June, 2018

June, 2018

What we are reading in June, 2018

By: Camille Truong, associate researcher, and Andrés Argüelles Moyao, Doctoral student, National Autonomous University of México, México. 


Camille Truong:

Van der Linde S, Suz LM, Orme CDL, Cox F, Andreae H, Asi E, Atkinson B, Benham S, Carroll C, Cools N, et al. (2018) Environment and host as large-scale controls of ectomycorrhizal fungi. Nature 558: 10.1038/s41586-018-0189-9.

Climate change is the hot topic of the century and scientists across the globe are trying to understand its impact on biodiversity. Because of their role in regulating carbon and nitrogen cycles, ectomycorrhizal (ECM) fungi play central roles for forest resilience to changes in CO2 levels, in correlation with carbon balance allocated to them by their plant-hosts and their capacity to store C belowground (Simard & Austin, 2010).

Local-scale studies repeatedly found that ECM fungi were strongly determined by soil parameters, but determinants at local scales are not necessarily their primary drivers at larger scales. Van der Linde et al. (2018) conducted an impressive meta-analysis of European trees using detailed soil, atmospheric and vegetation parameters from 20 European countries. As expected, host-plants were the strongest predictors of ECM belowground community composition (23%), followed by soil and atmospheric deposition (21%), while geographical distance and climatic variables explained 14% and 12% of the variation respectively. Although host generalism is considered the rule in ECM associations, the authors found that ECM specificity to European trees matched or exceeded generalism, particularly for conifers. Key environmental variables were nitrogen deposition, forest-floor pH, mean annual air temperature, potassium deposition and foliar nitrogen:phosophorus ratio. Although different species within a genus or family were both positively and negatively correlated with environmental variables, the response of ECM fungi to abiotic factors was generally phylogenetically conserved at least at the generic level. These results emphasize the role of ECM fungi for nitrogen cycling and plant nutrition. Nitrogen deposition due to human induced contamination may strongly disrupt the equilibrium of these ecosystems: By increasing nitrogen availability, fungi that release nitrogen from complex soil organic sources (for example, Cortinarius, Piloderma and Tricholoma) will be disadvantaged compared to fungi that use inorganic nitrogen (for example, Elaphomyces and Laccaria). Indeed, the authors observed that fungi that use organic nitrogen tended to be negative indicators for nitrogen deposition, and fungi that use inorganic nitrogen tended to be positive indicators. Again the fact that specialist species (especially with conifers) were more negatively affected by nitrogen deposition than generalists and broad-leaf specialists may be caused by differences in their enzymatic capability to acquire nitrogen from soil.

It is to be noted that more than 60% of the variation in ECM fungal communities remained unexplained and may be attributed to factors that were not accounted for, such as seasonality, disturbance, management history, and methodological pitfalls. Nevertheless this large-scale study of almost 10,000 soil cores from more than 100 plots across Europe revealed how atmospheric deposition is affecting species distributions in ECM communities and ring the bell to the effect of contamination and climate change on these forest ecosystems.

Simard SW, Austin M. 2010. The role of mycorrhizas in forest soil stability with climate change. In: Simard SW, Austin M, eds. Climate change and variability. Rijeka: Sciyo, 275–302.


Andrés Argüelles Moyao:

Argüelles-Moyao A, Garibay-Orijel R (2018) Ectomycorrhizal fungal communities in high mountain conifer forests in central Mexico and their potential use in the assisted migration of Abies religiosa. Mycorrhiza: 10.1007/s00572-018-0841-0

Mushrooms live in a diversity of habitats in the form of mycelia, propagules or sporocarps. The fungal community is structured by the interactions of these fungal species that vary in abundances and frequencies. These interactions largely influence ecosystem functions (Koide et al 2011). By studying the fungal community structure, community ecologists try to understand general rules that determine the community assembly.

The fungal colonization of new habitats by propagules depends of two major components, the host filtering and the abiotic filtering (pH, nitrogen availability, water). Both processes lead to competition for resources between fungal species in the community pool in a highly dynamic system that changes through time in correlation with changing environmental conditions. Species competitive interactions will therefore strongly affect the fungal community composition in correlation with host and abiotic factors (Koide et al 2011). Such interactions need to be taken in account in plant reintroduction procedures: For example, strongly competitive fungi present in the reintroduction site can displace ectomycorrhizal fungi co-introduced with their host (Flores-Rentería et al 2017). On the other hand, beneficial fungi can improve plant establishment in the field. These economic aspects are important for the success of mycorrhization programs.

