Elucidating wood decomposition by four species of Ganoderma from the United States
Graphical abstract
Wood decay caused by Ganoderma species in the United States. A) scanning electron micrograph (SEM) of non-decayed Quercus nigra wood (control), where “Xv” represent xylem vessels and “P” represent parenchyma cells (bar = 200 μm); B) Scanning electron micrograph of Q. nigra wood degraded by Ganoderma sessile (treatment), where arrows represent simultaneously decayed cells (bar = 100 μm); C) Percent mass loss of different wood types after 90 d of incubation across four Ganoderma species from the U.S. and a control; and D) Average colony area of growth when Ganoderma species were grown on media amended with water-soluble sapwood extracts from four types of wood and 2 % malt extract agar (MEA) as a control.
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.
Section snippets
Isolate collections
Isolates of G. curtisii, G. meredithiae, G. sessile, and G. zonatum were cultured from the sterile context tissue of basidiomata collected in Florida. Cultures were obtained by plating small pieces (<1 cm) of sterile context tissue onto basidiomycete-selective malt extract agar (BSMEA) medium, which was made with a base of malt extract agar (MEA) (Difco Laboratories, Franklin Lakes, NJ) according to the manufacturer's recipe with the addition of streptomycin (100 mg/L), benomyl 95 % (4 mg/L),
Laboratory decay microcosm studies
Differences in decay across fungal–wood combinations were evident after 90 d of incubation in the LDMs. The control wood blocks had the lowest levels of mass loss (0–9 %) compared to all Ganoderma taxa. The mass loss of the control wood blocks can be attributed to changes to wood during preparation (drying, hydrating, autoclaving, etc.). Host species ranked from least to most decay resistant were: water oak, sabal palm, loblolly pine, and live oak (Fig 1). Water oak was the least decay
Discussion
Species of Ganoderma are primary decay fungi that can be found on trees ranging from healthy to dead, and some species are more effective at decaying certain species of trees or types of wood (Hong and Jung, 2004, Sinclair and Lyon, 2005). One possible explanation for a tightly linked host affinity is that certain fungal species have coevolved with certain types of tree species, and have become more efficient at competing with other potential colonizers of a given host. For example, although
Acknowledgements
This project was funded by the F.A. Bartlett Tree Experts company and the International Society of Arboriculture (ISA) Florida Chapter Research Grant, and the authors are greatly appreciative. We are also grateful to Elden LeBrun, Monica Elliott, and Tim Broschat for assistance in preparing wooden blocks for this study.
References (45)
- et al.
Cultural studies of four North American species in the Ganoderma lucidum complex with comparisons to G. lucidum and G. tsugae
Mycol. Res.
(1989) Interspecific combative interactions between wood-decaying basidiomycetes
FEMS Microbiol. Ecol.
(2000)- et al.
Decay development in living sapwood of coniferous and deciduous trees inoculated with six wood decay fungi
For. Ecol. Manag.
(2008) - et al.
Distinguishing commercially grown Ganoderma lucidum from Ganoderma lingzhi from Europe and East Asia on the basis of morphology, molecular phylogeny, and triterpenic acid profiles
Phytochemistry
(2016) - et al.
Gene phylogeny of the Ganoderma lucidum complex based on ribosomal DNA sequences. Comparison with traditional taxonomic characters
Mycol. Res.
(1995) - et al.
Species associations during the succession of wood-inhabiting fungal communities
Fungal Ecol.
(2014) Wood decay under the microscope
Fungal Biol. Rev.
(2007)- et al.
Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics
PCR Protoc. Guide Methods Appl.
(1990) - et al.
Global diversity of the Ganoderma lucidum complex (Ganodermataceae, Polyporales) inferred from morphology and multilocus phylogeny
Phytochemistry
(2015) - et al.
Ganoderma meredithae, a new species on pines in the southeastern United States
Mycotaxon (USA)
(1988)
Comparative studies of delignification caused by Ganoderma species
Appl. Environ. Microbiol.
Decay of date palm wood by white-rot and brown-rot fungi
Can. J. Bot.
In vitro decay studies of selective delignification and simultaneous decay by the white rot fungi Ganoderma lucidum and G. tsugae
Can. J. Bot.
Cultural studies and genetics of sexuality of Ganoderma lucidum and G. tsugae in relation to the taxonomy of the G. lucidum complex
Mycologia
ASTM standard D1413–07
Observations on Polyporus lucidus Leys and some of its Allies from Europe and North America
Bot. Gaz.
Relative in vitro wood decay resistance of sapwood from landscape trees of southern temperate regions
HortScience
Selective delignification of eastern hemlock by Ganoderma tsugae
Phytopathology
Screening wood decayed by white rot fungi for preferential lignin degradation
Appl. Environ. Microbiol.
Delignification by wood-decay fungi
Annu. Rev. Phytopathol.
Resistance of hardwood vessels to degradation by white rot Basidiomycetes
Can. J. Bot.
Origins of decay in living deciduous trees: the role of moisture content and a re-appraisal of the expanded concept of tree decay
New Phytol.
Cited by (27)
Fungal skin for robots
2024, BioSystemsAn assessment of volatile organic compounds pollutant emissions from wood materials: A review
2022, ChemosphereCitation Excerpt :Wood-based composite panels (Villanueva et al., 2018) with various surface finishes are employed in the interior environment. Synthetic polymeric materials such as low-pressure laminate (LPL), polyvinyl chloride (PVC), or polypropylene (Loyd et al., 2018) are employed to manufacture these surface-finished items with a film or coating. Methods for making traditional wooden board items were straightforward.
Fungal symbionts of bark and ambrosia beetles can suppress decomposition of pine sapwood by competing with wood-decay fungi
2020, Fungal EcologyCitation Excerpt :However, the ascomycete beetle-associated fungi (Ophiostoma, Raffaelea, and Ambrosiozyma) caused less than 5% mass loss on average, suggesting that they did not utilize the structural components of the wood but mainly consumed the available labile sugars and extractives. In contrast, F. ambrosius caused mass loss that was comparable to the common free-living white-rot wood-decay fungus G. curtisii (Fig. 1) and similar to previous reports that used similar methods to measure decay from these fungi (Kasson et al., 2016; Loyd et al., 2018b). Flavodon ambrosius was the only beetle-associated fungus to cause detectable structural damage to sapwood.
Non-destructive diagnose of the biodeterioration of heritage assets through an optical microscopy
2020, Journal of Cultural Heritage