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Title: Evolution of high cellulolytic activity in symbiotic Streptomyces through selection of expanded gene content and coordinated gene expression

Abstract

In this study, the evolution of cellulose degradation was a defining event in the history of life. Without efficient decomposition and recycling, dead plant biomass would quickly accumulate and become inaccessible to terrestrial food webs and the global carbon cycle. On land, the primary drivers of plant biomass deconstruction are fungi and bacteria in the soil or associated with herbivorous eukaryotes. While the ecological importance of plant-decomposing microbes is well established, little is known about the distribution or evolution of cellulolytic activity in any bacterial genus. Here we show that in Streptomyces, a genus of Actinobacteria abundant in soil and symbiotic niches, the ability to rapidly degrade cellulose is largely restricted to two clades of host-associated strains and is not a conserved characteristic of the Streptomyces genus or host-associated strains. Our comparative genomics identify that while plant biomass degrading genes (CAZy) are widespread in Streptomyces, key enzyme families are enriched in highly cellulolytic strains. Transcriptomic analyses demonstrate that cellulolytic strains express a suite of multi-domain CAZy enzymes that are coregulated by the CebR transcriptional regulator. Using targeted gene deletions, we verify the importance of a highly expressed cellulase (GH6 family cellobiohydrolase) and the CebR transcriptional repressor to the cellulolytic phenotype.more » Evolutionary analyses identify complex genomic modifications that drive plant biomass deconstruction in Streptomyces, including acquisition and selective retention of CAZy genes and transcriptional regulators. Our results suggest that host-associated niches have selected some symbiotic Streptomyces for increased cellulose degrading activity and that symbiotic bacteria are a rich biochemical and enzymatic resource for biotechnology.« less

Authors:
ORCiD logo [1];  [1];  [1];  [2];  [1];  [1]; ORCiD logo [1];  [3];  [2];  [1]
  1. Univ. of Wisconsin-Madison, Madison, WI (United States). DOE Great Lakes Bioenergy Research Center and Dept. of Bacteriology
  2. Univ. of Wisconsin-Madison, Madison, WI (United States). DOE Great Lakes Bioenergy Research Center and Dept. of Biochemistry
  3. Univ. of Wisconsin-Madison, Madison, WI (United States). Dept. of Entomology
Publication Date:
Research Org.:
Univ. of Wisconsin-Madison, Madison, WI (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
OSTI Identifier:
1287326
Grant/Contract Number:  
FC02-07ER64494; AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
PLoS biology (Online)
Additional Journal Information:
Journal Name: PLoS biology (Online); Journal Volume: 14; Journal Issue: 6; Journal ID: ISSN 1545-7885
Publisher:
Public Library of Science
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; lytic polysaccharide monooxygenases; multiple sequence alignment; functional-characterization; phylogenetic analysis; transport-system; binding-protein; fungal genomes; reticuli; soil; cellulases; streptomyces; cellulose; plant genomics; evolutionary genetics; gene expression; sequence motif analysis; fungal evolution

Citation Formats

Book, Adam J., Lewin, Gina R., McDonald, Bradon R., Takasuka, Taichi E., Wendt-Pienkowski, Evelyn, Doering, Drew T., Suh, Steven, Raffa, Kenneth F., Fox, Brian G., and Currie, Cameron R. Evolution of high cellulolytic activity in symbiotic Streptomyces through selection of expanded gene content and coordinated gene expression. United States: N. p., 2016. Web. doi:10.1371/journal.pbio.1002475.
Book, Adam J., Lewin, Gina R., McDonald, Bradon R., Takasuka, Taichi E., Wendt-Pienkowski, Evelyn, Doering, Drew T., Suh, Steven, Raffa, Kenneth F., Fox, Brian G., & Currie, Cameron R. Evolution of high cellulolytic activity in symbiotic Streptomyces through selection of expanded gene content and coordinated gene expression. United States. doi:10.1371/journal.pbio.1002475.
Book, Adam J., Lewin, Gina R., McDonald, Bradon R., Takasuka, Taichi E., Wendt-Pienkowski, Evelyn, Doering, Drew T., Suh, Steven, Raffa, Kenneth F., Fox, Brian G., and Currie, Cameron R. Wed . "Evolution of high cellulolytic activity in symbiotic Streptomyces through selection of expanded gene content and coordinated gene expression". United States. doi:10.1371/journal.pbio.1002475. https://www.osti.gov/servlets/purl/1287326.
@article{osti_1287326,
title = {Evolution of high cellulolytic activity in symbiotic Streptomyces through selection of expanded gene content and coordinated gene expression},
author = {Book, Adam J. and Lewin, Gina R. and McDonald, Bradon R. and Takasuka, Taichi E. and Wendt-Pienkowski, Evelyn and Doering, Drew T. and Suh, Steven and Raffa, Kenneth F. and Fox, Brian G. and Currie, Cameron R.},
abstractNote = {In this study, the evolution of cellulose degradation was a defining event in the history of life. Without efficient decomposition and recycling, dead plant biomass would quickly accumulate and become inaccessible to terrestrial food webs and the global carbon cycle. On land, the primary drivers of plant biomass deconstruction are fungi and bacteria in the soil or associated with herbivorous eukaryotes. While the ecological importance of plant-decomposing microbes is well established, little is known about the distribution or evolution of cellulolytic activity in any bacterial genus. Here we show that in Streptomyces, a genus of Actinobacteria abundant in soil and symbiotic niches, the ability to rapidly degrade cellulose is largely restricted to two clades of host-associated strains and is not a conserved characteristic of the Streptomyces genus or host-associated strains. Our comparative genomics identify that while plant biomass degrading genes (CAZy) are widespread in Streptomyces, key enzyme families are enriched in highly cellulolytic strains. Transcriptomic analyses demonstrate that cellulolytic strains express a suite of multi-domain CAZy enzymes that are coregulated by the CebR transcriptional regulator. Using targeted gene deletions, we verify the importance of a highly expressed cellulase (GH6 family cellobiohydrolase) and the CebR transcriptional repressor to the cellulolytic phenotype. Evolutionary analyses identify complex genomic modifications that drive plant biomass deconstruction in Streptomyces, including acquisition and selective retention of CAZy genes and transcriptional regulators. Our results suggest that host-associated niches have selected some symbiotic Streptomyces for increased cellulose degrading activity and that symbiotic bacteria are a rich biochemical and enzymatic resource for biotechnology.},
doi = {10.1371/journal.pbio.1002475},
journal = {PLoS biology (Online)},
number = 6,
volume = 14,
place = {United States},
year = {2016},
month = {6}
}

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    Works referencing / citing this record:

    Streptomyces spp. in the biocatalysis toolbox
    journal, March 2018

    • Spasic, Jelena; Mandic, Mina; Djokic, Lidija
    • Applied Microbiology and Biotechnology, Vol. 102, Issue 8
    • DOI: 10.1007/s00253-018-8884-x

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    • Spasic, Jelena; Mandic, Mina; Djokic, Lidija
    • Applied Microbiology and Biotechnology, Vol. 102, Issue 8
    • DOI: 10.1007/s00253-018-8884-x