Evolution of High Cellulolytic Activity in Symbiotic Streptomyces through Selection of Expanded Gene Content and Coordinated Gene Expression.
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.
DOE Great Lakes Bioenergy Research Center, University of Wisconsin-Madison, Madison, Wisconsin, United States of America.|Department of Bacteriology, University of Wisconsin-Madison, Madison, Wisconsin, United States of America.
Adam J
0000-0001-8713-9213
AJ
Book
DOE Great Lakes Bioenergy Research Center, University of Wisconsin-Madison, Madison, Wisconsin, United States of America.|Department of Bacteriology, University of Wisconsin-Madison, Madison, Wisconsin, United States of America.
Gina R
GR
Lewin
DOE Great Lakes Bioenergy Research Center, University of Wisconsin-Madison, Madison, Wisconsin, United States of America.|Department of Bacteriology, University of Wisconsin-Madison, Madison, Wisconsin, United States of America.
Bradon R
BR
McDonald
DOE Great Lakes Bioenergy Research Center, University of Wisconsin-Madison, Madison, Wisconsin, United States of America.|Department of Biochemistry, University of Wisconsin-Madison, Madison, Wisconsin, United States of America.
Taichi E
TE
Takasuka
DOE Great Lakes Bioenergy Research Center, University of Wisconsin-Madison, Madison, Wisconsin, United States of America.|Department of Bacteriology, University of Wisconsin-Madison, Madison, Wisconsin, United States of America.
Evelyn
E
Wendt-Pienkowski
DOE Great Lakes Bioenergy Research Center, University of Wisconsin-Madison, Madison, Wisconsin, United States of America.|Department of Bacteriology, University of Wisconsin-Madison, Madison, Wisconsin, United States of America.
Drew T
DT
Doering
DOE Great Lakes Bioenergy Research Center, University of Wisconsin-Madison, Madison, Wisconsin, United States of America.|Department of Bacteriology, University of Wisconsin-Madison, Madison, Wisconsin, United States of America.
Steven
0000-0002-0781-4440
S
Suh
Department of Entomology, University of Wisconsin-Madison, Madison, Wisconsin, United States of America.
Kenneth F
KF
Raffa
DOE Great Lakes Bioenergy Research Center, University of Wisconsin-Madison, Madison, Wisconsin, United States of America.|Department of Biochemistry, University of Wisconsin-Madison, Madison, Wisconsin, United States of America.
Brian G
BG
Fox
DOE Great Lakes Bioenergy Research Center, University of Wisconsin-Madison, Madison, Wisconsin, United States of America.|Department of Bacteriology, University of Wisconsin-Madison, Madison, Wisconsin, United States of America.
Cameron R
CR
Currie
D001426:Bacterial Proteins / Q000235:genetics / Q000378:metabolism; D018533:Biomass; D002480:Cellulase / Q000235:genetics / Q000378:metabolism; D002482:Cellulose / Q000378:metabolism*; D019143:Evolution, Molecular; D020869:Gene Expression Profiling / Q000379:methods; D015964:Gene Expression Regulation, Bacterial; D023281:Genomics / Q000379:methods; D006868:Hydrolysis; D010802:Phylogeny; D010944:Plants / Q000378:metabolism / Q000382:microbiology; D012336:RNA, Ribosomal, 16S / Q000235:genetics; D012641:Selection, Genetic; D012988:Soil Microbiology; D013045:Species Specificity; D013302:Streptomyces / Q000145:classification / Q000235:genetics* / Q000378:metabolism; D013559:Symbiosis
D001426:Bacterial Proteins; D012336:RNA, Ribosomal, 16S; D002482:Cellulose; D002480:Cellulase