Potential of Cometabolic Transformation of Polysaccharides and Lignin in Lignocellulose by Soil Actinobacteria Toma ´s ˇ Ve ˇ trovsky ´ 1 , Kari Timo Steffen 2 , Petr Baldrian 1 * 1 Laboratory of Environmental Microbiology, Institute of Microbiology of the ASCR, v.v.i., Praha, Czech Republic, 2 Department of Applied Chemistry and Microbiology, University of Helsinki, Helsinki, Finland Abstract While it is known that several Actinobacteria produce enzymes that decompose polysaccharides or phenolic compounds in dead plant biomass, the occurrence of these traits in the environment remains largely unclear. The aim of this work was to screen isolated actinobacterial strains to explore their ability to produce extracellular enzymes that participate in the degradation of polysaccharides and their ability to cometabolically transform phenolic compounds of various complexities. Actinobacterial strains were isolated from meadow and forest soils and screened for their ability to grow on lignocellulose. The potential to transform 14 C-labelled phenolic substrates (dehydrogenation polymer (DHP), lignin and catechol) and to produce a range of extracellular, hydrolytic enzymes was investigated in three strains of Streptomyces spp. that possessed high lignocellulose degrading activity. Isolated strains showed high variation in their ability to produce cellulose- and hemicellulose-degrading enzymes and were able to mineralise up to 1.1% and to solubilise up to 4% of poplar lignin and to mineralise up to 11.4% and to solubilise up to 64% of catechol, while only minimal mineralisation of DHP was observed. The results confirm the potential importance of Actinobacteria in lignocellulose degradation, although it is likely that the decomposition of biopolymers is limited to strains that represent only a minor portion of the entire community, while the range of simple, carbon-containing compounds that serve as sources for actinobacterial growth is relatively wide. Citation: Ve ˇ trovsky ´ T, Steffen KT, Baldrian P (2014) Potential of Cometabolic Transformation of Polysaccharides and Lignin in Lignocellulose by Soil Actinobacteria. PLoS ONE 9(2): e89108. doi:10.1371/journal.pone.0089108 Editor: Michael Freitag, Oregon State University, United States of America Received November 22, 2013; Accepted January 18, 2014; Published February 13, 2014 Copyright: ß 2014 Ve ˇtrovsky ´ et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Funding: This work was supported by the Academy of Sciences of the Czech Republic (IAA603020901) and by the research concept of the Institute of Microbiology of the ASCR, v.v.i. (RVO61388971). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. * E-mail: baldrian@biomed.cas.cz Introduction Lignocellulose represents the dominant portion of plant biomass and is thus a key pool of carbon in terrestrial ecosystems. The decomposition of lignocellulose in soil environments, where it originates as aboveground or belowground litter, is thus an essential process of the carbon cycle. Microorganisms represent the key decomposers of lignocellulose in soils and especially fungi are often regarded as major lignocellulose decomposers [1], most likely because their larger, multicellular and often filamentous bodies are better suited for the exploitation of bulky substrates [2]. This potential has led to the evolution of efficient enzymatic systems responsible for the decomposition of biopolymers in several fungi [1,3–5]. The process of lignocellulose decomposition is mediated by extracellular enzymes that target its main components: the polysaccharides cellulose and hemicelluloses and polyphenolic lignin [6]. A wide array of enzymes is necessary for the complete decomposition of lignocellulose. The system for cellulose decom- position typically consists of endocellulases, cellobiohydrolases (exocellulases) and b-glucosidases. The hemicellulolytic system is composed of multiple glycosyl hydrolases that are specific for xylose-, mannose-, arabinose- and galactose-containing polysac- charides; and lignin degradation is mediated by oxidative enzymes, such as oxidases (laccases), peroxidases and auxiliary enzymes, that produce hydrogen peroxide [1,7,8]. Although fungi vary largely in their production of extracellular enzymes, several groups, including saprotrophic wood decompos- ers and cord-forming fungi, that inhabit litter and soil were shown to produce complete arrays of extracellular enzymes that decompose all of the components of lignocellulose [4,9]. Current advances in genome sequencing indicate that the theoretical potential of bacteria to degrade certain components of lignocel- lulose, e.g., cellulose, is relatively widespread [10]; and, for certain taxa, enzymes involved in decomposition were characterised [11]. Moreover, recent reports also show that bacteria may play a significant role in cellulose decomposition in soil environments [12]. However, the composition of bacterial enzymatic systems has not been systematically addressed, and it is difficult to estimate their potential to transform individual lignocellulose components. Actinobacteria seem to be good candidates for efficient lignocel- lulose decomposition, and their filamentous growth may help them access and utilise polymeric substrates [13]. Therefore, the involvement of certain Actinobacteria in the degradation of polysaccharides or phenolic compounds in dead plant biomass is generally accepted [14,15]. This is based on previous reports that suggest the presence of decomposer traits in several actinobacterial taxa. In the case of cellulose, the production of endocellulase by PLOS ONE | www.plosone.org 1 February 2014 | Volume 9 | Issue 2 | e89108