Lepa juurtel ektomükoriisat moodustavate seente biogeograafia ja ökoloogia

Väitekirja elektrooniline versioon ei sisalda publikatsioone.Antud doktoritöö adresseerib lepaga koos kasvavate ektomükoriissete seente biogeograafiat ja ökoloogiat. Oma laialdase leviku ja spetsiifilise seenestiku tõttu sobivad lepp ja tema juuresümbiondid heaks mudeliks uurimaks mitmesuguseid ökoloogilisi seaduspärasusi mis puudutavad ektomükoriiseid seeni ja neid mõjutavaid tegureid nii regionaalses kui globaalses skaalas. Oma töös testisin järgnevaid põhilisi hüpoteese: 1) globaalses skaalas mõjutab lepa seenekoosluse struktuuri enim peremeesliikide fülogeneetilised distantsid; 2) regionaalses skaalas mõjutab lepa juurtel ektomükoriisat moodustavate seente koosluse struktuuri mulla koostis, eriti pH ja fosfor; 3) globaalses skaalas on lepaga seotud ektomükoriisa seente liigiline mitmekesisus määratud aasta keskmise temperatuuri ja sademete hulga poolt; 4) lepaga seotud ektomükoriisa seente biogeograafia peegeldab peremehe globaalseid levikuteid. Selgus, et globaalses skaalas mõjutavad peremeesliikide fülogeneetilised distantsid 43% ulatuses lepaga seotud ektomükoriissete seente koosluse struktuuri. Ruumiline paiknevus mõjutab seenekoosluse struktuuri 10% ulatuses ning mulla pH–l ja aasta keskmisel temperatuuril on marginaalne mõju. Seevastu regionaalses skaalas, määravad mulla pH ja orgaanilise aine sisaldus, enim seenekoosluse struktuuri. Varasemad uuringud on leidnud, et peamised mõjutegurid, mis määravad ektomükoriissete seente liigirikkust globaalses skaalas, on aasta keskmine temperatuur ja sademete hulk. Meie uuringust selgus üllatuslikult, et lepaga seotud ektomükoriissete seente liigirikkus on enim mõjutatud ja positiivses seoses mulla kaltsiumisisaldusega. Samas leidis kinnitust negatiivne seos ektomükoriisa liigirikkuse ja sademete hulga vahel. Sarnaselt globaalsele mustrile, oli ka regionaalses skaalas liigirikkus negatiivses seoses mulla veesisaldusega. Võrreldes lepaga seotud seenekoosluste liigist ja arvulist koosseisu erinevate mandrite ja piirkondade vahel selgus, et tõenäoliselt on Beringia maismaasild olnud põhiline lepa levikutee Euraasia ja Ameerika vahel. Põhja ja Lõuna Euroopa seenekooslused osutusid väga sarnaseks, mis tõenäoliselt tuleneb jääaja järgsest lepa ja tema juursümbiontide levikust põhja suunas lõunapoolsetest refuugiumidest.This thesis examines the community structure, species richness and biogeography of Alnus-associated ectomycorrhizal (EcM) fungi from local to global scales. Alnus has a wide geographical range of distribution and low richness of fungal symbionts, which enables to address the following hypothesis: 1) host species and their phylogenetic relationships account for the strongest predictor of EcM fungal community composition at the intrageneric level at the global scale; 2) at regional scale, soil conditions such as pH and phosphorus concentration drive the EcM community structure rather than geographical and host genetic distance; 3) at global scale, Alnus-associated EcM fungal species richness is largely determined by the mean annual temperature and precipitation; 4) global biogeography of Alnus EcM communities reflects ancient migration routes of host. The main results and conclusions are the following 1) phylogenetic relations among hosts account for strongest predictor of EcM community structure, while geographical and edaphic variables have a relatively low impact at the global scale; 2) at the regional scale edaphic variables were the dominant determinants of EcM fungal community structure; 3) soil calcium accounted for the key determinant of Alnus-associated EcM fungal species richness at the global scale, while soil humidity was the most influential at the local and regional scales; 4) Beringia is likely to be primary migration route of Alnus from Eurasia to America rather than North Atlantic land bridge 5) high similarity between North and South Europe probably results from recent post-glacial recolonisation

The curse of the uncultured fungus

The international DNA sequence databases abound in fungal sequences not annotated beyond the kingdom level, typically bearing names such as “uncultured fungus”. These sequences beget low-resolution mycological results and invite further deposition of similarly poorly annotated entries. What do these sequences represent? This study uses a 767,918-sequence corpus of public full-length fungal ITS sequences to estimate what proportion of the 95,055 “uncultured fungus” sequences that represent truly unidentifiable fungal taxa – and what proportion of them that would have been straightforward to annotate to some more meaningful taxonomic level at the time of sequence deposition. Our results suggest that more than 70% of these sequences would have been trivial to identify to at least the order/family level at the time of sequence deposition, hinting that factors other than poor availability of relevant reference sequences explain the low-resolution names. We speculate that researchers’ perceived lack of time and lack of insight into the ramifications of this problem are the main explanations for the low-resolution names. We were surprised to find that more than a fifth of these sequences seem to have been deposited by mycologists rather than researchers unfamiliar with the consequences of poorly annotated fungal sequences in molecular repositories. The proportion of these needlessly poorly annotated sequences does not decline over time, suggesting that this problem must not be left unchecked

Tree diversity and species identity effects on soil fungi, protists and animals are context dependent

