_facet Mamtimin, Tursunay
Han, Huawen
Khan, Aman
Feng, Pengya
Zhang, Qing
Ma, Xiaobiao
Fang, Yitian
Liu, Pu
Kulshrestha, Saurabh
Shigaki, Toshiro
Li, Xiangkai
author_sort Mamtimin, Tursunay
collection PubMed
description 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. GRAPHICAL ABSTRACT: [Image: see text] SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40168-023-01550-w.
format Online
Article
Text
id pubmed-10161430
institution National Center for Biotechnology Information
language English
publishDate 2023
publisher BioMed Central
record_format MEDLINE/PubMed
spelling pubmed-101614302023-05-06 Gut microbiome of mealworms (Tenebrio molitor Larvae) show similar responses to polystyrene and corn straw diets Mamtimin, Tursunay Han, Huawen Khan, Aman Feng, Pengya Zhang, Qing Ma, Xiaobiao Fang, Yitian Liu, Pu Kulshrestha, Saurabh Shigaki, Toshiro Li, Xiangkai Microbiome Research 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. GRAPHICAL ABSTRACT: [Image: see text] SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40168-023-01550-w. BioMed Central 2023-05-05 /pmc/articles/PMC10161430/ /pubmed/37147715 http://dx.doi.org/10.1186/s40168-023-01550-w Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Mamtimin, Tursunay
Han, Huawen
Khan, Aman
Feng, Pengya
Zhang, Qing
Ma, Xiaobiao
Fang, Yitian
Liu, Pu
Kulshrestha, Saurabh
Shigaki, Toshiro
Li, Xiangkai
Gut microbiome of mealworms (Tenebrio molitor Larvae) show similar responses to polystyrene and corn straw diets
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 Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10161430/
https://www.ncbi.nlm.nih.gov/pubmed/37147715
http://dx.doi.org/10.1186/s40168-023-01550-w
work_keys_str_mv AT mamtimintursunay gutmicrobiomeofmealwormstenebriomolitorlarvaeshowsimilarresponsestopolystyreneandcornstrawdiets
AT hanhuawen gutmicrobiomeofmealwormstenebriomolitorlarvaeshowsimilarresponsestopolystyreneandcornstrawdiets
AT khanaman gutmicrobiomeofmealwormstenebriomolitorlarvaeshowsimilarresponsestopolystyreneandcornstrawdiets
AT fengpengya gutmicrobiomeofmealwormstenebriomolitorlarvaeshowsimilarresponsestopolystyreneandcornstrawdiets
AT zhangqing gutmicrobiomeofmealwormstenebriomolitorlarvaeshowsimilarresponsestopolystyreneandcornstrawdiets
AT maxiaobiao gutmicrobiomeofmealwormstenebriomolitorlarvaeshowsimilarresponsestopolystyreneandcornstrawdiets
AT fangyitian gutmicrobiomeofmealwormstenebriomolitorlarvaeshowsimilarresponsestopolystyreneandcornstrawdiets
AT liupu gutmicrobiomeofmealwormstenebriomolitorlarvaeshowsimilarresponsestopolystyreneandcornstrawdiets
AT kulshresthasaurabh gutmicrobiomeofmealwormstenebriomolitorlarvaeshowsimilarresponsestopolystyreneandcornstrawdiets
AT shigakitoshiro gutmicrobiomeofmealwormstenebriomolitorlarvaeshowsimilarresponsestopolystyreneandcornstrawdiets
AT lixiangkai gutmicrobiomeofmealwormstenebriomolitorlarvaeshowsimilarresponsestopolystyreneandcornstrawdiets