Transcriptomic characterization of Caecomyces churrovis: a novel, non-rhizoid-forming lignocellulolytic anaerobic fungus
Abstract Anaerobic gut fungi are the primary colonizers of plant material in the rumen microbiome, but are poorly studied due to a lack of characterized isolates. While most genera of gut fungi form extensive rhizoidal networks, which likely participate in mechanical disruption of plant cell walls,...
| Main Authors: | , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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BMC
2017-12-01
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| Series: | Biotechnology for Biofuels |
| Subjects: | |
| Online Access: | http://link.springer.com/article/10.1186/s13068-017-0997-4 |
| _version_ | 1818209211503345664 |
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| author | John K. Henske Sean P. Gilmore Doriv Knop Francis J. Cunningham Jessica A. Sexton Chuck R. Smallwood Vaithiyalingam Shutthanandan James E. Evans Michael K. Theodorou Michelle A. O’Malley |
| author_facet | John K. Henske Sean P. Gilmore Doriv Knop Francis J. Cunningham Jessica A. Sexton Chuck R. Smallwood Vaithiyalingam Shutthanandan James E. Evans Michael K. Theodorou Michelle A. O’Malley |
| author_sort | John K. Henske |
| collection | DOAJ |
| description | Abstract Anaerobic gut fungi are the primary colonizers of plant material in the rumen microbiome, but are poorly studied due to a lack of characterized isolates. While most genera of gut fungi form extensive rhizoidal networks, which likely participate in mechanical disruption of plant cell walls, fungi within the Caecomyces genus do not possess these rhizoids. Here, we describe a novel fungal isolate, Caecomyces churrovis, which forms spherical sporangia with a limited rhizoidal network yet secretes a diverse set of carbohydrate active enzymes (CAZymes) for plant cell wall hydrolysis. Despite lacking an extensive rhizoidal system, C. churrovis is capable of growth on fibrous substrates like switchgrass, reed canary grass, and corn stover, although faster growth is observed on soluble sugars. Gut fungi have been shown to use enzyme complexes (fungal cellulosomes) in which CAZymes bind to non-catalytic scaffoldins to improve biomass degradation efficiency. However, transcriptomic analysis and enzyme activity assays reveal that C. churrovis relies more on free enzymes compared to other gut fungal isolates. Only 15% of CAZyme transcripts contain non-catalytic dockerin domains in C. churrovis, compared to 30% in rhizoid-forming fungi. Furthermore, C. churrovis is enriched in GH43 enzymes that provide complementary hemicellulose degrading activities, suggesting that a wider variety of these activities are required to degrade plant biomass in the absence of an extensive fungal rhizoid network. Overall, molecular characterization of a non-rhizoid-forming anaerobic fungus fills a gap in understanding the roles of CAZyme abundance and associated degradation mechanisms during lignocellulose breakdown within the rumen microbiome. |
| first_indexed | 2024-12-12T04:57:06Z |
| format | Article |
| id | doaj.art-f5f62fcb56204de7a060ebda12eb6dff |
| institution | Directory Open Access Journal |
| issn | 1754-6834 |
| language | English |
| last_indexed | 2024-12-12T04:57:06Z |
| publishDate | 2017-12-01 |
| publisher | BMC |
| record_format | Article |
| series | Biotechnology for Biofuels |
