Catabolic repression in early-diverging anaerobic fungi is partially mediated by natural antisense transcripts

Solomon, Kevin V.; Henske, John K.; Gilmore, Sean P.; Lipzen, Anna; Grigoriev, Igor V.; Thompson, Dawn; O'Malley, Michelle A.

doi:10.1016/j.fgb.2018.09.004

Title: Catabolic repression in early-diverging anaerobic fungi is partially mediated by natural antisense transcripts

Full Record
Other Related Research

Abstract

Early-diverging anaerobic fungi (order: Neocallimastigomycota), lignocelluolytic chytrid-like fungi central to fiber degradation in the digestive tracts of large herbivores, are attractive sources of cellulases and hemicellulases for biotechnology. Enzyme expression is tightly regulated and coordinated through mechanisms that remain unelucidated to optimize hydrolytic efficiency. Our analysis of anaerobic fungal transcriptomes reveals hundreds of cis-natural antisense transcripts (cis-NATs), which we hypothesize play an integral role in this regulation. Through integrated genomic and transcriptomic sequencing on a range of catabolic substrates, we validate these NATs in three species (Anaeromyces robustus, Neocallimasix californiae, and Piromyces finnis), and analyze their expression patterns and prevalence to gain insight into their function. NAT function was diverse and conserved across the three fungal genomes studied, with 10% of all metabolic process NATs associated with lignocellulose hydrolysis. Despite these similarities, however, only eleven gene targets were conserved orthologs. Several NATs were dynamically regulated by lignocellulosic substrates while their gene targets were unregulated. This observation is consistent with a hypothesized, but untested, regulatory mechanism where selected genes are exclusively regulated at the transcriptional/post-transcriptional level by NATs. However, only genes with high NAT relative expression levels displayed this phenomenon, suggesting a selection mechanism that favors larger dynamic ranges for moremore »« less

Authors:

^[1]; Henske, John K. ^[1]; Gilmore, Sean P. ^[1]; Lipzen, Anna ^[2]; Grigoriev, Igor V. ^[3]; Thompson, Dawn ^[4]; O'Malley, Michelle A. ^[1]

Univ. of California, Santa Barbara, CA (United States). Department of Chemical Engineering
USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States); Univ. of California, Berkeley, CA (United States). Department of Plant and Microbial Biology
Ginkgo Bioworks, Boston, MA (United States)

Publication Date:: Sat Sep 15 00:00:00 EDT 2018

Research Org.:: Univ. of California, Santa Barbara, CA (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Org.:: USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division

OSTI Identifier:: 1485150

Alternate Identifier(s):: OSTI ID: 1619109; OSTI ID: 1636925

Grant/Contract Number:: SC0010352; AC02-05CH11231; AC05-76RL01830

Resource Type:: Accepted Manuscript

Journal Name:: Fungal Genetics and Biology

Additional Journal Information:: Journal Volume: 121; Journal Issue: C; Journal ID: ISSN 1087-1845

Publisher:: Elsevier

Country of Publication:: United States

Language:: English

Subject:: 59 BASIC BIOLOGICAL SCIENCES; Antisense; RNA; Anaerobic fungi; Catabolic regulation

Citation Formats


                    Solomon, Kevin V., Henske, John K., Gilmore, Sean P., Lipzen, Anna, Grigoriev, Igor V., Thompson, Dawn, and O'Malley, Michelle A. Catabolic repression in early-diverging anaerobic fungi is partially mediated by natural antisense transcripts.  United States: N. p., 2018. 
Web.  doi:10.1016/j.fgb.2018.09.004.

Copy to clipboard


                    Solomon, Kevin V., Henske, John K., Gilmore, Sean P., Lipzen, Anna, Grigoriev, Igor V., Thompson, Dawn, & O'Malley, Michelle A. Catabolic repression in early-diverging anaerobic fungi is partially mediated by natural antisense transcripts.  United States.  https://doi.org/10.1016/j.fgb.2018.09.004

Copy to clipboard


                    Solomon, Kevin V., Henske, John K., Gilmore, Sean P., Lipzen, Anna, Grigoriev, Igor V., Thompson, Dawn, and O'Malley, Michelle A. Sat .  
"Catabolic repression in early-diverging anaerobic fungi is partially mediated by natural antisense transcripts".  United States.  https://doi.org/10.1016/j.fgb.2018.09.004.  https://www.osti.gov/servlets/purl/1485150.

