Polysaccharide Degradation Capability of Actinomycetales Soil Isolates from a Semiarid Grassland of the Colorado Plateau

Among the bacteria, members of the orderActinomycetales are considered quintessential degraders of complex polysaccharides in soils. However, studies examining complex polysaccharide degradation byActinomycetales (other thanStreptomyces spp.) in soils are limited. Here, we examine the lignocellulolytic and chitinolytic potential of 112Actinomycetales strains, encompassing 13 families, isolated from a semiarid grassland of the Colorado Plateau in Utah. Members of theStreptomycetaceae ,Pseudonocardiaceae ,Micromonosporaceae , andPromicromonosporaceae families exhibited robust activity against carboxymethyl cellulose, xylan, chitin, and pectin substrates (except for low/no pectinase activity by theMicromonosporaceae ). When incubated in a hydrated mixture of blendedStipa andHilaria grass biomass over a 5-week period,Streptomyces andSaccharothrix (a member of thePseudonocardiaceae ) isolates produced high levels of extracellular enzyme activity, such as endo- and exocellulase, glucosidase, endo- and exoxylosidase, and arabinofuranosidase. These characteristics make them well suited to degrade the cellulose and hemicellulose components of grass cell walls. On the basis of the polysaccharide degradation profiles of the isolates, relative abundance ofActinomycetales sequences in 16S rRNA gene surveys of Colorado Plateau soils, and analysis of genes coding for polysaccharide-degrading enzymes among 237Actinomycetales genomes in the CAZy database and 5 genomes from our isolates, we posit thatStreptomyces spp. and select members of thePseudonocardiaceae andMicromonosporaceae likely play an important role in the degradation of hemicellulose, cellulose, and chitin substances in dryland soils.IMPORTANCE Shifts in the relative abundance ofActinomycetales taxa have been observed in soil microbial community surveys during large, manipulated climate change field studies. However, our limited understanding of the ecophysiology of diverseActinomycetales taxa in soil systems undermines attempts to determine the underlying causes of the population shifts or their impact on carbon cycling in soil. This study combines a systematic analysis of the polysaccharide degradation potential of a diverse collection ofActinomycetales isolates from surface soils of a semiarid grassland with analysis of genomes from five of these isolates and publicly availableActinomycetales genomes for genes encoding polysaccharide-active enzymes. The results address an important gap in knowledge ofActinomycetales ecophysiology—identification of key taxa capable of facilitating lignocellulose degradation in dryland soils. Information from this study will benefit future metagenomic studies related to carbon cycling in dryland soils by providing a baseline linkage ofActinomycetales phylogeny with lignocellulolytic functional potential.