| spelling | doaj.art-f5f62fcb56204de7a060ebda12eb6dff2022-12-22T00:37:20ZengBMCBiotechnology for Biofuels1754-68342017-12-0110111210.1186/s13068-017-0997-4Transcriptomic characterization of Caecomyces churrovis: a novel, non-rhizoid-forming lignocellulolytic anaerobic fungusJohn K. Henske0Sean P. Gilmore1Doriv Knop2Francis J. Cunningham3Jessica A. Sexton4Chuck R. Smallwood5Vaithiyalingam Shutthanandan6James E. Evans7Michael K. Theodorou8Michelle A. O’Malley9Department of Chemical Engineering, University of CaliforniaDepartment of Chemical Engineering, University of CaliforniaDepartment of Chemical Engineering, University of CaliforniaDepartment of Chemical Engineering, University of CaliforniaDepartment of Chemical Engineering, University of CaliforniaEnvironmental Molecular Sciences Laboratory, Pacific Northwest National LaboratoryEnvironmental Molecular Sciences Laboratory, Pacific Northwest National LaboratoryEnvironmental Molecular Sciences Laboratory, Pacific Northwest National LaboratoryAgriculture Centre for Sustainable Energy Systems (ACSES), Animal Production, Welfare and Veterinary Sciences, Harper Adams UniversityDepartment of Chemical Engineering, University of CaliforniaAbstract Anaerobic gut fungi are the primary colonizers of plant material in the rumen microbiome, but are poorly studied due to a lack of characterized isolates. While most genera of gut fungi form extensive rhizoidal networks, which likely participate in mechanical disruption of plant cell walls, fungi within the Caecomyces genus do not possess these rhizoids. Here, we describe a novel fungal isolate, Caecomyces churrovis, which forms spherical sporangia with a limited rhizoidal network yet secretes a diverse set of carbohydrate active enzymes (CAZymes) for plant cell wall hydrolysis. Despite lacking an extensive rhizoidal system, C. churrovis is capable of growth on fibrous substrates like switchgrass, reed canary grass, and corn stover, although faster growth is observed on soluble sugars. Gut fungi have been shown to use enzyme complexes (fungal cellulosomes) in which CAZymes bind to non-catalytic scaffoldins to improve biomass degradation efficiency. However, transcriptomic analysis and enzyme activity assays reveal that C. churrovis relies more on free enzymes compared to other gut fungal isolates. Only 15% of CAZyme transcripts contain non-catalytic dockerin domains in C. churrovis, compared to 30% in rhizoid-forming fungi. Furthermore, C. churrovis is enriched in GH43 enzymes that provide complementary hemicellulose degrading activities, suggesting that a wider variety of these activities are required to degrade plant biomass in the absence of an extensive fungal rhizoid network. Overall, molecular characterization of a non-rhizoid-forming anaerobic fungus fills a gap in understanding the roles of CAZyme abundance and associated degradation mechanisms during lignocellulose breakdown within the rumen microbiome.http://link.springer.com/article/10.1186/s13068-017-0997-4Anaerobic fungiNeocallimastigomycotaCellulaseEnzymeCellulosome |
| spellingShingle | John K. Henske Sean P. Gilmore Doriv Knop Francis J. Cunningham Jessica A. Sexton Chuck R. Smallwood Vaithiyalingam Shutthanandan James E. Evans Michael K. Theodorou Michelle A. O’Malley Transcriptomic characterization of Caecomyces churrovis: a novel, non-rhizoid-forming lignocellulolytic anaerobic fungus Biotechnology for Biofuels Anaerobic fungi Neocallimastigomycota Cellulase Enzyme Cellulosome |
| title | Transcriptomic characterization of Caecomyces churrovis: a novel, non-rhizoid-forming lignocellulolytic anaerobic fungus |
| title_full | Transcriptomic characterization of Caecomyces churrovis: a novel, non-rhizoid-forming lignocellulolytic anaerobic fungus |
| title_fullStr | Transcriptomic characterization of Caecomyces churrovis: a novel, non-rhizoid-forming lignocellulolytic anaerobic fungus |
| title_full_unstemmed | Transcriptomic characterization of Caecomyces churrovis: a novel, non-rhizoid-forming lignocellulolytic anaerobic fungus |
| title_short | Transcriptomic characterization of Caecomyces churrovis: a novel, non-rhizoid-forming lignocellulolytic anaerobic fungus |
| title_sort | transcriptomic characterization of caecomyces churrovis a novel non rhizoid forming lignocellulolytic anaerobic fungus |
| topic | Anaerobic fungi Neocallimastigomycota Cellulase Enzyme Cellulosome |
| url | http://link.springer.com/article/10.1186/s13068-017-0997-4 |
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