Abstract
Lignin and its degradation, particularly in forest ecosystems, play a major role in the global carbon cycle. Filamentous fungi equipped with extracellular oxidoreductases (oxidative enzymes), i.e., laccase, manganese-dependent peroxidases and several other peroxidases, are the key players in the bioconversion of lignin. In particular, for coarse woody debris (CWD), this process is poorly understood and the activities of laccase and peroxidases have never been studied on a large field scale. We investigated the activities of these enzymes in 701 samples of Fagus sylvatica, Picea abies and Pinus sylvestris CWD across three regions in Germany and analyzed their dependence on pH, water content, wood density, total lignin, organic extractives, metals, water-soluble lignin fragments and fungal species richness. Respective enzyme activities were present in 79 % of all samples, and the activities were highly variable and more frequent in F. sylvatica than in coniferous wood. Logistic regressions and correlations between enzyme activities and the variables revealed that the fungal community structure and the amount of water-soluble lignin fragments are most important determinants, and that the prevalent acidic pH in CWD is suitable to facilitate laccase and manganese peroxidase activities. Concentrations of metals (manganese, copper, iron) were sufficient to ensure synthesis and functioning of relevant enzymes. Based on this large field study, we conclude that laccase and peroxidases in CWD are highly relevant for lignin degradation, but the variable pattern of their secretion is the result of a complex array of wood parameters and the fungal community structure, which could only partly be resolved.
Highlights
The degradation of lignin is of fundamental importance for the global carbon cycle (Dixon et al 1994; Lundell et al 2014; Weedon et al 2009), especially in dead wood that represents globally 5 % of organic carbon in forest ecosystems (FAO 2010)
We investigated the activities of these enzymes in 701 samples of Fagus sylvatica, Picea abies and Pinus sylvestris coarse woody debris (CWD) across three regions in Germany and analyzed their dependence on pH, water content, wood density, total lignin, organic extractives, metals, watersoluble lignin fragments and fungal species richness
By analyzing 701 CDW samples of F. sylvatica, P. abies and P. sylvestris across three regions in Germany, we frequently found activities of extracellular oxidoreductases, i.e., laccase (Lacc), manganese peroxidase (MnP) and several other peroxidases [subsumed under general peroxidase (GenP) and referred to as manganese-independent peroxidases (Morais et al 2002)], which highlights their importance for the chemical modification and decomposition of lignin and for carbon cycling in forests
Summary
The degradation of lignin is of fundamental importance for the global carbon cycle (Dixon et al 1994; Lundell et al 2014; Weedon et al 2009), especially in dead wood that represents globally 5 % of organic carbon in forest ecosystems (FAO 2010). Saprotrophic wood-inhabiting fungi can be classified, as a result of different degradation strategies, by the type of rot they are causing: white rot, brown rot and soft rot (type I and II) (Hatakka and Hammel 2011) All of these fungi are able to utilize and mineralize cellulose and hemicelluloses by different hydrolytic enzymes. Fungal secretory peroxidases can be phylogenetically divided into three large groups: (1) high-redox potential class II peroxidases, i.e., manganese peroxidase (MnP, EC 1.11.1.13), lignin peroxidase (LiP, EC 1.11.1.14), versatile peroxidase (VP, EC 1.11.1.16) and low-redox potential generic peroxidase (GP, EC 1.11.1.7), (2) dye-decolorizing peroxidases (DyP, EC 1.11.1.19) and (3) unspecific peroxygenases (UPO, EC 1.11.2.1) (Hofrichter 2002; Hofrichter and Ullrich 2014; Hofrichter et al 2010) Among these peroxidases, only MnP, LiP and VP were shown to disintegrate polymeric lignin, while DyP and UPO have merely been demonstrated to cleave non-phenolic b-O-4-lignin model dimers (Hofrichter et al 2010), and GP-type enzymes, on contrary, are rather involved in the polymerization of lignin (Kjalke et al 1992). Equipped with varying sets of these oxidative enzymes, WRF reduce the lignin content of dead wood remarkably (Schwarze 2007)
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