Top-down control of soil fungal community composition by a globally distributed keystone consumer.

The relative contribution of top-down and bottom-up processes regulating primary decomposers can influence the strength of the link between the soil animal community and ecosystem functioning. Although soil bacterial communities are regulated by bottom-up and top-down processes, the latter are considered to be less important in structuring the diversity and functioning of fungal-dominated ecosystems. Despite the huge diversity of mycophagous (fungal-feeding) soil fauna, and their potential to reverse the outcomes of competitive fungal interactions, top-down grazing effects have never been found to translate to community-level changes. We constructed soil mesocosms to investigate the potential of isopods grazing on cord-forming basidiomycete fungi to influence the community composition and functioning of a complex woodland soil microbial community. Using metagenomic sequencing we provide conclusive evidence of direct top-down control at the community scale in fungal-dominated woodland soil. By suppressing the dominant cord-forming basidiomycete fungi, isopods prevented the competitive exclusion of surrounding litter fungi, increasing diversity in a community containing several hundred fungal species. This isopod-induced modification of community composition drove a shift in the soil enzyme profile, and led to a restructuring of the wider mycophagous invertebrate community. We highlight characteristics of different soil ecosystems that will give rise to such top-down control. Given the ubiquity of isopods and basidiomycete fungi in temperate and boreal woodland ecosystems, such top-down community control could be of widespread significance for global carbon and nutrient cycling.

[1]  S. Scheu,et al.  Biodiversity and Litter Decomposition in Terrestrial Ecosystems , 2005 .

[2]  Samuel B. Fey,et al.  Thermal sensitivity predicts the establishment success of nonnative species in a mesocosm warming experiment. , 2012, Ecology.

[3]  Robert C. Edgar,et al.  BIOINFORMATICS APPLICATIONS NOTE , 2001 .

[4]  Lynne Boddy,et al.  Species-specific effects of soil fauna on fungal foraging and decomposition , 2011, Oecologia.

[5]  K. McCann The diversity–stability debate , 2000, Nature.

[6]  Tadashi Fukami,et al.  Do assembly history effects attenuate from species to ecosystem properties? A field test with wood-inhabiting fungi. , 2012, Ecology letters.

[7]  R. Paine Food Web Complexity and Species Diversity , 1966, The American Naturalist.

[8]  C. Mora,et al.  How Many Species Are There on Earth and in the Ocean? , 2011, PLoS biology.

[9]  T. Crowther,et al.  Interactive effects of warming and invertebrate grazing on the outcomes of competitive fungal interactions. , 2012, FEMS microbiology ecology.

[10]  R. Knight,et al.  Rapid denoising of pyrosequencing amplicon data: exploiting the rank-abundance distribution , 2010, Nature Methods.

[11]  Petr Baldrian,et al.  Cellulose utilization in forest litter and soil: identification of bacterial and fungal decomposers. , 2012, FEMS microbiology ecology.

[12]  D. Parkinson,et al.  Do mites and Collembola affect pine litter fungal biomass and microbial respiration , 1998 .

[13]  J. Lawton,et al.  Linking Species and Ecosystems , 1996 .

[14]  D. Wardle,et al.  The dual importance of competition and predation as regulatory forces in terrestrial ecosystems: evidence from decomposer food-webs , 1993, Oecologia.

[15]  Petr Baldrian,et al.  Estimation of fungal biomass in forest litter and soil , 2013 .

[16]  T. Crowther,et al.  Thermal acclimation in widespread heterotrophic soil microbes. , 2013, Ecology letters.

[17]  Lynne Boddy,et al.  Functional and ecological consequences of saprotrophic fungus–grazer interactions , 2012, The ISME Journal.

[18]  P. Baldrian Wood-inhabiting ligninolytic basidiomycetes in soils: Ecology and constraints for applicability in bioremediation , 2008 .

[19]  D. Wardle The influence of biotic interactions on soil biodiversity. , 2006, Ecology letters.

[20]  Hartley,et al.  Impacts of rising atmospheric carbon dioxide on model terrestrial ecosystems , 1998, Science.

[21]  D. Moorhead,et al.  A THEORETICAL MODEL OF LITTER DECAY AND MICROBIAL INTERACTION , 2006 .

[22]  N. Ostle,et al.  Microbial contributions to climate change through carbon cycle feedbacks , 2008, The ISME Journal.