Copy to clipboard


                    
@article{osti_1485150,

  title        = {Catabolic repression in early-diverging anaerobic fungi is partially mediated by natural antisense transcripts},

  author       = {Solomon, Kevin V. and Henske, John K. and Gilmore, Sean P. and Lipzen, Anna and Grigoriev, Igor V. and Thompson, Dawn and O'Malley, Michelle A.},

  abstractNote = {Early-diverging anaerobic fungi (order: Neocallimastigomycota), lignocelluolytic chytrid-like fungi central to fiber degradation in the digestive tracts of large herbivores, are attractive sources of cellulases and hemicellulases for biotechnology. Enzyme expression is tightly regulated and coordinated through mechanisms that remain unelucidated to optimize hydrolytic efficiency. Our analysis of anaerobic fungal transcriptomes reveals hundreds of cis-natural antisense transcripts (cis-NATs), which we hypothesize play an integral role in this regulation. Through integrated genomic and transcriptomic sequencing on a range of catabolic substrates, we validate these NATs in three species (Anaeromyces robustus, Neocallimasix californiae, and Piromyces finnis), and analyze their expression patterns and prevalence to gain insight into their function. NAT function was diverse and conserved across the three fungal genomes studied, with 10% of all metabolic process NATs associated with lignocellulose hydrolysis. Despite these similarities, however, only eleven gene targets were conserved orthologs. Several NATs were dynamically regulated by lignocellulosic substrates while their gene targets were unregulated. This observation is consistent with a hypothesized, but untested, regulatory mechanism where selected genes are exclusively regulated at the transcriptional/post-transcriptional level by NATs. However, only genes with high NAT relative expression levels displayed this phenomenon, suggesting a selection mechanism that favors larger dynamic ranges for more precise control of gene expression. In addition to this mode, we observed two other possible regulatory fates: canonical transcriptional regulation with no NAT response, and positive co-regulation of target mRNA and cognate NAT, which we hypothesize is a fine-tuning strategy to locally negate control outputs from global regulators. Our work reveals the complex contributions of antisense RNA to the catabolic response in anaerobic fungi, highlighting its importance in understanding lignocellulolytic activity for bioenergy applications. More importantly, the relative expression of NAT to target may form a critical determinant of transcriptional vs post-transcriptional (NAT) control of gene expression in primitive anaerobic fungi.},

  doi          = {10.1016/j.fgb.2018.09.004},

  journal      = {Fungal Genetics and Biology},

  number       = C,

  volume       = 121,

  place        = {United States},

  year         = {Sat Sep 15 00:00:00 EDT 2018},

  month        = {Sat Sep 15 00:00:00 EDT 2018}

}

Copy to clipboard

Journal Article:

Free Publicly Available Full Text

Accepted Manuscript (Publisher)

Accepted Manuscript (DOE)

Publisher's Version of Record

https://doi.org/10.1016/j.fgb.2018.09.004

Other availability

Search WorldCat to find libraries that may hold this journal

Citation Metrics:

Cited by: 6 works

Citation information provided by
Web of Science

Save / Share:

Export Metadata

Save to My Library

Similar Records in DOE PAGES and OSTI.GOV collections:

Gene Regulation Shifts Shed Light on Fungal Adaption in Plant Biomass Decomposers

Journal Article Zhang, Jiwei ; Silverstein, Kevin A. T. ; Castaño, Jesus David ; ... - mBio (Online)

