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

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.

doi:10.1371/journal.pbio.1002475

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

Journal Article · Wed Jun 08 00:00:00 EDT 2016 · PLoS Biology (Online)

DOI:https://doi.org/10.1371/journal.pbio.1002475· OSTI ID:1287326

^[1]; Lewin, Gina R. ^[1]; McDonald, Bradon R. ^[1]; Takasuka, Taichi E. ^[2]; Wendt-Pienkowski, Evelyn ^[1]; Doering, Drew T. ^[1];

^[1]; Raffa, Kenneth F. ^[3]; Fox, Brian G. ^[2]; Currie, Cameron R. ^[1]

Univ. of Wisconsin-Madison, Madison, WI (United States). DOE Great Lakes Bioenergy Research Center and Dept. of Bacteriology
Univ. of Wisconsin-Madison, Madison, WI (United States). DOE Great Lakes Bioenergy Research Center and Dept. of Biochemistry
Univ. of Wisconsin-Madison, Madison, WI (United States). Dept. of Entomology

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.

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Research Organization:: Univ. of Wisconsin, Madison, WI (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: FC02-07ER64494; AC02-05CH11231

OSTI ID:: 1287326

Journal Information:: PLoS Biology (Online), Vol. 14, Issue 6; ISSN 1545-7885

Publisher:: Public Library of ScienceCopyright Statement

Country of Publication:: United States

Language:: English

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