Space and patchiness affects diversity-function relationships in fungal decay communities.
Journal
The ISME journal
ISSN: 1751-7370
Titre abrégé: ISME J
Pays: England
ID NLM: 101301086
Informations de publication
Date de publication:
03 2021
03 2021
Historique:
received:
04
05
2020
accepted:
05
10
2020
revised:
01
10
2020
pubmed:
18
10
2020
medline:
22
4
2021
entrez:
17
10
2020
Statut:
ppublish
Résumé
The space in which organisms live determines health and physicality, shaping the way in which they interact with their peers. Space, therefore, is critically important for species diversity and the function performed by individuals within mixed communities. The biotic and abiotic factors defined by the space that organisms occupy are ecologically significant and the difficulty in quantifying space-defined parameters within complex systems limits the study of ecological processes. Here, we overcome this problem using a tractable system whereby spatial heterogeneity in interacting fungal wood decay communities demonstrates that scale and patchiness of territory directly influence coexistence dynamics. Spatial arrangement in 2- and 3-dimensions resulted in measurable metabolic differences that provide evidence of a clear biological response to changing landscape architecture. This is of vital importance to microbial systems in all ecosystems globally, as our results demonstrate that community function is driven by the effects of spatial dynamics.
Identifiants
pubmed: 33067587
doi: 10.1038/s41396-020-00808-7
pii: 10.1038/s41396-020-00808-7
pmc: PMC8027639
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
720-731Références
Brown JH, Maurer BA. Macroecology: the division of food and space among species on continents. Science. 1989;243:1145–50.
pubmed: 17799895
O’Leary J, Eastwood DC, Müller CT, Boddy L. Emergent properties arising from spatial heterogeneity influence fungal community dynamics. Fungal Ecol. 2018;33:32–9.
Hiscox J, Savoury M, Toledo S, Kingscott-Edmunds J, Bettridge A, Waili NA, et al. Threesomes destabilise certain relationships: multispecies interactions between wood decay fungi in natural resources. FEMS Microbiol Ecol. 2017;93:fix014.
pmcid: 5399798
Froidevaux JSP, Zellweger F, Bollmann K, Jones G, Obrist MK. From field surveys to LIDAR: shining a light on how bats respond to forest structure. Remote Sens Environ. 2016;175:242–50.
Galand PE, Pereira O, Hochart C, Christophe A, Debroas D. A strong link between marine microbial community composition and function challenges the idea of functional redundancy. ISME J. 2018;12:2470–8.
pubmed: 29925880
pmcid: 6155072
O’Leary J, Hiscox J, Eastwood DC, Savoury M, Langley A, McDowell SW, et al. The whiff of decay: linking volatile production and extracellular enzymes to outcomes of fungal interactions under environmental change. Fungal Ecol. 2019;39:336–48.
Karadimou EK, Kallimanis AS, Tsiripidia I, Dimopoulos P. Functional diversity exhibits a diverse relationship with area, even a decreasing one. Sci Rep. 2016;6:35420.
pubmed: 27752086
pmcid: 5067660
Kolesidis DA, Boddy L, Eastwood DC, Yuan C, Fowler MS. Predicting fungal community dynamics driven by competition for space. Fungal Ecol. 2019;40:13–22.
Kerr B, Riley MA, Feldman MW, Bohannan BJM. Local dispersal promotes biodiversity in a real-life game of rock-paper-scissors. Nature.2002;418:171–4.
pubmed: 12110887
Reichenbach T, Mobilia M, Frey E. Mobility promotes and jeopardizes biodiversity in rock-paper-scissors games. Nature. 2007;448:1046–9.
pubmed: 17728757
Doherty JM, Callaway JC, Zedler JB. Diversity-function relationships changed in a long-term restoration experiment. Ecol Appl. 2011;21:2143–55.
pubmed: 21939050
Song Y, Wang P, Li G, Zhou D. Relationships between functional diversity and ecosystem functioning: a review. Acta Ecol Sin. 2011;34:85–91.
