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Metatranscriptome Profiling of a Specialized Microbial Consortium during the Degradation of Nixtamalized Maize Pericarp

Lignocellulose degradation by microbial consortia is multifactorial; hence, it must be analyzed from a holistic perspective. In this study, the temporal transcriptional activity of consortium PM-06, a nixtamalized maize pericarp (NMP) degrader, was determined and related to structural and physicoche...

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Autores principales: Serrano-Gamboa, José Germán, Fócil-Espinosa, Carlos Abraham, Cabello-Yeves, Pedro J., Coutinho, Felipe H., Rojas-Herrera, Rafael Antonio, Sánchez-González, Mónica Noel
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8729791/
https://www.ncbi.nlm.nih.gov/pubmed/34985337
http://dx.doi.org/10.1128/spectrum.02318-21
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author Serrano-Gamboa, José Germán
Fócil-Espinosa, Carlos Abraham
Cabello-Yeves, Pedro J.
Coutinho, Felipe H.
Rojas-Herrera, Rafael Antonio
Sánchez-González, Mónica Noel
author_facet Serrano-Gamboa, José Germán
Fócil-Espinosa, Carlos Abraham
Cabello-Yeves, Pedro J.
Coutinho, Felipe H.
Rojas-Herrera, Rafael Antonio
Sánchez-González, Mónica Noel
author_sort Serrano-Gamboa, José Germán
collection PubMed
description Lignocellulose degradation by microbial consortia is multifactorial; hence, it must be analyzed from a holistic perspective. In this study, the temporal transcriptional activity of consortium PM-06, a nixtamalized maize pericarp (NMP) degrader, was determined and related to structural and physicochemical data to give insights into the mechanism used to degrade this substrate. Transcripts were described in terms of metabolic profile, carbohydrate-active enzyme (CAZyme) annotation, and taxonomic affiliation. The PM-06 gene expression pattern was closely related to the differential rates of degradation. The environmental and physiological conditions preceding high-degradation periods were crucial for CAZyme expression. The onset of degradation preceded the period with the highest degradation rate in the whole process, and in this time, several CAZymes were upregulated. Functional analysis of expressed CAZymes indicated that PM-06 overcomes NMP recalcitrance through modular enzymes operating at the proximity of the insoluble substrate. Increments in the diversity of expressed modular CAZymes occurred in the last stages of degradation where the substrate is more recalcitrant and environmental conditions are stressing. Taxonomic affiliation of CAZyme transcripts indicated that Paenibacillus macerans was fundamental for degradation. This microorganism established synergistic relationships with Bacillus thuringiensis for the degradation of cellulose and hemicellulose and with Microbacterium, Leifsonia, and Nocardia for the saccharification of oligosaccharides. IMPORTANCE Nixtamalized maize pericarp is an abundant residue of the tortilla industry. Consortium PM-06 efficiently degraded this substrate in 192 h. In this work, the temporal transcriptional profile of PM-06 was determined. Findings indicated that differential degradation rates are important sample selection criteria since they were closely related to the expression of carbohydrate-active enzymes (CAZymes). The initial times of degradation were crucial for the consumption of nixtamalized pericarp. A transcriptional profile at the onset of degradation is reported for the first time. Diverse CAZyme genes were rapidly transcribed after inoculation to produce different enzymes that participated in the stage with the highest degradation rate in the whole process. This study provides information about the regulation of gene expression and mechanisms used by PM-06 to overcome recalcitrance. These findings are useful in the design of processes and enzyme cocktails for the degradation of this abundant substrate.
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spelling pubmed-87297912022-01-06 Metatranscriptome Profiling of a Specialized Microbial Consortium during the Degradation of Nixtamalized Maize Pericarp Serrano-Gamboa, José Germán Fócil-Espinosa, Carlos Abraham Cabello-Yeves, Pedro J. Coutinho, Felipe H. Rojas-Herrera, Rafael Antonio Sánchez-González, Mónica Noel Microbiol Spectr Research Article Lignocellulose degradation by microbial consortia is multifactorial; hence, it must be analyzed from a holistic perspective. In this study, the temporal transcriptional activity of consortium PM-06, a nixtamalized maize pericarp (NMP) degrader, was determined and related to structural and physicochemical data to give insights into the mechanism used to degrade this substrate. Transcripts were described in terms of metabolic profile, carbohydrate-active enzyme (CAZyme) annotation, and taxonomic affiliation. The PM-06 gene expression pattern was closely related to the differential rates of degradation. The environmental and physiological conditions preceding high-degradation periods were crucial for CAZyme expression. The onset of degradation preceded the period with the highest degradation rate in the whole process, and in this time, several CAZymes were upregulated. Functional analysis of expressed CAZymes indicated that PM-06 overcomes NMP recalcitrance through modular enzymes operating at the proximity of the insoluble substrate. Increments in the diversity of expressed modular CAZymes occurred in the last stages of degradation where the substrate is more recalcitrant and environmental conditions are stressing. Taxonomic affiliation of CAZyme transcripts indicated that Paenibacillus macerans was fundamental for degradation. This microorganism established synergistic relationships with Bacillus thuringiensis for the degradation of cellulose and hemicellulose and with Microbacterium, Leifsonia, and Nocardia for the saccharification of oligosaccharides. IMPORTANCE Nixtamalized maize pericarp is an abundant residue of the tortilla industry. Consortium PM-06 efficiently degraded this substrate in 192 h. In this work, the temporal transcriptional profile of PM-06 was determined. Findings indicated that differential degradation rates are important sample selection criteria since they were closely related to the expression of carbohydrate-active enzymes (CAZymes). The initial times of degradation were crucial for the consumption of nixtamalized pericarp. A transcriptional profile at the onset of degradation is reported for the first time. Diverse CAZyme genes were rapidly transcribed after inoculation to produce different enzymes that participated in the stage with the highest degradation rate in the whole process. This study provides information about the regulation of gene expression and mechanisms used by PM-06 to overcome recalcitrance. These findings are useful in the design of processes and enzyme cocktails for the degradation of this abundant substrate. American Society for Microbiology 2022-01-05 /pmc/articles/PMC8729791/ /pubmed/34985337 http://dx.doi.org/10.1128/spectrum.02318-21 Text en Copyright © 2022 Serrano-Gamboa et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Serrano-Gamboa, José Germán
Fócil-Espinosa, Carlos Abraham
Cabello-Yeves, Pedro J.
Coutinho, Felipe H.
Rojas-Herrera, Rafael Antonio
Sánchez-González, Mónica Noel
Metatranscriptome Profiling of a Specialized Microbial Consortium during the Degradation of Nixtamalized Maize Pericarp
title Metatranscriptome Profiling of a Specialized Microbial Consortium during the Degradation of Nixtamalized Maize Pericarp
title_full Metatranscriptome Profiling of a Specialized Microbial Consortium during the Degradation of Nixtamalized Maize Pericarp
title_fullStr Metatranscriptome Profiling of a Specialized Microbial Consortium during the Degradation of Nixtamalized Maize Pericarp
title_full_unstemmed Metatranscriptome Profiling of a Specialized Microbial Consortium during the Degradation of Nixtamalized Maize Pericarp
title_short Metatranscriptome Profiling of a Specialized Microbial Consortium during the Degradation of Nixtamalized Maize Pericarp
title_sort metatranscriptome profiling of a specialized microbial consortium during the degradation of nixtamalized maize pericarp
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8729791/
https://www.ncbi.nlm.nih.gov/pubmed/34985337
http://dx.doi.org/10.1128/spectrum.02318-21
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