Loss of diversity in wood-inhabiting fungal communities affects decomposition activity in Norway spruce wood

ORIGINAL RESEARCH ARTICLE

Front. Microbiol., 20 May 2014 | http://dx.doi.org/10.3389/fmicb.2014.00230

Lara Valentín1,2, Tiina Rajala1, Mikko Peltoniemi1, Jussi Heinonsalo3, Taina Pennanen1 and Raisa Mäkipää1*

• 1Vantaa Research Unit, Finnish Forest Research Institute, Vantaa, Finland
• 2Department of Chemical Engineering, Technical School of Engineering, Universitat Autònoma de Barcelona, Barcelona, Spain
• 3Department of Food and Environmental Sciences, University of Helsinki, Helsinki, Finland

Hundreds of wood-inhabiting fungal species are now threatened, principally due to a lack of dead wood in intensively managed forests, but the consequences of reduced fungal diversity on ecosystem functioning are not known. Several experiments have shown that primary productivity is negatively affected by a loss of species, but the effects of microbial diversity on decomposition are less studied. We studied the relationship between fungal diversity and the in vitro decomposition rate of slightly, moderately and heavily decayed Picea abies wood with indigenous fungal communities that were diluted to examine the influence of diversity. Respiration rate, wood-degrading hydrolytic enzymes and fungal community structure were assessed during a 16-week incubation. The number of observed OTUs in DGGE was used as a measure of fungal diversity. Respiration rate increased between early- and late-decay stages. Reduced fungal diversity was associated with lower respiration rates during intermediate stages of decay, but no effects were detected at later stages. The activity of hydrolytic enzymes varied among decay stages and fungal dilutions. Our results suggest that functioning of highly diverse communities of the late-decay stage were more resistant to the loss of diversity than less diverse communities of early decomposers. This indicates the accumulation of functional redundancy during the succession of the fungal community in decomposing substrates.

Introduction

The loss of species diversity alters ecosystem function, stability and the ability to provide goods and services to society (Loreau et al., 2001; Hooper et al., 2005; Wertz et al., 2006; Cardinale et al., 2012). Several experiments have shown that primary productivity is negatively affected by a loss of plant species (Loreau et al., 2001; Hooper et al., 2012) and ecosystem stability is reduced by decreasing functional diversity (Hooper et al., 2005). Biodiversity affects the rate of key ecosystem processes such as decomposition and nutrient cycling (Loreau et al., 2001; Hättenschwiler et al., 2005; Gessner et al., 2010). In boreal forests, where fungal communities are major decomposers (Rayner and Boddy, 1988; Lindahl and Boberg, 2008; Stenlid et al., 2008), a high diversity of soil fungi can enhance the decomposition rate (Tiunov and Scheu, 2005), especially under environmental fluctuations such as variations in temperature regimes (Toljander et al., 2011). Hundreds of fungal species in Fennoscandian forests are now threatened, principally due to a lack of dead wood in a forest landscape that is intensively managed (Siitonen, 2001). The consequences of reduced fungal diversity on decomposition are unknown. Furthermore, the stability and function of forest ecosystems might be dramatically affected if the fungal capacity to resist habitat perturbation is continuously exceeded, as is the case for many species in managed forests (Stenlid et al., 2008).

Since fungal species produce complementary enzymes, the presence of many species can improve the communities' efficiency to degrade a wide range of litter constituents and thus enhance decomposition rate (Gessner et al., 2010). Experiments with selected fungal species and their combinations revealed a strong positive relationship between fungal diversity and decomposition rate, which became asymptotic at a relatively low level of diversity (Setälä and McLean, 2004; Tiunov and Scheu, 2005). In experiments involving a few species, facilitation and resource partitioning have been observed (Tiunov and Scheu, 2005). In more diverse terrestrial fungal communities, antagonistic mechanisms might prevail (Boddy, 2000; Gessner et al., 2010) and the colonization sequence of wood-degrading fungi can further affect decomposition (Fukami et al., 2010). Studies of the decomposition rate in manipulated fungal communities are mostly performed with a few cultured species, and the results might be a poor reflection of natural communities, especially if certain community members have a greater proportional influence on the decomposition rate than the totality of the fungal community (Robinson et al., 2005).

Decaying Norway spruce logs harbor diverse fungal communities (Ovaskainen et al., 2010; Rajala et al., 2011; Kubartová et al., 2012), where the number of active species is far higher than that considered in experimental studies. Species number tends to increase with mass loss (and related changes in the substrate quality) and peaks in the most decayed logs (Rajala et al., 2012). Decomposition of cell wall polymers in wood is a complex process that is driven by a succession of species with different litter-degrading enzymes (Baldrian, 2008; Stenlid et al., 2008). During the decay process of dead wood over several decades, the fungal decomposer community changes from one dominated by ascomycetes to one of white- and brown-rot basidiomycetes, before slowly becoming one composed mainly by the mycorrhizal species found in the underlying soil (Rajala et al., 2010, 2012). Wood-degrading fungi (white-rot and brown-rot fungi) decompose polysaccharides by producing hydrolases, but only white-rot fungi efficiently degrade lignin via oxidative metalloenzymes (e.g., laccase and manganese peroxidase) (Lundell et al., 2010). Experiments with decomposing leaves and needles have linked enzyme activities (EA) with fungal communities (Šnajdr et al., 2011; Žifèáková et al., 2011), but to our knowledge, no study has yet analyzed such a relationship with the fungal community in decomposing wood. Therefore, we studied wood substrates in different stages of decay to examine the effects of manipulated fungal diversity on enzyme production and decomposition rate during the entire process.

The overall objective of this study was to examine the relationship between fungal diversity and decomposition rate by manipulating fungal communities obtained from decaying Norway spruce wood. We designed a microcosm experiment to investigate: (1) whether a reduced diversity of wood-inhabiting fungi affects the decomposition of Norway spruce wood and, if so, (2) whether functional redundancy and stability of the decomposition process varies among decay stages, and (3) whether changes in fungal diversity and rate of decomposition are related to changes in hydrolytic enzyme production. We tested the hypothesis that CO2 production and enzyme activity in the dead wood are affected by the decay stage of the substrate and diversity of the decomposing species. Furthermore, we hypothetisized that the decomposition activity (measured as CO2 production) is correlated to overall variation of the fungal community and the decomposition increases to direction that is parallel to increasing species diversity (measured as number of detected OTUs).

Materials and Methods

Wood Samples

The study material was collected from an unmanaged forest in Lapinjärvi (Southern Finland, 60°39.413′N, 26°7.352′E, altitude 50 m, temperature sum 1300°C d; further details are provided in Rajala et al., 2012). Wood samples were obtained from stem discs sawn on site from 46 fallen Norway spruce (Picea abies) logs (diameter >5 cm at breast height). Logs were classified as early, intermediate or late stages of decay (I, III, and V according to Mäkinen et al., 2006). Sample discs were sawn in May 2011 and stored in plastic bags at −18°C until processing in the laboratory. The properties of the wood (C/N ratio, lignin content and density) for individual discs were analyzed as described in Rajala et al. (2010) and the mean values of 14 discs from early-decay stages, 12 discs from intermediate-decay stages and 16 discs from late-decay stages were calculated (Table 1).

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