Brian J. Pickles

Navigating the labyrinth: a guide to sequence‐based, community ecology of arbuscular mycorrhizal fungi

Data generated from next generation sequencing (NGS) will soon comprise the majority of information about arbuscular mycorrhizal fungal (AMF) communities. Although these approaches give deeper insight, analysing NGS data involves decisions that can significantly affect results and conclusions. This is particularly true for AMF community studies, because much remains to be known about their basic biology and genetics. During a workshop in 2013, representatives from seven research groups using NGS for AMF community ecology gathered to discuss common challenges and directions for future research. Our goal was to improve the quality and accessibility of NGS data for the AMF research community. Discussions spanned sampling design, sample preservation, sequencing, bioinformatics and data archiving. With concrete examples we demonstrated how different approaches can significantly alter analysis outcomes. Failure to consider the consequences of these decisions may compound bias introduced at each step along the workflow. The products of these discussions have been summarized in this paper in order to serve as a guide for any researcher undertaking NGS sequencing of AMF communities.

Local adaptation in migrated interior Douglas‐fir seedlings is mediated by ectomycorrhizas and other soil factors

Separating edaphic impacts on tree distributions from those of climate and geography is notoriously difficult. Aboveground and belowground factors play important roles, and determining their relative contribution to tree success will greatly assist in refining predictive models and forestry strategies in a changing climate. In a common glasshouse, seedlings of interior Douglas-fir (Pseudotsuga menziesii var. glauca) from multiple populations were grown in multiple forest soils. Fungicide was applied to half of the seedlings to separate soil fungal and nonfungal impacts on seedling performance. Soils of varying geographic and climatic distance from seed origin were compared, using a transfer function approach. Seedling height and biomass were optimized following seed transfer into drier soils, whereas survival was optimized when elevation transfer was minimised. Fungicide application reduced ectomycorrhizal root colonization by c. 50%, with treated seedlings exhibiting greater survival but reduced biomass. Local adaptation of Douglas-fir populations to soils was mediated by soil fungi to some extent in 56% of soil origin by response variable combinations. Mediation by edaphic factors in general occurred in 81% of combinations. Soil biota, hitherto unaccounted for in climate models, interacts with biogeography to influence plant ranges in a changing climate.

Host and habitat filtering in seedling root-associated fungal communities: taxonomic and functional diversity are altered in ‘novel’ soils

Climatic and land use changes have significant consequences for the distribution of tree species, both through natural dispersal processes and following management prescriptions. Responses to these changes will be expressed most strongly in seedlings near current species range boundaries. In northern temperate forest ecosystems, where changes are already being observed, ectomycorrhizal fungi contribute significantly to successful tree establishment. We hypothesised that communities of fungal symbionts might therefore play a role in facilitating, or limiting, host seedling range expansion. To test this hypothesis, ectomycorrhizal communities of interior Douglas-fir and interior lodgepole pine seedlings were analysed in a common greenhouse environment following growth in five soils collected along an ecosystem gradient. Currently, Douglas-fir’s natural distribution encompasses three of the five soils, whereas lodgepole pine’s extends much further north. Host filtering was evident amongst the 29 fungal species encountered: 7 were shared, 9 exclusive to Douglas-fir and 13 exclusive to lodgepole pine. Seedlings of both host species formed symbioses with each soil fungal community, thus Douglas-fir did so even where those soils came from outside its current distribution. However, these latter communities displayed significant taxonomic and functional differences to those found within the host distribution, indicative of habitat filtering. In contrast, lodgepole pine fungal communities displayed high functional similarity across the soil gradient. Taxonomic and/or functional shifts in Douglas-fir fungal communities may prove ecologically significant during the predicted northward migration of this species; especially in combination with changes in climate and management operations, such as seed transfer across geographical regions for forestry purposes.

Mycorrhizal Networks and Forest Resilience to Drought

Many forest ecosystems are experiencing increased drought stress because of changing patterns of aridity, caused by both climate change and human land-use activities. Mycorrhizal fungi are known to provide their hosts with increased drought resistance in many circumstances, either through improved resource acquisition, direct uptake of water, or translocation of water obtained by their hosts. The ability of many mycorrhizal fungi to form mycelial networks, in which an individual mycelium connects to the roots of multiple host plants, provides a mechanism for the redistribution of water into upper soil layers experiencing low soil water potential. Here we review the roles of mycorrhizal fungi and mycorrhizal networks in water uptake and hydraulic redistribution, and consider how these may interact with host plants to moderate forest responses to increasing drought pressure. Lastly we present knowledge gaps and suggest several areas which would benefit from further research.

The paleosymbiosis hypothesis: host plants can be colonised by root symbionts that have been inactive for centuries to millenia

ABSTRACT Paleoecologists have speculated that post‐glacial migration of tree species could have been facilitated by mycorrhizal symbionts surviving glaciation as resistant propagules belowground. The general premise of this idea, which we call the ‘paleosymbiosis hypothesis’, is that host plants can access and be colonised by fungal root symbionts that have been inactive for millennia. Here, we explore the plausibility of this hypothesis by synthesising relevant findings from a diverse literature. For example, the paleoecology literature provided evidence of modern roots penetrating paleosols containing ancient (>6000 years) fungal propagules, though these were of unknown condition. With respect to propagule longevity, the available evidence is of mixed quality, but includes convincing examples consistent with the paleosymbiosis hypothesis (i.e. >1000 years viable propagules). We describe symbiont traits and environmental conditions that should favour the development and preservation of an ancient propagule bank, and discuss the implications for our understanding of soil symbiont diversity and ecosystem functioning. We conclude that the paleosymbiosis hypothesis is plausible in locations where propagule deposition and preservation conditions are favourable (e.g. permafrost regions). We encourage future belowground research to consider and explore the potential temporal origins of root symbioses. &NA; Graphical Abstract Figure. The authors assess evidence that certain mycorrhizal fungi may produce resistant propagules that remain viable for hundreds to thousands of years before colonising host plants, this is the ‘paleosymbiosis hypothesis’.

Exploring the symbiont diversity of ancient western redcedars: arbuscular mycorrhizal fungi of long-lived hosts

Arbuscular mycorrhizal fungi (AMF) are globally distributed, monophyletic root symbionts with ancient origins. Their contribution to carbon cycling and nutrient dynamics is ecologically important, given their obligate association with over 70% of vascular plant species. Current understanding of AMF species richness and community structure is based primarily on studies of grasses, herbs and agricultural crops, typically in disturbed environments. Few studies have considered AMF interactions with long‐lived woody perennial species in undisturbed ecosystems. Here we examined AMF communities associated with roots and soils of young, mature and old western redcedar (Thuja plicata) at two sites in the old‐growth temperate rainforests of British Columbia. Due to the unique biology of AMF, community richness and structure were assessed using a conservative, clade‐based approach. We found 91 AMF OTUs across all samples, with significantly greater AMF richness in the southern site, but no differences in richness along the host chronosequence at either site. All host age classes harboured AMF communities that were overdispersed (more different to each other than expected by chance), with young tree communities most resembling old tree communities. A comparison with similar clade richness data obtained from the literature indicates that western redcedar AMF communities are as rich as those of grasses, tropical trees and palms. Our examination of undisturbed temperate old‐growth rainforests suggests that priority effects, rather than succession, are an important aspect of AMF community assembly in this ecosystem.