ABSTRACT Fungi dominate the recycling of carbon sequestered in woody biomass. This process of organic turnover was first evolved among “white rot” fungi that degrade lignin to access carbohydrates and later evolved multiple times toward more efficient strategies to selectively target carbohydrates—“brown rot.” The brown rot adaption was often explained by mechanisms to deploy reactive oxygen species (ROS) to oxidatively attack wood structures. However, its genetic basis remains unclear, especially in the context of gene contractions of conventional carbohydrate-active enzymes (CAZYs) relative to white rot ancestors. Here, we hypothesized that these apparent gains in brown rot efficiency despite gene lossesmore »« less
Cited by 41
https://doi.org/10.1128/mBio.02176-19
A parts list for fungal cellulosomes revealed by comparative genomics

Journal Article Haitjema, Charles H. ; Gilmore, Sean P. ; Henske, John K. ; ... - Nature Microbiology

Cellulosomes are large, multi-protein complexes that tether plant biomass degrading enzymes together for improved hydrolysis1. These complexes were first described in anaerobic bacteria where species specific dockerin domains mediate assembly of enzymes onto complementary cohesin motifs interspersed within non-catalytic protein scaffolds1. The versatile protein assembly mechanism conferred by the bacterial cohesin-dockerin interaction is now a standard design principle for synthetic protein-scale pathways2,3. For decades, analogous structures have been reported in the early branching anaerobic fungi, which are known to assemble by sequence divergent non-catalytic dockerin domains (NCDD)4. However, the enzyme components, modular assembly mechanism, and functional role of fungal cellulosomesmore »« less
https://doi.org/10.1038/nmicrobiol.2017.87
A parts list for fungal cellulosomes revealed by comparative genomics

Journal Article Haitjema, Charles H. ; Gilmore, Sean P. ; Henske, John K. ; ... - Nature Microbiology

Cellulosomes are large, multiprotein complexes that tether plant biomass-degrading enzymes together for improved hydrolysis1. These complexes were first described in anaerobic bacteria, where species-specific dockerin domains mediate the assembly of enzymes onto cohesin motifs interspersed within protein scaffolds1. The versatile protein assembly mechanism conferred by the bacterial cohesin-dockerin interaction is now a standard design principle for synthetic biology2,3. For decades, analogous structures have been reported in anaerobic fungi, which are known to assemble by sequence-divergent non-catalytic dockerin domains (NCDDs)4. However, the components, modular assembly mechanism and functional role of fungal cellulosomes remain unknown5,6. Here, we describe a comprehensive set ofmore »« less
Cited by 114
https://doi.org/10.1038/nmicrobiol.2017.87

Full Text Available
Engineering Anaerobic Gut Fungi for Lignocellulose Breakdown

Technical Report O'Malley, Michelle Ann

Biofuels derived from plant biomass (lignocellulose) are attractive alternatives to petroleum-based products, as they avoid many of the economic and environmental problems that plague traditional energy sources. Breakdown of plant waste into simple sugars would translate into the production of renewable fuels via microbial fermentation. However, existing technologies are insufficient to allow for industrial-scale production of these products due to difficulties associated with the recalcitrance of crude lignin-rich biomass, and the high cost/poor performance of known cellulolytic enzymes (cellulases). Therefore, there is a critical need to develop new technologies to break down lignocellulosic biomass into fermentable sugars for downstream fuelmore »« less
https://doi.org/10.2172/1485149

Full Text Available
A Genomic Catalog of Stress Response Genes in Anaerobic Fungi for Applications in Bioproduction

Journal Article Swift, Candice L. ; Malinov, Nikola G. ; Mondo, Stephen J. ; ... - Frontiers in Fungal Biology

Anaerobic fungi are a potential biotechnology platform to produce biomass-degrading enzymes. Unlike model fungi such as yeasts, stress responses that are relevant during bioprocessing have not yet been established for anaerobic fungi. In this work, we characterize both the heat shock and unfolded protein responses of four strains of anaerobic fungi ( Anaeromyces robustus, Caecomyces churrovis, Neocallimastix californiae , and Piromyces finnis ). The inositol-requiring 1 (Ire1) stress sensor, which typically initiates the fungal UPR, was conserved in all four genomes. However, these genomes also encode putative transmembrane kinases with catalytic domains that are similar to the metazoan stress-sensing enzymemore »« less
https://doi.org/10.3389/ffunb.2021.708358

Similar Records