Elucidating wood decomposition by four species of Ganoderma from the United States

Highlights

• Strategies of decomposition by Ganoderma shows diverse patterns of attack.

• Understanding decay caused by Ganoderma provides new knowledge about white rot degradation.

• Ganoderma zonatum, unlike other Ganoderma species, can penetrate secondary cell walls causing cavities.

• Water-soluble wood extracts of different wood types affect Ganoderma species growth rates differently.

• In vitro growth rate of Ganoderma spp. is not always proportional to decay rate.

Abstract

The laccate (shiny or varnished) Ganoderma contain fungi that are important wood decay fungi of living trees and decomposers of woody debris. They are also an important group of fungi for their degradative enzymes and bioprocessing potential. Laboratory decay microcosms (LDMs) were used to study the relative decay ability of G anoderma curtisii, Ganoderma meredithiae, Ganoderma sessile, and G anoderma zonatum, which are four commonly encountered Ganoderma species in the U.S., across four wood types (Pinus taeda, Quercus nigra, Q uercus virginiana, and Sabal palmetto). Generally, all Ganoderma species were able to decay all types of wood tested despite not being associated with only certain wood types in nature. G. sessile, on average caused the most decay across all wood types. Among the wood types tested, water oak (Q. nigra) had the most mass loss by all species of Ganoderma. Scanning electron microscopy was used to assess micromorphological decay patterns across all treatments. All Ganoderma species simultaneously decayed wood cells of all wood types demonstrating their ability to attack all cell wall components. However, G. zonatum caused selective delignification in some sclerenchyma fibers of the vascular bundles in palm (S. palmetto) as well as in fibers of water oak. In addition, G. zonatum hyphae penetrated fibers of palm and oak wood causing an unusual decay not often observed in basidiomycetes resulting in cavity formation in secondary walls. Cavities within the secondary walls of fibers gradually expanded and coalesced resulting in degradation of the S2 layer. Differences in colony growth rates were observed when Ganoderma species were grown on medium amended with water soluble sapwood extracts from each wood type. G. meredithiae had enhanced growth on all media amended with sapwood extracts, while G. curtisii, G. sessile and G. zonatum had slower growth on loblolly pine extract amended medium.

Introduction

Ganoderma Karst. is a large and diverse genus of wood decay fungi that contains species that cause white rot of the roots and lower trunk of trees belonging to many plant families (Murrill, 1902, Murrill, 1908, Schwarze and Ferner, 2003, Zhou et al., 2015). White rot fungi possess enzymatic and non-enzymatic processes that breakdown cellulose, lignin and other structural components of wood and may degrade these components simultaneously or may selectively attack some cell wall components (such as lignin and hemicellulose) over cellulose (Blanchette, 1984a, Blanchette, 1984b, Blanchette, 1991, Eriksson et al., 2012). Interspecific variation in wood decay rates exists within the genus Ganoderma and in vitro decay rates are proportional to the in vitro growth rates of isolates of a given species in axenic culture (Blanchette, 1984b, Adaskaveg and Gilbertson, 1986a, Adaskaveg et al., 1991). For example, isolates that were identified as G anoderma lucidum (sensu lato) caused approximately 20 and 45 % more mass loss in grape and silver leaf oak wood blocks, respectively, relative to isolates of G anoderma tsugae Murrill over a 20 week period of incubation, and the isolates G. lucidum grew 2–3 times as fast as isolates of G. tsugae in culture (Adaskaveg and Gilbertson, 1986a). Some wood decay fungi selectively degrade lignin, while others simultaneously decay all structural wood sugars (Blanchette, 1991). In vitro decay studies have shown that some Ganoderma species, such as G anoderma oregonense and G. tsugae, selectively delignified and simultaneously decayed wood cells, while others, such as G anoderma meredithiae simultaneously decayed cells with only localized areas of moderate delignification (Blanchette, 1984a, Blanchette, 1991, Adaskaveg et al., 1990). In addition, G anoderma zonatum mostly simultaneously decayed wood cells, but also delignified localized areas of some cell walls (Adaskaveg et al., 1990).

