Comparative and pangenomic analysis of the genus Streptomyces

Abstract

Streptomycetes are highly metabolically gifted bacteria with the abilities to produce bioproducts that have profound economic and societal importance. These bioproducts are produced by metabolic pathways including those for the biosynthesis of secondary metabolites and catabolism of plant biomass constituents. Advancements in genome sequencing technologies have revealed a wealth of untapped metabolic potential from Streptomyces genomes. Here, we report the largest Streptomyces pangenome generated by using 205 complete genomes. Metabolic potentials of the pangenome and individual genomes were analyzed, revealing degrees of conservation of individual metabolic pathways and strains potentially suitable for metabolic engineering. Of them, Streptomyces bingchenggensis was identified as a potent degrader of plant biomass. Polyketide, non-ribosomal peptide, and gamma-butyrolactone biosynthetic enzymes are primarily strain specific while ectoine and some terpene biosynthetic pathways are highly conserved. A large number of transcription factors associated with secondary metabolism are strain-specific while those controlling basic biological processes are highly conserved. Although the majority of genes involved in morphological development are highly conserved, there are strain-specific varieties which may contribute to fine tuning the timing of cellular differentiation. Overall, these results provide insights into the metabolic potential, regulation and physiology of streptomycetes, which will facilitate further exploitation of these important bacteria.

Figure 1

(A) Sources of the 205 streptomycetes used in this study. (B) Phylogenetic tree of the 205 streptomycetes using the 16S rRNA sequences. Sequences were aligned using PhyML. Red boxes indicate S. bingchenggensis BCW-1 and S. viridosporus ATCC 39115. (C) Clusters of the 205 strains based on the similarity of the 25 CAZymes families (see Fig. S3 for further information) and the relative numbers of CAZymes and CAZyme groups encoded in each genome. (D) Completeness of the protocatechuate and catechol catabolic pathways encoded in each genome. The pathway is complete if the genome encoded all the 6 enzymes each pathway requires. S. bingchenggensis BCW-1 and S. viridosporus ATCC 39115 encode the complete β-ketoadipate pathway responsible for protocatechuate and catechol catabolism. S. bingchenggensis BCW-1 also encodes a variety of CAZymes likely to be involved in polysaccharide depolymerization.

Figure 2

(A) Change in the pangenome size as a function of the number of genomes. X axis is the number of genomes used to construct the pangenome and Y axis is the number of orthologous groups identified in the same pangenome. (B) Change in the number of orthologous groups conserved in all the genomes and at least 95% genomes with the varying number of genomes. (C) The total number of proteins in each conservation bin from the Streptomyces pangenome. The bar colours correspond to the scheme indicated in Fig. 3A.

Figure 3

The total number of proteins in each COG (A) and KEGG (B) category and the percentage in each conservation bin.

Figure 4

The total number of proteins in each CAZyme group (A) and antiSMASH BGC type (C) and the percentage in each conservation bin. (B) The total number of CAZymes and CAZyme groups encoded in each genome. The colour codes are the same as those in Fig. 3.

Figure 5

The total number of proteins in each sigma factor group (A) and other transcription factor family (B) and the percentage in each conservation bin. The colour codes are the same as those in Fig. 3.

Figure 6

(A) Conservation of Bld and Whi proteins. (B) The total number of proteins in chaplin family and the percentage in each conservation bin. The colour codes are the same as those in Fig. 3.