Evolution of High Cellulolytic Activity in Symbiotic Streptomyces through Selection of Expanded Gene Content and Coordinated Gene Expression

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.

Long-Term Warming Alters Carbohydrate Degradation Potential in Temperate Forest Soils

“…These include spatial and temporal heterogeneity in substrate availability and community structure (88), seasonal differences in transcriptional response (89), expression of isoenzymes and/or uptake transporters with different K m / V max tradeoffs (2), gene-gene interactions (90), and interactions between substrate quality, quantity, and microbial physiology (24). Furthermore, metagenomics is liable to access the genomes of both active and inactive, living and dead cells (91).…”

Evolution and Ecology ofActinobacteriaand Their Bioenergy Applications

“…Subsequently, a variety of Streptomyces strains isolated from soil have been shown to grow on cellulose (16, 120, 144), hemicellulose (45, 61), and potentially even lignin (34, 163) (Figure 2 b ). However, the majority of strains tested cannot grow on crystalline cellulose or hemicellulose, suggesting that most Streptomyces species in the soil only use the breakdown products of plant cell wall polymers (18). Other genera of Actinobacteria have also been implicated in plant biomass degradation in the soil, including Cellulomonas , Nocardia , and Micromonospora , again on the basis of their high prevalence in soil and the ability of some isolates to grow on plant biomass-derived substrates (57, 90, 163).…”

Antimicrobial Activity of Actinobacteria Isolated From the Guts of Subterranean Termites

“…Clustering observed in phylogenetic analysis with other insect-associated Actinobacteria, however, may suggest a more permanent association between Actinobacteria and the termite gut. Book et al (2016) identified a number of Streptomyces clades dominated by host-associated strains. Genetic similarity of Actinobacteria isolated in this study with bacteria from these host-associated lineages may be supportive of a more stable association.…”