[23]  S. Scheu,et al.  Adding to 'the enigma of soil animal diversity': fungal feeders and saprophagous soil invertebrates prefer similar food substrates , 2003 .

[24]  M. Bradford,et al.  Impacts of Soil Faunal Community Composition on Model Grassland Ecosystems , 2002, Science.

[25]  P. D. Ruiter,et al.  TOP-DOWN IS BOTTOM-UP: DOES PREDATION IN THE RHIZOSPHERE REGULATE ABOVEGROUND DYNAMICS? , 2003 .

[26]  M. Vestberg,et al.  Application of soil enzyme activity test kit in a field experiment , 2001 .

[27]  L. Tedersoo,et al.  454 Pyrosequencing and Sanger sequencing of tropical mycorrhizal fungi provide similar results but reveal substantial methodological biases. , 2010, The New phytologist.

[28]  S. Allison,et al.  Resistance, resilience, and redundancy in microbial communities , 2008, Proceedings of the National Academy of Sciences.

[29]  J. Kopecký,et al.  Active and total microbial communities in forest soil are largely different and highly stratified during decomposition , 2011, The ISME Journal.

[30]  K. Treseder,et al.  Microbial communities and their relevance for ecosystem models: Decomposition as a case study , 2010 .

[31]  K. Newell Interaction between two decomposer basidiomycetes and a collembolan under Sitka spruce: Distribution, abundance and selective grazing , 1984 .

[32]  J. Amador,et al.  Role of the anecic earthworm Lumbricus terrestris L. in the distribution of plant residue nitrogen in a corn (Zea mays)-soil system , 2005 .

[33]  D. Wardle,et al.  Ecological Linkages Between Aboveground and Belowground Biota , 2004, Science.

[34]  K. R. Clarke,et al.  Change in marine communities : an approach to statistical analysis and interpretation , 2001 .

[35]  J. C. Moore,et al.  The detrital food web in a shortgrass prairie , 1987, Biology and Fertility of Soils.

[36]  L. Boddy,et al.  Impacts of elevated temperature on the growth and functioning of decomposer fungi are influenced by grazing collembola , 2012 .

[37]  H. Friberg,et al.  New primers to amplify the fungal ITS2 region--evaluation by 454-sequencing of artificial and natural communities. , 2012, FEMS microbiology ecology.

[38]  Andy F. S. Taylor,et al.  ClassII peroxidase-encoding genes are present in a phylogenetically wide range of ectomycorrhizal fungi , 2009, The ISME Journal.

[39]  Bryan S. Griffiths,et al.  Impact of Protozoan Grazing on Bacterial Community Structure in Soil Microcosms , 2002, Applied and Environmental Microbiology.

[40]  Lynne Boddy,et al.  Outcomes of fungal interactions are determined by soil invertebrate grazers. , 2011, Ecology letters.

[41]  M. Tena,et al.  Sugar beet herbicides and soil nitrification , 1984 .

[42]  O. Gascuel,et al.  SeaView version 4: A multiplatform graphical user interface for sequence alignment and phylogenetic tree building. , 2010, Molecular biology and evolution.

[43]  Adam Godzik,et al.  Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences , 2006, Bioinform..

[44]  L. Boddy,et al.  Interspecific combative interactions between wood-decaying basidiomycetes. , 2000, FEMS microbiology ecology.

[45]  Lynne Boddy,et al.  SAPROTROPHIC CORD-FORMING FUNGI : MEETING THE CHALLENGE OF HETEROGENEOUS ENVIRONMENTS , 1999 .

[46]  M. Gessner,et al.  Diversity meets decomposition. , 2010, Trends in ecology & evolution.

[47]  S. Allison,et al.  Stoichiometry of soil enzyme activity at global scale. , 2008, Ecology letters.

[48]  W. Boer,et al.  Disruption of root carbon transport into forest humus stimulates fungal opportunists at the expense of mycorrhizal fungi , 2010, The ISME Journal.

[49]  J. Lennon,et al.  Microbial seed banks: the ecological and evolutionary implications of dormancy , 2011, Nature Reviews Microbiology.

[50]  W. Topp,et al.  Distribution pattern of woodlice (Isopoda) and millipedes (Diplopoda) in four primeval forests of the Western Carpathians (Central Slovakia) , 2006 .