Cargando…

Transcriptomic characterization of Caecomyces churrovis: a novel, non-rhizoid-forming lignocellulolytic anaerobic fungus

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 wit...

Descripción completa

Detalles Bibliográficos
Autores principales: Henske, John K., Gilmore, Sean P., Knop, Doriv, Cunningham, Francis J., Sexton, Jessica A., Smallwood, Chuck R., Shutthanandan, Vaithiyalingam, Evans, James E., Theodorou, Michael K., O’Malley, Michelle A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5737911/
https://www.ncbi.nlm.nih.gov/pubmed/29270219
http://dx.doi.org/10.1186/s13068-017-0997-4
_version_ 1783287596955205632
author Henske, John K.
Gilmore, Sean P.
Knop, Doriv
Cunningham, Francis J.
Sexton, Jessica A.
Smallwood, Chuck R.
Shutthanandan, Vaithiyalingam
Evans, James E.
Theodorou, Michael K.
O’Malley, Michelle A.
author_facet Henske, John K.
Gilmore, Sean P.
Knop, Doriv
Cunningham, Francis J.
Sexton, Jessica A.
Smallwood, Chuck R.
Shutthanandan, Vaithiyalingam
Evans, James E.
Theodorou, Michael K.
O’Malley, Michelle A.
author_sort Henske, John K.
collection PubMed
description 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. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s13068-017-0997-4) contains supplementary material, which is available to authorized users.
format Online
Article
Text
id pubmed-5737911
institution National Center for Biotechnology Information
language English
publishDate 2017
publisher BioMed Central
record_format MEDLINE/PubMed
spelling pubmed-57379112017-12-21 Transcriptomic characterization of Caecomyces churrovis: a novel, non-rhizoid-forming lignocellulolytic anaerobic fungus Henske, John K. Gilmore, Sean P. Knop, Doriv Cunningham, Francis J. Sexton, Jessica A. Smallwood, Chuck R. Shutthanandan, Vaithiyalingam Evans, James E. Theodorou, Michael K. O’Malley, Michelle A. Biotechnol Biofuels Research 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. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s13068-017-0997-4) contains supplementary material, which is available to authorized users. BioMed Central 2017-12-20 /pmc/articles/PMC5737911/ /pubmed/29270219 http://dx.doi.org/10.1186/s13068-017-0997-4 Text en © The Author(s) 2017 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research
Henske, John K.
Gilmore, Sean P.
Knop, Doriv
Cunningham, Francis J.
Sexton, Jessica A.
Smallwood, Chuck R.
Shutthanandan, Vaithiyalingam
Evans, James E.
Theodorou, Michael K.
O’Malley, Michelle A.
Transcriptomic characterization of Caecomyces churrovis: a novel, non-rhizoid-forming lignocellulolytic anaerobic fungus
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 Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5737911/
https://www.ncbi.nlm.nih.gov/pubmed/29270219
http://dx.doi.org/10.1186/s13068-017-0997-4
work_keys_str_mv AT henskejohnk transcriptomiccharacterizationofcaecomyceschurrovisanovelnonrhizoidforminglignocellulolyticanaerobicfungus
AT gilmoreseanp transcriptomiccharacterizationofcaecomyceschurrovisanovelnonrhizoidforminglignocellulolyticanaerobicfungus
AT knopdoriv transcriptomiccharacterizationofcaecomyceschurrovisanovelnonrhizoidforminglignocellulolyticanaerobicfungus
AT cunninghamfrancisj transcriptomiccharacterizationofcaecomyceschurrovisanovelnonrhizoidforminglignocellulolyticanaerobicfungus
AT sextonjessicaa transcriptomiccharacterizationofcaecomyceschurrovisanovelnonrhizoidforminglignocellulolyticanaerobicfungus
AT smallwoodchuckr transcriptomiccharacterizationofcaecomyceschurrovisanovelnonrhizoidforminglignocellulolyticanaerobicfungus
AT shutthanandanvaithiyalingam transcriptomiccharacterizationofcaecomyceschurrovisanovelnonrhizoidforminglignocellulolyticanaerobicfungus
AT evansjamese transcriptomiccharacterizationofcaecomyceschurrovisanovelnonrhizoidforminglignocellulolyticanaerobicfungus
AT theodoroumichaelk transcriptomiccharacterizationofcaecomyceschurrovisanovelnonrhizoidforminglignocellulolyticanaerobicfungus
AT omalleymichellea transcriptomiccharacterizationofcaecomyceschurrovisanovelnonrhizoidforminglignocellulolyticanaerobicfungus