The taxonomy of Ganoderma species in North America is problematic and currently under study. In North America, many laccate (varnished) individuals that occur on hardwoods have been labeled historically as G. lucidum sensu lato (Atkinson, 1908, Adaskaveg and Gilbertson, 1986a, Adaskaveg and Gilbertson, 1986b, Adaskaveg and Gilbertson, 1989, Gilbertson and Ryvarden, 1986, Moncalvo et al., 1995). Molecular phylogenetic investigations now show that G. lucidum sensu stricto (Curtis) Karst. is found native to Europe and possibly parts of Asia (Nobles, 1965, Zhou et al., 2015, Hennicke et al., 2016). In addition, species such as G anoderma curtisii (Berk.) Muriill and G anoderma sessile Murrill, which were once lumped into G. lucidum sensu lato, have been shown to be quite distinct from each other and neither are conspecific with members of the G. lucidum s.s. clade, which includes the temperate North American species G. oregonense Murrill and G. tsugae Murrill (Adaskaveg and Gilbertson, 1988, Zhou et al., 2015).

In addition to differences in the decay ability of various white rot fungi, tree species can differ in their chemical characteristics and physical resistance to decay (Scheffer and Cowling, 1966, Adaskaveg and Gilbertson, 1986a, Adaskaveg et al., 1991, Baietto and Wilson, 2010). Living trees can actively compartmentalize infections and wounds, but the efficiency of this defense strategy can be different between tree species (Shigo and Hillis, 1973, Boddy and Rayner, 1983). In addition, defense chemicals such as resins, phenols, and tannins can be produced in wood, especially after damage to the living sapwood, which can impede the growth of many decay fungi (Scheffer and Cowling, 1966). Pines produce resins and antimicrobial chemicals such as pinosylvins and monomethyl ethers, following wounds, insect attacks or desiccation of wood (Jorgensen, 1961). Oak trees produce phenolic compounds in sapwood following colonization by fungi or insects, wounding of cambium, and possibly desiccation, and it there are differences in decay resistance across different oak species (Shigo, 1985, Scheffer and Morrell, 1998, Deflorio et al., 2008). Since heartwood has little active response growth, relative to sapwood, antimicrobial chemicals are deposited in wood cells naturally, when sapwood dies and forms heartwood (Schwarze et al., 2013). In many types of trees the heartwood is chemically more resistant than sapwood due to deposited extractives (e.g. phenolic compounds) that are composed of decay resistant chemicals (Schwarze et al., 2013). In a study focusing on decay in living sapwood of trees, true heartwood forming species such as oak and Douglas fir had a higher concentration of phenolic compounds and were more decay resistant, relative to beech and sycamores (Deflorio et al., 2008). Sapwood of conifers is on average more resistant to decay relative to sapwood of hardwood trees (Baietto and Wilson, 2010). Lastly, trees with high wood density such as mesquite, have inherently higher wood decay resistance, likely due to a larger concentration of antimicrobial extractives due to greater surface area of the more dense woods (Scheffer, 1973, Adaskaveg and Gilbertson, 1986a). In a previous study focusing on in vitro relative decay of Ganoderma species, isolates of G. lucidum were incapable of decaying mesquite wood (density = 0.71 g/cm³), while mass loss of approximately 60 % was observed on less dense wood such as grape (0.37 g/cm³) (Adaskaveg and Gilbertson, 1986a) (http://db.worldagroforestry.org).

It is likely that certain Ganoderma species have evolved to have an affinity for certain tree groups. For example, G. zonatum Murrill has only been found in association with the decay of palm wood and G. tsugae is typically associated only with hemlock trees (Blanchette, 1984a, Gilbertson and Ryvarden, 1986, Elliott and Broschat, 2001). In addition, G. meredithiae Adask. & Gilb. was originally described as a unique species distinguishing it from G. curtisii and G. lucidum by having an affinity for pines and growing at a slower rate in culture (Adaskaveg and Gilbertson, 1988). For most taxonomic works, knowledge of host species can be an important diagnostic criterion for identification of some species of Ganoderma (Gilbertson and Ryvarden, 1986).

Due to taxonomic confusion, reevaluations of functional differences between common Ganoderma species are needed to better understand the biology of this cosmopolitan group of wood decay fungi. The major objectives of this research are to i) determine quantitative and qualitative differences in decay between commonly observed Ganoderma species in the United States across multiple wood types, and ii) investigate the role that water-soluble sapwood extracts have on the linear growth rates of Ganoderma species.