Co-occurring Fungal Functional Groups Respond Differently to Tree Neighborhoods and Soil Properties Across Three Tropical Rainforests in Panama
Abiotic and biotic drivers of co-occurring fungal functional guilds across regional-scale environmental gradients remain poorly understood. We characterized fungal communities using Illumina sequencing from soil cores collected across three Neotropical rainforests in Panama that vary in soil properties and plant community composition. We classified each fungal OTU into different functional guilds, namely plant pathogens, saprotrophs, arbuscular mycorrhizal (AM), or ectomycorrhizal (ECM). We measured soil properties and nutrients within each core and determined the tree community composition and richness around each sampling core. Canonical correspondence analyses showed that soil pH and moisture were shared potential drivers of fungal communities for all guilds. However, partial the Mantel tests showed different strength of responses of fungal guilds to composition of trees and soils. Plant pathogens and saprotrophs were more strongly correlated with soil properties than with tree composition; ECM fungi showed a stronger correlation with tree composition than with soil properties; and AM fungi were correlated with soil properties, but not with trees. In conclusion, we show that co-occurring fungal guilds respond differently to abiotic and biotic environmental factors, depending on their ecological function. This highlights the joint role that abiotic and biotic factors play in determining composition of fungal communities, including those associated with plant hosts.
KeywordsMycorrhizal fungi Functional groups Soil phosphorus Microbial ecology ITS1 Metabarcoding Plant–soil (below ground) interactions Panama
We thank members of the Jones Lab at Oregon State University Department of Botany & Plant Pathology for helpful comments on the manuscript and Dayana Agudo and Aleksandra Bielnicka for laboratory support.
Sequencing data are available in GenBank (Bioproject number PRJNA363090). Tree neighborhood, OTU table, root biomass, and soil property data are available in Dryad doi 10.5061/dryad.sc38s.
Smithsonian Tropical Research Institute (STRI) offered logistical support. Financial support for this work comes from Oregon State University and the National Science Foundation (DEB 1542681), a fellowship from Oregon State University, and an internship from STRI.
Compliance with Ethical Standards
Conflict of Interest
The authors declare that they have no conflict of interest.
- 13.Brown JKM, Tellier A (2011) Plant-parasite coevolution: bridging the gap between genetics and ecology. Annu Rev Phytopathol 49:345–367. https://doi.org/10.1146/annurev-phyto-072910-095301 CrossRefPubMedGoogle Scholar
- 15.Campos-Soriano L, García-Martínez J, Segundo BS (2012) The arbuscular mycorrhizal symbiosis promotes the systemic induction of regulatory defence-related genes in rice leaves and confers resistance to pathogen infection. Mol Plant Pathol 13:579–592. https://doi.org/10.1111/j.1364-3703.2011.00773.x CrossRefGoogle Scholar
- 16.Carson WP, Anderson JT, Leigh E, Schnitzer SA (2008) Challenges associated with testing and falsifying the Janzen-Connell hypothesis: a review and critique. Tropical Forest Community Ecology 210–241Google Scholar
- 21.Condit R, Pẽrez R, Aguilar S, Lao S (2013b) Data from tree censuses and inventories in Panama; https://doi.org/10.5479/data.stri.2016.0622
- 22.Connell JH (1971) On the role of natural enemies in preventing competitive exclusion in some marine animals and in rain forest trees. Dyn Popul 298:312Google Scholar
- 23.Core Team R (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
- 28.Duchesne LC, Peterson RL, Ellis BE (1988) Pine root exudate stimulates the synthesis of antifungal compounds by the ectomycorrhizal fungus Paxillus involutus. New Phytol 108:471–476. https://doi.org/10.1111/j.1469-8137.1988.tb04188.x CrossRefGoogle Scholar
- 35.Gadgil PD, Gadgil RL (1975) Suppression of litter decomposition by mycorrhizal roots of Pinus radiata. N Z J For Sci 5:33–41Google Scholar
- 36.Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes - application to the identification of mycorrhizae and rusts. Mol Ecol 2:113–118. https://doi.org/10.1111/j.1365-294X.1993.tb00005.x CrossRefPubMedGoogle Scholar
- 42.Hättenschwiler S, Tiunov AV, Scheu S (2005) Biodiversity and litter decomposition in terrestrial ecosystems. Annu Rev Ecol Evol Syst 36:191–218. https://doi.org/10.1146/annurev.ecolsys.36.112904.151932 CrossRefGoogle Scholar
- 45.Herre EA, Kyllo D, Mangan S, et al (2005) An overview of arbuscular mycorrhizal fungi composition, distribution, and host effects from a tropical moist forest. In: Burslem D, Pinard M, Hartley S (eds) Biotic interactions in the tropics: Their role in the maintenance of species diversity. Cambridge University Press, Cambridge, UK, pp 204–225Google Scholar
- 59.Lee C-S, Lee Y-J, Jeun Y-C (2005) Observations of infection structures on the leaves of cucumber plants pre-treated with arbuscular mycorrhiza Glomus intraradices after challenge inoculation with Colletotrichum orbiculare. Plant Pathol J 21:237–243. https://doi.org/10.5423/PPJ.2005.21.3.237 CrossRefGoogle Scholar
- 60.Legendre P, Legendre L (2012) Chapter 11 - Canonical analysis. In: Legendre P, Legendre L (eds) Developments in Environmental Modelling. Elsevier, pp 625–710Google Scholar
- 71.Oksanen J, Blanchet FG, Friendly M, et al (2017) vegan: Community Ecology Package. R package version 2.4–5. https://CRAN.R-project.org/package=vegan
- 78.Robson AD, Abbott LK (1989) 4 - The Effect of Soil Acidity on Microbial Activity in Soils. In: Robson AD (ed) Soil Acidity and Plant Growth. Academic Press, pp 139–165Google Scholar
- 81.Senechkin IV, van Overbeek LS, van Bruggen AHC (2014) Greater Fusarium wilt suppression after complex than after simple organic amendments as affected by soil pH, total carbon and ammonia-oxidizing bacteria. Appl Soil Ecol 73:148–155. https://doi.org/10.1016/j.apsoil.2013.09.003 CrossRefGoogle Scholar
- 84.Smith SE, Read D (2008) 5 - Mineral nutrition, toxic element accumulation and water relations of arbuscular mycorrhizal plants. In: Mycorrhizal Symbiosis (Third Edition). Academic Press, London, pp 145–187Google Scholar
- 85.Smith SE, Anderson IC, Smith FA (2015) Mycorrhizal associations and phosphorus acquisition: from cells to ecosystems. Annu Plant Rev 48:409–440Google Scholar
- 92.Tedersoo L, Bahram M, Põlme S, Kõljalg U, Yorou NS, Wijesundera R, … Abarenkov K (2014) Global diversity and geography of soil fungi. Science 346(6213). doi: https://doi.org/10.1126/science.1256688
- 96.Turner BL, Romero TE (2009) Short-Term Changes in Extractable Inorganic Nutrients during Storage of Tropical Rain Forest Soils. Soil Science Society of America Journal 73:1972–1979. https://doi.org/10.2136/sssaj2008.0407
- 101.White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. PCR Protoc Guide Methods Appl 18:315–322Google Scholar