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Co‑cultivation of the anaerobic fungus Caecomyces churrovis with Methanobacterium bryantii enhances transcription of carbohydrate binding modules, dockerins, and pyruvate formate lyases on specific substrates

Anaerobic fungi and methanogenic archaea are two classes of microorganisms found in the rumen microbiome that metabolically interact during lignocellulose breakdown. Here, stable synthetic co-cultures of the anaerobic fungus Caecomyces churrovis and the methanogen Methanobacterium bryantii (not nati...

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Autores principales: Brown, Jennifer L., Swift, Candice L., Mondo, Stephen J., Seppala, Susanna, Salamov, Asaf, Singan, Vasanth, Henrissat, Bernard, Drula, Elodie, Henske, John K., Lee, Samantha, LaButti, Kurt, He, Guifen, Yan, Mi, Barry, Kerrie, Grigoriev, Igor V., O’Malley, Michelle A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8665504/
https://www.ncbi.nlm.nih.gov/pubmed/34893091
http://dx.doi.org/10.1186/s13068-021-02083-w
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author Brown, Jennifer L.
Swift, Candice L.
Mondo, Stephen J.
Seppala, Susanna
Salamov, Asaf
Singan, Vasanth
Henrissat, Bernard
Drula, Elodie
Henske, John K.
Lee, Samantha
LaButti, Kurt
He, Guifen
Yan, Mi
Barry, Kerrie
Grigoriev, Igor V.
O’Malley, Michelle A.
author_facet Brown, Jennifer L.
Swift, Candice L.
Mondo, Stephen J.
Seppala, Susanna
Salamov, Asaf
Singan, Vasanth
Henrissat, Bernard
Drula, Elodie
Henske, John K.
Lee, Samantha
LaButti, Kurt
He, Guifen
Yan, Mi
Barry, Kerrie
Grigoriev, Igor V.
O’Malley, Michelle A.
author_sort Brown, Jennifer L.
collection PubMed
description Anaerobic fungi and methanogenic archaea are two classes of microorganisms found in the rumen microbiome that metabolically interact during lignocellulose breakdown. Here, stable synthetic co-cultures of the anaerobic fungus Caecomyces churrovis and the methanogen Methanobacterium bryantii (not native to the rumen) were formed, demonstrating that microbes from different environments can be paired based on metabolic ties. Transcriptional and metabolic changes induced by methanogen co-culture were evaluated in C. churrovis across a variety of substrates to identify mechanisms that impact biomass breakdown and sugar uptake. A high-quality genome of C. churrovis was obtained and annotated, which is the first sequenced genome of a non-rhizoid-forming anaerobic fungus. C. churrovis possess an abundance of CAZymes and carbohydrate binding modules and, in agreement with previous studies of early-diverging fungal lineages, N6-methyldeoxyadenine (6mA) was associated with transcriptionally active genes. Co-culture with the methanogen increased overall transcription of CAZymes, carbohydrate binding modules, and dockerin domains in co-cultures grown on both lignocellulose and cellulose and caused upregulation of genes coding associated enzymatic machinery including carbohydrate binding modules in family 18 and dockerin domains across multiple growth substrates relative to C. churrovis monoculture. Two other fungal strains grown on a reed canary grass substrate in co-culture with the same methanogen also exhibited high log2-fold change values for upregulation of genes encoding carbohydrate binding modules in families 1 and 18. Transcriptional upregulation indicated that co-culture of the C. churrovis strain with a methanogen may enhance pyruvate formate lyase (PFL) function for growth on xylan and fructose and production of bottleneck enzymes in sugar utilization pathways, further supporting the hypothesis that co-culture with a methanogen may enhance certain fungal metabolic functions. Upregulation of CBM18 may play a role in fungal–methanogen physical associations and fungal cell wall development and remodeling. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13068-021-02083-w.
