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Plastics shape the black soldier fly larvae gut microbiome and select for biodegrading functions

BACKGROUND: In the last few years, considerable attention has been focused on the plastic-degrading capability of insects and their gut microbiota in order to develop novel, effective, and green strategies for plastic waste management. Although many analyses based on 16S rRNA gene sequencing are ava...

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Autores principales: De Filippis, Francesca, Bonelli, Marco, Bruno, Daniele, Sequino, Giuseppina, Montali, Aurora, Reguzzoni, Marcella, Pasolli, Edoardo, Savy, Davide, Cangemi, Silvana, Cozzolino, Vincenza, Tettamanti, Gianluca, Ercolini, Danilo, Casartelli, Morena, Caccia, Silvia
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10500907/
https://www.ncbi.nlm.nih.gov/pubmed/37705113
http://dx.doi.org/10.1186/s40168-023-01649-0
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author De Filippis, Francesca
Bonelli, Marco
Bruno, Daniele
Sequino, Giuseppina
Montali, Aurora
Reguzzoni, Marcella
Pasolli, Edoardo
Savy, Davide
Cangemi, Silvana
Cozzolino, Vincenza
Tettamanti, Gianluca
Ercolini, Danilo
Casartelli, Morena
Caccia, Silvia
author_facet De Filippis, Francesca
Bonelli, Marco
Bruno, Daniele
Sequino, Giuseppina
Montali, Aurora
Reguzzoni, Marcella
Pasolli, Edoardo
Savy, Davide
Cangemi, Silvana
Cozzolino, Vincenza
Tettamanti, Gianluca
Ercolini, Danilo
Casartelli, Morena
Caccia, Silvia
author_sort De Filippis, Francesca
collection PubMed
description BACKGROUND: In the last few years, considerable attention has been focused on the plastic-degrading capability of insects and their gut microbiota in order to develop novel, effective, and green strategies for plastic waste management. Although many analyses based on 16S rRNA gene sequencing are available, an in-depth analysis of the insect gut microbiome to identify genes with plastic-degrading potential is still lacking. RESULTS: In the present work, we aim to fill this gap using Black Soldier Fly (BSF) as insect model. BSF larvae have proven capability to efficiently bioconvert a wide variety of organic wastes but, surprisingly, have never been considered for plastic degradation. BSF larvae were reared on two widely used plastic polymers and shotgun metagenomics was exploited to evaluate if and how plastic-containing diets affect composition and functions of the gut microbial community. The high-definition picture of the BSF gut microbiome gave access for the first time to the genomes of culturable and unculturable microorganisms in the gut of insects reared on plastics and revealed that (i) plastics significantly shaped bacterial composition at species and strain level, and (ii) functions that trigger the degradation of the polymer chains, i.e., DyP-type peroxidases, multicopper oxidases, and alkane monooxygenases, were highly enriched in the metagenomes upon exposure to plastics, consistently with the evidences obtained by scanning electron microscopy and (1)H nuclear magnetic resonance analyses on plastics. CONCLUSIONS: In addition to highlighting that the astonishing plasticity of the microbiota composition of BSF larvae is associated with functional shifts in the insect microbiome, the present work sets the stage for exploiting BSF larvae as “bioincubators” to isolate microbial strains and enzymes for the development of innovative plastic biodegradation strategies. However, most importantly, the larvae constitute a source of enzymes to be evolved and valorized by pioneering synthetic biology approaches. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40168-023-01649-0.
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spelling pubmed-105009072023-09-15 Plastics shape the black soldier fly larvae gut microbiome and select for biodegrading functions De Filippis, Francesca Bonelli, Marco Bruno, Daniele Sequino, Giuseppina Montali, Aurora Reguzzoni, Marcella Pasolli, Edoardo Savy, Davide Cangemi, Silvana Cozzolino, Vincenza Tettamanti, Gianluca Ercolini, Danilo Casartelli, Morena Caccia, Silvia Microbiome Research BACKGROUND: In the last few years, considerable attention has been focused on the plastic-degrading capability of insects and their gut microbiota in order to develop novel, effective, and green strategies for plastic waste management. Although many analyses based on 16S rRNA gene sequencing are available, an in-depth analysis of the insect gut microbiome to identify genes with plastic-degrading potential is still lacking. RESULTS: In the present work, we aim to fill this gap using Black Soldier Fly (BSF) as insect model. BSF larvae have proven capability to efficiently bioconvert a wide variety of organic wastes but, surprisingly, have never been considered for plastic degradation. BSF larvae were reared on two widely used plastic polymers and shotgun metagenomics was exploited to evaluate if and how plastic-containing diets affect composition and functions of the gut microbial community. The high-definition picture of the BSF gut microbiome gave access for the first time to the genomes of culturable and unculturable microorganisms in the gut of insects reared on plastics and revealed that (i) plastics significantly shaped bacterial composition at species and strain level, and (ii) functions that trigger the degradation of the polymer chains, i.e., DyP-type peroxidases, multicopper oxidases, and alkane monooxygenases, were highly enriched in the metagenomes upon exposure to plastics, consistently with the evidences obtained by scanning electron microscopy and (1)H nuclear magnetic resonance analyses on plastics. CONCLUSIONS: In addition to highlighting that the astonishing plasticity of the microbiota composition of BSF larvae is associated with functional shifts in the insect microbiome, the present work sets the stage for exploiting BSF larvae as “bioincubators” to isolate microbial strains and enzymes for the development of innovative plastic biodegradation strategies. However, most importantly, the larvae constitute a source of enzymes to be evolved and valorized by pioneering synthetic biology approaches. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40168-023-01649-0. BioMed Central 2023-09-14 /pmc/articles/PMC10500907/ /pubmed/37705113 http://dx.doi.org/10.1186/s40168-023-01649-0 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This 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
De Filippis, Francesca
Bonelli, Marco
Bruno, Daniele
Sequino, Giuseppina
Montali, Aurora
Reguzzoni, Marcella
Pasolli, Edoardo
Savy, Davide
Cangemi, Silvana
Cozzolino, Vincenza
Tettamanti, Gianluca
Ercolini, Danilo
Casartelli, Morena
Caccia, Silvia
Plastics shape the black soldier fly larvae gut microbiome and select for biodegrading functions
title Plastics shape the black soldier fly larvae gut microbiome and select for biodegrading functions
title_full Plastics shape the black soldier fly larvae gut microbiome and select for biodegrading functions
title_fullStr Plastics shape the black soldier fly larvae gut microbiome and select for biodegrading functions
title_full_unstemmed Plastics shape the black soldier fly larvae gut microbiome and select for biodegrading functions
title_short Plastics shape the black soldier fly larvae gut microbiome and select for biodegrading functions
title_sort plastics shape the black soldier fly larvae gut microbiome and select for biodegrading functions
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10500907/
https://www.ncbi.nlm.nih.gov/pubmed/37705113
http://dx.doi.org/10.1186/s40168-023-01649-0
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