Argüelles-Moyao and Garibay-Orijel (2018) used a community ecology approach to identify ectomycorrhizal fungal communities in a wide range of Mexican hosts and habitats. By doing so they identified potential fungal species with a low probability to suffer from competition when introduced in a new site. They hypothesized that ectomycorrhizal fungal species present in all sites (core-diversity) are the best candidates for re-introductions. The mycobiome is defined as all fungi present in an ecosystem (Peay et al 2016; Pagano et al 2017), which is analogous to the pan-genome concept, i.e. all genes present in a clade or group of organisms (Tettelin et al 2005). The mycobiome is composed by the core-diversity (species shared by all sites) and the accessory diversity (site-specific species) (Unterseher et al 2011; Yang et al 2016). This concept is used mainly in bacterial microbiome studies (Caporaso et al 2010), but can also be applied to determine endemic fungal communities (Talbot et al 2014).

In the soil fungal community from high altitude coniferous forests in central Mexico, the species present in the core-diversity represented 17% of the whole community of 1746 MOTU’s (Molecular Operative Taxonomic Unit). The ecological dominant families across sites (Russulaceae, Atheliaceae, and Clavulinaceae) were different from the core-diversity (Russulaceae, Clavulinaceae, and Inocybaceae). These families can dominate the soil community in the form of mycelia or propagules, therefore their root colonization capabilities and competitive abilities in field conditions need to be evaluated. For example, as the propagule bank is composed by asexual and sexual propagules with rates of germination (Nara 2009), the dominant Russulaceae species may not be the first colonizers of saplings in field condition. Furthermore, germination rates can affect the community assembly aside the species interactions, in processes like the priority effect (Kennedy et al 2005; Kennedy et al 2009), time of arriving (Peay 2018), and competitive interaction (Mujic et al 2016; Smith et al 2018). All this information is crucial to establish re-introduction programs of assisted migration of Abies religiosa, an endemic ectomycorrhizal plant from central Mexico that is severely threatened by climate change. Abies religiosa provides important ecosystem services, economic values, and is the only overwinter refuge of Monarch butterfly.

Forest management involves the control of external pressures such as climate change, invasive pests, and anthropogenic land-uses. Assisted migration is a human-aided plant translocation (Dumroese et al 2015) that involves the movement of one plant species to a predicted distribution range. Inoculations with ectomycorrhizal fungi have been recommended in forest practices to favor the plant reintroduction (Pérez-Moreno and Martinez-Reyes 2014; Nara 2015). As exemplified above, the fungal inoculum should be chosen from the core-diversity of the area to facilitate the migration of Abies religiosa.

Additional factors, such as fungal species turnover in soil, should be taken into consideration in reintroduction programs. Deforested soils have often lost ecosystem functions linked to fungal species, due to soil erosion or compaction (Sessitsch et al 2001; Meliani et al 2012). In consequence, reintroduction programs will have a higher chance of success in habitats with similar fungal species in the propagule bank, because the fungal present in the soil propagule bank are the main colonizer of saplings in field conditions (Pickles et al 2015). The species turnover analysis in Argüelles-Moyao and Garibay-Orijel (2018), points to Pinus montezumae as a potential habitat for Abies religiosa due to the lowest species dissimilarity.

Finally, the “hierarchical model of ectomycorrhizal fungal communities” can give information from the fungal community to select candidate fungal species for reintroduction programs. Based on the model prediction, these candidate species can be further evaluated with experiments.