Bardgett RD, Freeman C, Ostle NJ. Microbial contributions to climate change through carbon cycle feedbacks. ISME J. 2008;2:805–14.
pubmed: 18615117
Boddy L. Interspecific combative interactions between wood‐decaying basidiomycetes. FEMS Microbiol Ecol. 2000;31:185–94.
pubmed: 10719199
Hiscox J, O’Leary J, Boddy L. Fungus wars: basidiomycete battles in wood decay. Stud Mycol. 2018;89:117–24.
pubmed: 29910518
pmcid: 6002336
Valášková V, Baldrian P. Estimation of bound and free fractions of lignocellulose degrading enzymes of wood rotting fungi Pleurotus ostreatus, Trametes versicolor and Piptiporus betulinus. Res Microbiol. 2006;157:119–24.
pubmed: 16125911
Martinez D, Challacombe J, Morgenstern I, Hibbett D, Schmoll M, Kubicek CP, et al. Genome, transcriptome, and secretome analysis of wood decay fungus Postia placenta supports unique mechanisms of lifnocellulose conversion. PNAS.2009;106:1954–9.
pubmed: 19193860
pmcid: 2644145
Hynes J, Müller CT, Jones HT, Boddy L. Changes in volatile production during the course of fungal mycelial interactions between Hypholoma fasciculare and Resinicium bicolor. J Chem Ecol. 2007;33:43–57.
pubmed: 17146718
Hiscox J, Baldrian P, Rogers HJ, Boddy L. Changes in oxidative enzyme activity during interspecific mycelial interactions involving the white-rot fungus Trametes versicolor. Fungal Genet Biol. 2010;47:562–71.
pubmed: 20371297
El Ariebi N, Hiscox J, Scriven SA, Müller CT, Boddy L. Production and effects of volatile organic compounds during interspecific interactions. Fungal Ecol. 2016;20:144–54.
Maynard DS, Crowther TW, Bradford MA. Competitive network determines the direction of the diversity-function relationship. PNAS. 2017;114:11464–9.
pubmed: 29073072
pmcid: 5664546
Hiscox J, Savoury M, Vaughan IP, Müller CT, Boddy L. Antagonistic fungal interactions influence carbon dioxide evolution from decomposing wood. Fungal Ecol. 2015;14:24–32.
Hiscox J, Savoury M, Müller CT, Lindahl BD, Rogers HJ, Boddy L. Priority effects during fungal community establishment in beech wood. ISME J. 2015;9:2246–60.
pubmed: 25798754
pmcid: 4579477
Hiscox J, Savoury M, Johnston SR, Parfitt D, Müller CT, Rodgers H, et al. Location, location, location: priority effects in wood decay communities may vary between sites. Environ Microbiol. 2016;18:1954–69.
pubmed: 26626102
Floudas D, Binder M, Riley R, Barry K, Blanchette RA, Henrissat B, et al. The Paleozoic origin of enzymatic lignin decomposition reconstructed from 31 fungal genomes. Science. 2012;336:1715–9.
pubmed: 22745431
Brown M, Dunn WB, Dobson P, Patel Y, Winder CL, Francis-McIntyre S, et al. Mass spectrometry tools and metabolite-specific databases for molecular indentification in metabolomics. Analyst. 2009;134:1322–32.
pubmed: 19562197
Dunn WB, Broadhurst D, Begley P, Zelena E, Francis-McIntyre S, Anderson N, et al. Procedures for large-scale metabolic profiling of serum and plasma using gas chromatography and liquid chromatography coupled to mass spectrometry. Nat Protoc. 2011; 6:1060–83.
Kirwan JA, Weber RJM, Broadhurst DI, Viant MR. Direct infusion mass spectrometry metabolomics dataset: a benchmark for data processing and quality control. Sci Data. 2014;1:140012.
pubmed: 25977770
pmcid: 4381748
Southam AD, Weber RJ, Engel J, Jones MR, Viant MR. A complete workflow for high-resolution spectral-stitching nanoelectrospray direct-infusion mass-spectrometry-based metabolomics and lipidomics. Nat Protoc. 2017;12:310.
Weber RJM, Viant MR. MI-Pack: increased confidence of metabolite identification in mass spectra by integrating accurate masses and metabolic pathways. Chemom Intell Lab Syst. 2010;104:75–82.
