Competitive and Antagonistic Interactions

Basidiomycetes degrading lignocellulose-rich material exude many different extracellular enzymes and small compounds, mediators, which are involved in the degradation of the different polymers. The oligomers released by the extracellular enzymes form the actual growth substrates for the fungi. These oligomers are, however, also appropriate substrates for most wood- and litter-inhabiting bacteria. Hence, whereas the contribution of bacteria to lignocellulose degradation is probably minor, they can profit from the degradation activities of fungi (Figure 1). Obviously, this could create a situation where the fungus is deprived of a large part of its growth substrates. How do lignocellulolytic basidiomycetes deal with this?

Bacteria t

Wood polymers

Extracellular fungal enzymes

_Fungi_

Figure 1 Competition between basidiomycetes and bacteria in decaying wood. The attack of wood polymers is mainly by fungal extracellular enzymes and mediators. The low-molecular weight products (LMW) released by the enzymes are the actual substrates for fungal growth. Bacteria are potentially strong competitors for LMW not for the wood polymers themselves. This situation creates dependency of the bacteria on fungal activity.

It seems that the most obvious strategy is inhibition of surrounding bacteria. Indeed, there are clear indications that such a strategy is employed by several basidiomycetes. The white-rot fungus Pleurotus ostreatus drastically reduces the number of bacterial colony-forming units in both soil and straw (Lang et al., 1997; Gramms et al., 1999). Similar findings have been reported for the fairy ring fungus Marasmius oreades during the degradation of soil organic matter (Smith, 1980). Gramms (1987) reported the killing of the microflora of timber blocks and sawdust around basidiomycete mycelia.

We have examined the effects of two white-rot fungi, Hypholoma fasciculare and Resinicium bicolor, on numbers of bacteria near exploratory hyphae (cords) in soil and on numbers of bacteria inhabiting beech wood blocks (Folman, Boddy and de Boer, unpublished results). Culturable bacteria increased slightly, but significantly, in the vicinity of soil mycelia. In contrast, numbers of culturable wood-inhabiting bacteria and total (detected by microscopy) bacteria were considerably reduced after colonization of the blocks by the rot fungi. The fact that not only numbers of colony-forming units but also total microscopic numbers decreased points at a fungal-induced lysis of wood-inhabiting bacteria. In a follow-up study with H. fasciculare we observed that decrease in numbers of wood-inhabiting bacteria was already apparent only a few weeks after colonization of the wood blocks by the fungus.

Several mechanisms can be involved in the killing of wood-inhabiting bacteria by basidiomycetes. Decay fungi can rapidly decrease the pH of the resources they colonize by exuding organic acids, for example oxalic acid. A rapid drop in pH is likely to be detrimental to many bacteria, in particular when undissociated forms of weak organic acids are present as well (Booth, 1985). These undissociated organic acids cross the bacteria cell membrane passively by diffusion and cause a drop in the intracellular pH of the bacteria. Bacteria have been shown to adapt to low pH, but this is a gradual process (De Boer et al., 1995).

The production of reactive oxygen species, for example hydroxyl radicals, involved in the modification or degradation of lignin may also be harmful to many bacteria. There is some evidence that decay fungi actually inhibit bacteria

LMW products in this process, for example production of hydroxyl radicals by the brown-rot fungus Antrodia vaillantii increased during interaction with the bacterium Pseudomonas fluorescens (Tornberg and Olsson, 2002). Bacteria surviving in wood colonized by decay fungi must have sufficient antioxidative activity to protect themselves from being attacked by free radicals.

Saptrotrophic basidiomycetes are known for their production of secondary metabolites, and these compounds may also play an important role in the inhibition or killing of bacteria (Lorenzen and Anke, 1998; Abraham, 2001; Liu, 2005). It has already been indicated that secondary metabolites can play an important role in the competition between wood-rot fungi (Heilmann-Clausen and Boddy, 2005).

Several basidiomycetes produce organohalogens, including chloroform which is a biocidal compound (Hoekstra et al., 1998; Verhagen et al., 1998). The role of organohalogen production by basidiomycetes is not clear, so far, but it has been suggested that they may also function as mediators in lignin degradation (Oberg et al., 1997). Organohalogens may, however, also suppress competing fungi and bacteria, an aspect that has not yet been examined.

Secondary metabolites may also enhance the competitive position of bacteria against lignocellulolytic basidiomycetes. However, the bacteria are in an incongruous situation as the supply of growth substrates depends on the extracellular enzyme production of the fungus (Figure 1). Hence, strong suppression of the fungus would finally result in starvation of the bacteria. Antagonism of bacteria against fungi appears to be more profitable during the initial stage of wood decay when easily degradable compounds are present. This is a stage where both non-lignocellulolytic fungi and bacteria are present and antagonistic interactions have been indicated (Payne et al., 2000). The bacterial community that develops during this initial decay stage may also inhibit or delay colonization of wood by lignocellulolytic fungi (Greaves, 1970). Hence, for a better understanding of bacterial antagonism against wood-rotting basidiomycetes, it is important to know whether the bacteria are early colonizers of wood or established/maintained during growth and activities of rot fungi.

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