Abstract
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.
Highlights
Cellulose is the principal component of plant cell walls and the most abundant organic compound in terrestrial ecosystems [1]
The bacterial genus Streptomyces is abundant in soil, appears to readily form symbiotic associations with eukaryotic hosts, and has long been thought to contribute to plant biomass degradation
We show that the ability to rapidly deconstruct cellulose is surprisingly rare in the genus Streptomyces but is enriched in symbiotic stains associated with diverse insect hosts that feed on plant biomass
Summary
Cellulose is the principal component of plant cell walls and the most abundant organic compound in terrestrial ecosystems [1]. While cellulose deconstruction is critical to ecosystem functioning and the global carbon cycle, only select lineages of fungi and bacteria have evolved the ability to efficiently degrade this highly recalcitrant substrate [2,3,4,5,6,7]. These cellulolytic microbes are abundant in the soil and are commonly associated with herbivorous eukaryotes. Understanding the distribution and evolution of cellulolytic activity in ecologically important bacteria connects microbial diversity to ecosystem function and the global carbon cycle and provides a powerful approach to identify enzymes for the production of biofuels and other biocommodities
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