Argüelles-Moyao A, Garibay-Orijel R (2018) Ectomycorrhizal fungal communities in high mountain conifer forests in central Mexico and their potential use in the assisted migration of Abies religiosa. Mycorrhiza. doi: https://doi.org/10.1007/s00572-018-0841-0
Caporaso JG, Kuczynski J, Stombaugh J, et al (2010) QIIME allows analysis of high- throughput community sequencing data Intensity normalization improves color calling in SOLiD sequencing. Nat Publ Gr 7:335–336. doi: 10.1038/nmeth0510-335
Dumroese RK, Williams MI, Stanturf JA, Clair JBS (2015) Considerations for restoring temperate forests of tomorrow: forest restoration, assisted migration, and bioengineering. New For 46:947–964. doi: 10.1007/s11056-015-9504-6
Flores-Rentería D, Barradas VL, Álvarez-Sánchez J (2017) Ectomycorrhizal pre-inoculation of Pinus hartwegii and Abies religiosa is replaced by native fungi in a temperate forest of central Mexico. Symbiosis 1–14. doi: 10.1007/s13199-017-0498-z
Kennedy PG, Bruns TD, Phytologist SN, May N (2005) Priority Pinus effects muricata determine between seedlings two the outcome of ectomycorrhizal species colonizing competition Rhizopogon. New Phytol 166:631–638.
Kennedy PG, Peay KG, Bruns TD (2009) Root tip competition among ectomycorrhizal fungi: Are priority effects a rule or an exception? Ecology 90:2098–2107. doi: 10.1890/08-1291.1
Koide RT, Fernandez C, Petprakob K (2011) General principles in the community ecology of ectomycorrhizal fungi. Ann For Sci 68:45–55. doi: 10.1007/s13595-010-0006-6
Meliani A, Bensoltane A, Mederbel K (2012) Microbial Diversity and Abundance in Soil: Related to Plant and Soil Type. Am J Plant Nutr Fertil Technol 2:10–18. doi: 10.3923/ajpnft.2012.10.18
Mujic AB, Durall DM, Spatafora JW, Kennedy PG (2016) Competitive avoidance not edaphic specialization drives vertical niche partitioning among sister species of ectomycorrhizal fungi. New Phytol 209:1174–1183. doi: 10.1111/nph.13677
Nara K (2009) Spores of ectomycorrhizal fungi: Ecological strategies for germination and dormancy. New Phytol 181:245–248. doi: 10.1111/j.1469-8137.2008.02691.x
Nara K (2015) The Role of Ectomycorrhizal Networks in Seedling Establishment and Primary Succession. In: Horton TR (ed) Mycorrhizal networks. Springer, pp 117–201
Pagano M, Correa E, Duarte N, et al (2017) Advances in Eco-Efficient Agriculture: The Plant-Soil Mycobiome. Agriculture 7:14. doi: 10.3390/agriculture7020014
Peay KG (2018) Timing of mutualist arrival has a greater effect on Pinus muricata seedling growth than interspecific competition. J Ecol 106:514–523. doi: 10.1111/1365-2745.12915
Peay KG, Kennedy PG, Talbot JM (2016) Dimensions of biodiversity in the Earth mycobiome. Nat Rev Microbiol 14:434–447. doi: 10.1038/nrmicro.2016.59
Pérez-Moreno J, Martinez-Reyes M (2014) Edible Ectomycorrhizal Mushrooms: Biofactories for Sustainable Development. In: Guevara-Gonzales R, Torres-Pacheco I (eds) Biosyst. Eng. Biofactories Food Prod. Century XXI. Springer International Publishing, Switzerland, pp 151–233
Pickles BJ, Gorzelak MA, Green DS, et al (2015) Host and habitat filtering in seedling root-associated fungal communities: taxonomic and functional diversity are altered in “novel” soils. Mycorrhiza 25:517–531. doi: 10.1007/s00572-015-0630-y
Sessitsch A, Weilharter A, Martin H, et al (2001) Microbial Population Structures in Soil Particle Size Fractions of a Long-Term Fertilizer Field Experiment. Appl Environ Microbiol 67:4215–4224. doi: 10.1128/AEM.67.9.4215
Smith GR, Steidinger BS, Bruns TD, Peay KG (2018) Competition–colonization tradeoffs structure fungal diversity. ISME J 1–10. doi: 10.1038/s41396-018-0086-0
Talbot JM, Bruns TD, Taylor JW, et al (2014) Endemism and functional convergence across the North American soil mycobiome. Proc Natl Acad Sci U S A 111:6341–6. doi: 10.1073/pnas.1402584111
Tettelin H, Masignani V, Cieslewicz MJ, et al (2005) Genome analysis of multiple pathogenic isolates of Streptococcus agalactiae: implications for the microbial “pan-genome”. Proc Natl Acad Sci U S A 102:13950–5. doi: 10.1073/pnas.0506758102
Unterseher M, Jumpponen A, Öpik M, et al (2011) Species abundance distributions and richness estimations in fungal metagenomics – Lessons learned from community ecology. Mol Ecol 20:275–285. doi: 10.1111/j.1365-294X.2010.04948.x
Yang T, Sun H, Shen C, Chu H (2016) Fungal Assemblages in Different Habitats in an Erman’s Birch Forest. Front Microbiol 7:1–12. doi: 10.3389/fmicb.2016.01368