R Core Team. R: a language and environment for statistical computing. R Foundation for Statistical Computing; 2014. http://www.R-project.org/ .
Xia J, Wishart DS. Using MetaboAnalyst 3.0 for comprehensive metabolomics data analysis. Curr Protoc Bioinform. 2016;55:14.10.1–91.
Stelund H, Gorzsas A, Persson P, Sundberg B, Trygg J. Orthogonal projections to latent structures discriminant analysis modelling on in situ FT-IR spectral imaging of liver tissue for identifying sources of variability. Anal Chem. 2008;80:6898–906.
Benjamini Y, Hochberg Y. Controlling the false discovery rate—a practical and powerful approach to multiple testing. J R Stat Soc B. 1995;57:289–300.
Smilde AK, Jansen JJ, Hoefsloot HC, Lamers RJ, van der Greef J, Timmerman ME. ANOVA-simultaneous component analysis (ASCA): a new tool for analyzing designed metabolomics data. Bioinformatics. 2005;21:3043–8.
pubmed: 15890747
Engel J, Blanchet L, Bloemen B, van den Heuvel LP, Engelke UHF, Wevers RA, et al. Regularized MANOVA (rMANOVA) in untargeted metabolomics. Anal Chim Acta. 2015;899:1–12.
pubmed: 26547490
Hochberg Y. A sharper Bonferonni procedure for multiple tests of significance. Biometrika. 1988;75:800–80.
Jacomy M, Venturini T, Heymann S, Bastian M. ForceAtlas2, a continuous graph layout algorithm for handy network visualisation designed for the Gephi Software. PLoS ONE. 2014;9:e98679.
pubmed: 24914678
pmcid: 4051631
Sci2 Team. Science of science (Sci2) tool. Indiana University and SciTech Strategies; 2009. https://sci2.cns.iu.edu .
Bastian M, Heymann S, Jacomy M. Gephi: an open source software for exploring and manipulating networks. International AAAI conference on Weblogs and Social Media. Denmark: Aalborg University; 2009. pp. 361–362.
Johnston SR, Boddy L, Weightman AJ. Bacteria in decomposing wood and their interactions with wood-decay fungi. FEMS Microb Ecol. 2016;92:fiw179.
Blanchette RA, Shaw CG. Associations among bacteria, yeasts, and basidiomycetes during wood decay. Phytopathology. 1978;68:6317.
Tilman D, Knops J, Wedin D, Reich P, Ritchie M, Siemann E. The influence of functional diversity and competition on ecosystem processes. Science. 1997;277:1300–2.
Lambers JHR, Harpole WS, Tilman D, Knops J, Reich PB. Mechanisms responsible for the positive diversity-productivity relationship in Minnesota grassland. Ecol Lett. 2004;7:661–8.
Hillebrand H, Matthiessen B. Biodiversity in a complex world: consolidation and progress in functional biodiversity research. Ecol Lett. 2009;12:1405–19.
pubmed: 19849711
Freschet GT, Weedon JT, Aets R, van Hal JR, Cornelissen JHC. Interspecific differences in wood decay rates: insights from a new short-term method to study long-term wood decomposition. J Ecol. 2011;100:161–70.
Hobbie SE. Effects of plant species on nutrient cycling. Trends Ecol Evol. 1992;7:336–9.
pubmed: 21236058
Davidson EA, Janssens IA. Temperature sensitivity of soil carbon decomposition and feedbacks to climate change. Nature. 2006;440:165–73.
pubmed: 16525463
Kandeler E, Tscherko D, Bruce KD, Stemmer M, Hobbs PJ, Bardgett RD, et al. Structure and function of the soil microbial community in microhabitats of a heavy metal polluted soil. Biol Fertil Soils. 2000;32:390–400.
Wagner M, Loy A, Nogueira R, Purkhold U, Lee N, Daims H. Microbial community composition and function in wastewater treatment plants. Antonie Van Leeuwenhoek. 2002;81:665–80.
pubmed: 12448762
Tremaroli V, Bäckhed F. Functional interactions between the gut microbiota and host metabolism. Nature. 2012;489:241–9.