A thready affair: linking fungal diversity and community dynamics to terrestrial decomposition processes

REVIEW ARTICLE A thready affair: linking fungal diversity and community dynamics to terrestrial decomposition processes Annemieke van der Wal1, Thomas D. Geydan1,2, Thomas W. Kuyper2 & Wietse de Boer1,2 1 Department of Microbial Ecology, Netherlands Institute of Ecology, Wageningen, The Netherlands; and 2Department of Soil Quality, Wageningen University, Wageningen, The Netherlands Received 16 April 2012; revised 2 August 2012; accepted 21 August 2012. Final version published online 10 October 2012. DOI: 10.1111/1574-6976.12001 Editor: Steffan Kjellberg MICROBIOLOGY REVIEWS Keywords fungal ecology; carbon cycling; diversity– functioning relationship; niche differentiation; global change; succession. Abstract Filamentous fungi are critical to the decomposition of terrestrial organic matter and, consequently, in the global carbon cycle. In particular, their contribution to degradation of recalcitrant lignocellulose complexes has been widely studied. In this review, we focus on the functioning of terrestrial fungal decomposers and examine the factors that affect their activities and community dynamics. In relation to this, impacts of global warming and increased N deposition are discussed. We also address the contribution of fungal decomposer studies to the development of general community ecological concepts such as diversity– functioning relationships, succession, priority effects and home–field advantage. Finally, we indicate several research directions that will lead to a more complete understanding of the ecological roles of terrestrial decomposer fungi such as their importance in turnover of rhizodeposits, the consequences of interactions with other organisms and niche differentiation. Introduction The kingdom Fungi is a monophyletic eukaryotic lineage consisting of chemo-organotrophic organisms with two distinct growth forms: spherical cells (yeasts) and threadlike structures called hyphae (filamentous fungi). The hyphal growth form is of particular importance in terrestrial ecosystems as it enables exploration of soils via bridging of air-filled gaps (pores) and penetration of solid material (Hoffland et al., 2004; Klein & Paschke, 2004; Money, 2007; Wurzbacher et al., 2010). In addition, hyphae have the ability to translocate nutrients across nutrient-poor patches and to supply growth-limiting elements to zones of metabolic activity (Frey et al., 2000). Fungi have, therefore, been characterized as spatial integrators (Ritz, 2007). The mycelial growth form also facilitates biomass recycling, which further increases efficiency in nutrient use in patchy environments (Boddy, 1999; Falconer et al., 2007). Due to the success of the hyphal growth form in terrestrial environments, fungi have become important components of terrestrial ecosystem FEMS Microbiol Rev 37 (2013) 477–494 functioning (De Boer et al., 2005), especially with respect to the decomposition of organic matter. Decay of organic matter controls the balance between soil carbon storage and CO2 release into the atmosphere, and releases mineral nutrients, which are again made available for plant growth. In this review, we will focus on communities of fungi that play a critical role in decomposition processes. Although the link between fungal ecology and carbon cycling is generally acknowledged, the dynamics and interactions of fungal species during decomposition processes are still not fully understood. Topics that have received increasing attention during the last decade are fungal niche differentiation, the relationship between fungal diversity and decomposition, the role of decomposer fungi in the rhizosphere, the impact of climate changes on functioning of fungal communities, incorporation of fungal factors in decomposition models, effects of fungal species on fungal community composition (priority effects) and the selection of a fungal community composition that is specialized in decomposing the litter of the local plant species or vegetation (home-field advantage). ª 2012 Federation of European Microbiological Societies Published by John Wiley & Sons Ltd. All rights reserved Correspondence: Annemieke van der Wal, Netherlands Institute of Ecology, Droevendaalsesteeg 10, PO Box 50, 6708 PB Wageningen, The Netherlands. Tel.: +31 (0)317 473491; fax: +31 (0)317 473675; e-mail: 478 Developments in these research topics in relation to decomposition processes will be presented and discussed. Phylogenetic diversity of saprotrophic fungi Fungi and the decomposition processes Fungi make a major contribution to terrestrial organic matter decomposition, in particular of the more recalcitrant fractions (Dighton, 2003; De Boer et al., 2006; Berg & McClaugherty, 2008). The ability to decompose these recalcitrant fractions of terrestrial organic matter is based on a combination of morphological characteristics (hyphal growth form) allowing penetration of solid material, and physiological characteristics (extracellular enzymes) allowing degradation of the lignocellulose complex (Money, 2007; Baldrian & Valášková, 2008; Floudas et al., 2012). In particular, the ability to decompose lignin, a heterologous aromatic polymer, appears to be mainly restricted to Basidiomycota (Agaricomycotina) that are known as white-rot fungi (Baldrian, 2008; Floudas et al., 2012), although lignin breakdown has been reported for the Xylariales, within the Ascomycota (Worrall et al., 1997; Osono et al., 2011a, b). In addition, ª 2012 Federation of European Microbiological Societies Published by John Wiley & Sons Ltd. All rights reserved so-called brown-rot fungi have the ability to modify lignin, thereby gaining access to cellulose which together with hemi-cellulose forms the major energy resource for litter- and wood-degrading fungi (Curling et al., 2002; Yelle et al., 2008; Eastwood et al., 2011; Martinez et al., 2011). Cellulolytic ascomycetes, even though they are not able to degrade or modify lignin like white- and brown-rot fungi, can contribute significantly to the decomposition of lignin-rich organic matter, as thin perforation hyphae of these fungi can reach cellulose-rich layers in woody cell walls (Schmidt, 2006). Modification of lignin, as well as decomposition of lignin derivatives, has also been reported for bacteria (Bugg et al., 2011). Such processes may be important for lignin degradation in environments where growth of fungi is restricted, for example, by periodic anoxic conditions (DeAngelis et al., 2011). However, the direct contribution of bacteria to decomposition of natural lignocellulose complexes in terrestrial ecosystems, that is, the attack of these complexes by bacterial enzymes, appears to be minor (Kirby, 2005; Floudas et al., 2012; Schneider et al., 2012). However, bacteria may have an important indirect impact on the decomposition of lignocellulose-rich organic material and formation of humus, namely via metabolizing intermediates released by fungal enzymes or via other interactions with fun (...truncated)