An evolutionary signal to fungal succession during plant litter decay.

Sasha Vivelo,Jennifer M Bhatnagar

doi:10.1093/femsec/fiz145

Abstract

ABSTRACTEcologists have frequently observed a pattern of fungal succession during litter decomposition, wherein different fungal taxa dominate different stages of decay in individual ecosystems. However, it is unclear which biological features of fungi give rise to this pattern. We tested a longstanding hypothesis that fungal succession depends on the evolutionary history of species, such that different fungal phyla prefer different decay stages. To test this hypothesis, we performed a meta-analysis across studies in 22 different ecosystem types to synthesize fungal decomposer abundances at early, middle and late stages of plant litter decay. Fungal phyla varied in relative abundance throughout decay, with fungi in the Ascomycota reaching highest relative abundance during early stages of decay (P < 0.001) and fungi in the Zygomycota reaching highest relative abundance during late stages of decay (P < 0.001). The best multiple regression model to explain variation in abundance of these fungal phyla during decay included decay stage, as well as plant litter type and climate factors. Most variation in decay-stage preference of fungal taxa was observed at basal taxonomic levels (phylum and class) rather than finer taxonomic levels (e.g. genus). For many finer-scale taxonomic groups and functional groups of fungi, plant litter type and climate factors were better correlates with relative abundance than decay stage per se, suggesting that the patchiness of fungal community composition in space is related to both resource and climate niches of different fungal taxa. Our study indicates that decomposer fungal succession is partially rooted in fungal decomposers’ deep evolutionary history, traceable to the divergence among phyla.

Highlights

Decomposer fungi cycle up to 36 Gt carbon (C) per year through soils (Talbot 2017), releasing ∼3× more CO2 to the atmosphere annually than human emissions (Lal and Follett 2009; Giardina et al 2014)
We hypothesized that there would be a common taxonomic pattern of fungal succession across ecosystems, and that this pattern would be rooted in the evolutionary history of fungi, where different fungal phyla prefer early vs. late stages of decay across ecosystems
Certain frequently observed genera (Cladosporium, Flagellospora, Pestalotiopsis, Articulospora, Aureobasidium, Lemonniera, Mucor, Umbelopsis and Epicoccum) showed significant decay-stage preferences that remained consistent across multiple biomes (Fig. 4; Table S4, Supporting Information). Some of these patterns parallel those reported in a large literature review of fungal succession (Kjøller and Struwe 2002); for example, we found that Cladosporium and Epicoccum are generally early colonizers, and that Aureobasidium tended to decline in relative abundance after mid decay

Summary

Introduction

Decomposer fungi cycle up to 36 Gt carbon (C) per year through soils (Talbot 2017), releasing ∼3× more CO2 to the atmosphere annually than human emissions (Lal and Follett 2009; Giardina et al 2014). Fungal decomposer communities show patterns of assembly similar to those observed among plant and animal communities (Rayner and Boddy 1988; Lindner et al 2011; Ottosson et al 2014), where different species become dominant at different points in Received: 24 April 2019; Accepted: 5 September 2019 C FEMS 2019. Fungal phyla differ in their inherent growth rates and reproductive strategies; most Ascomycota can reproduce either sexually or asexually and proliferate quickly under favorable circumstances, whereas many Basidiomycota are thought to be obligate sexual reproducers and so may grow more slowly during the decomposition process (Webster and Weber 2007) Such relationships between preferred decay stage and the inherent growth rates of fungi would be consistent with island biogeography theory developed for plants and animals, which suggests that species with high reproduction and growth rates are more likely to establish during the early stages of succession (MacArthur and Wilson 1967; Andrews et al 1987). Other fungal phyla (e.g. lineages in the phyla Zoopagomycota and Mucoromycota) are important decomposers of plant matter (White et al 2006; Mundra et al 2016) and no clear hypothesis has been laid out regarding the decay-stage preference for these lineages

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