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spelling pubmed-86655042021-12-13 Co‑cultivation of the anaerobic fungus Caecomyces churrovis with Methanobacterium bryantii enhances transcription of carbohydrate binding modules, dockerins, and pyruvate formate lyases on specific substrates Brown, Jennifer L. Swift, Candice L. Mondo, Stephen J. Seppala, Susanna Salamov, Asaf Singan, Vasanth Henrissat, Bernard Drula, Elodie Henske, John K. Lee, Samantha LaButti, Kurt He, Guifen Yan, Mi Barry, Kerrie Grigoriev, Igor V. O’Malley, Michelle A. Biotechnol Biofuels Research Anaerobic fungi and methanogenic archaea are two classes of microorganisms found in the rumen microbiome that metabolically interact during lignocellulose breakdown. Here, stable synthetic co-cultures of the anaerobic fungus Caecomyces churrovis and the methanogen Methanobacterium bryantii (not native to the rumen) were formed, demonstrating that microbes from different environments can be paired based on metabolic ties. Transcriptional and metabolic changes induced by methanogen co-culture were evaluated in C. churrovis across a variety of substrates to identify mechanisms that impact biomass breakdown and sugar uptake. A high-quality genome of C. churrovis was obtained and annotated, which is the first sequenced genome of a non-rhizoid-forming anaerobic fungus. C. churrovis possess an abundance of CAZymes and carbohydrate binding modules and, in agreement with previous studies of early-diverging fungal lineages, N6-methyldeoxyadenine (6mA) was associated with transcriptionally active genes. Co-culture with the methanogen increased overall transcription of CAZymes, carbohydrate binding modules, and dockerin domains in co-cultures grown on both lignocellulose and cellulose and caused upregulation of genes coding associated enzymatic machinery including carbohydrate binding modules in family 18 and dockerin domains across multiple growth substrates relative to C. churrovis monoculture. Two other fungal strains grown on a reed canary grass substrate in co-culture with the same methanogen also exhibited high log2-fold change values for upregulation of genes encoding carbohydrate binding modules in families 1 and 18. Transcriptional upregulation indicated that co-culture of the C. churrovis strain with a methanogen may enhance pyruvate formate lyase (PFL) function for growth on xylan and fructose and production of bottleneck enzymes in sugar utilization pathways, further supporting the hypothesis that co-culture with a methanogen may enhance certain fungal metabolic functions. Upregulation of CBM18 may play a role in fungal–methanogen physical associations and fungal cell wall development and remodeling. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13068-021-02083-w. BioMed Central 2021-12-10 /pmc/articles/PMC8665504/ /pubmed/34893091 http://dx.doi.org/10.1186/s13068-021-02083-w Text en © The Author(s) 2021 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
Brown, Jennifer L.
Swift, Candice L.
Mondo, Stephen J.
Seppala, Susanna
Salamov, Asaf
Singan, Vasanth
Henrissat, Bernard
Drula, Elodie
Henske, John K.
Lee, Samantha
LaButti, Kurt
He, Guifen
Yan, Mi
Barry, Kerrie
Grigoriev, Igor V.
O’Malley, Michelle A.
Co‑cultivation of the anaerobic fungus Caecomyces churrovis with Methanobacterium bryantii enhances transcription of carbohydrate binding modules, dockerins, and pyruvate formate lyases on specific substrates
title Co‑cultivation of the anaerobic fungus Caecomyces churrovis with Methanobacterium bryantii enhances transcription of carbohydrate binding modules, dockerins, and pyruvate formate lyases on specific substrates
title_full Co‑cultivation of the anaerobic fungus Caecomyces churrovis with Methanobacterium bryantii enhances transcription of carbohydrate binding modules, dockerins, and pyruvate formate lyases on specific substrates
title_fullStr Co‑cultivation of the anaerobic fungus Caecomyces churrovis with Methanobacterium bryantii enhances transcription of carbohydrate binding modules, dockerins, and pyruvate formate lyases on specific substrates
title_full_unstemmed Co‑cultivation of the anaerobic fungus Caecomyces churrovis with Methanobacterium bryantii enhances transcription of carbohydrate binding modules, dockerins, and pyruvate formate lyases on specific substrates
title_short Co‑cultivation of the anaerobic fungus Caecomyces churrovis with Methanobacterium bryantii enhances transcription of carbohydrate binding modules, dockerins, and pyruvate formate lyases on specific substrates
title_sort co‑cultivation of the anaerobic fungus caecomyces churrovis with methanobacterium bryantii enhances transcription of carbohydrate binding modules, dockerins, and pyruvate formate lyases on specific substrates
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8665504/
https://www.ncbi.nlm.nih.gov/pubmed/34893091
http://dx.doi.org/10.1186/s13068-021-02083-w
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