Plant species richness and the presence of certain influential species (sampling effect) drive the stability and functionality of ecosystems as well as primary production and biomass of consumers. However, little is known about these floristic effects on richness and community composition of soil biota in forest habitats owing to methodological constraints. We developed a DNA metabarcoding approach to identify the major eukaryote groups directly from soil with roughly species-level resolution. Using this method, we examined the effects of tree diversity and individual tree species on soil microbial biomass and taxonomic richness of soil biota in two experimental study systems in Finland and Estonia and accounted for edaphic variables and spatial autocorrelation. Our analyses revealed that the effects of tree diversity and individual species on soil biota are largely context dependent. Multiple regression and structural equation modelling suggested that biomass, soil pH, nutrients and tree species directly affect richness of different taxonomic groups. The community composition of most soil organisms was strongly correlated due to similar response to environmental predictors rather than causal relationships. On a local scale, soil resources and tree species have stronger effect on diversity of soil biota than tree species richness per se

Shifts in ectomycorrhizal fungal communities and exploration types relate to the environment and fine-root traits across interior Douglas-fir forests of western Canada

Large-scale studies that examine the responses of ectomycorrhizal fungi across biogeographic gradients are necessary to assess their role in mediating current and predicted future alterations in forest ecosystem processes. We assessed the extent of environmental filtering on interior Douglas-fir (Pseudotsuga menziesii var. glauca (Beissn.) Franco) ectomycorrhizal fungal communities across regional gradients in precipitation, temperature, and soil fertility in interior Douglas-fir dominated forests of western Canada. We also examined relationships between fine-root traits and mycorrhizal fungal exploration types by combining root and fungal trait measurements with next-generation sequencing. Temperature, precipitation, and soil C:N ratio affected fungal community dissimilarities and exploration type abundance but had no effect on fungal richness and α‐diversity. Fungi with rhizomorphs (e.g., Piloderma sp.) and/or proteolytic abilities (e.g., Cortinarius sp.) dominated communities in warmer and less fertile environments. Ascomycetes (e.g., Cenococcum geophilum) and/or shorter distance explorers, which are potentially cost the plant less C, were favored in colder/drier climates where soils were richer in total nitrogen. Environmental filtering of ectomycorrhizal fungal communities is potentially related to co-evolutionary history between Douglas-fir populations and fungal symbionts, suggesting success of interior Douglas-fir as climate changes may be dependent on maintaining strong associations with local communities of mycorrhizal fungi. No evidence for a link between root and fungal resource foraging strategies was found at the regional scale. This lack of evidence further supports the need for a separate mycorrhizal symbiosis framework, independent from root trait frameworks, to aid in understanding below-ground plant uptake strategies across environments

Global patterns in endemicity and vulnerability of soil fungi

Fungi are highly diverse organisms, which provide multiple ecosystem services. However, compared with charismatic animals and plants, the distribution patterns and conservation needs of fungi have been little explored. Here, we examined endemicity patterns, global change vulnerability and conservation priority areas for functional groups of soil fungi based on six global surveys using a high-resolution, long-read metabarcoding approach. We found that the endemicity of all fungi and most functional groups peaks in tropical habitats, including Amazonia, Yucatan, West-Central Africa, Sri Lanka, and New Caledonia, with a negligible island effect compared with plants and animals. We also found that fungi are predominantly vulnerable to drought, heat and land-cover change, particularly in dry tropical regions with high human population density. Fungal conservation areas of highest priority include herbaceous wetlands, tropical forests, and woodlands. We stress that more attention should be focused on the conservation of fungi, especially root symbiotic arbuscular mycorrhizal and ectomycorrhizal fungi in tropical regions as well as unicellular early-diverging groups and macrofungi in general. Given the low overlap between the endemicity of fungi and macroorganisms, but high conservation needs in both groups, detailed analyses on distribution and conservation requirements are warranted for other microorganisms and soil organisms

Global patterns in endemicity and vulnerability of soil fungi

Fungi are highly diverse organisms, which provide multiple ecosystem services. However, compared with charismatic animals and plants, the distribution patterns and conservation needs of fungi have been little explored. Here, we examined endemicity patterns, global change vulnerability and conservation priority areas for functional groups of soil fungi based on six global surveys using a high-resolution, long-read metabarcoding approach. We found that the endemicity of all fungi and most functional groups peaks in tropical habitats, including Amazonia, Yucatan, West-Central Africa, Sri Lanka, and New Caledonia, with a negligible island effect compared with plants and animals. We also found that fungi are predominantly vulnerable to drought, heat and land-cover change, particularly in dry tropical regions with high human population density. Fungal conservation areas of highest priority include herbaceous wetlands, tropical forests, and woodlands. We stress that more attention should be focused on the conservation of fungi, especially root symbiotic arbuscular mycorrhizal and ectomycorrhizal fungi in tropical regions as well as unicellular early-diverging groups and macrofungi in general. Given the low overlap between the endemicity of fungi and macroorganisms, but high conservation needs in both groups, detailed analyses on distribution and conservation requirements are warranted for other microorganisms and soil organisms

Global diversity and distribution of nitrogen-fixing bacteria in the soil

Our knowledge of microbial biogeography has advanced in recent years, yet we lack knowledge of the global diversity of some important functional groups. Here, we used environmental DNA from 327 globally collected soil samples to investigate the biodiversity patterns of nitrogen-fixing bacteria by focusing on the nifH gene but also amplifying the general prokaryotic 16S SSU region. Globally, N-fixing prokaryotic communities are driven mainly by climatic conditions, with most groups being positively correlated with stable hot or seasonally humid climates. Among soil parameters, pH, but also soil N content were most often shown to correlate with the diversity of N-fixer groups. However, specific groups of N-fixing prokaryotes show contrasting responses to the same variables, notably in Cyanobacteria that were negatively correlated with stable hot climates, and showed a U-shaped correlation with soil pH, contrary to other N-fixers. Also, the non-N-fixing prokaryotic community composition was differentially correlated with the diversity and abundance of N-fixer groups, showing the often-neglected impact of biotic interactions among bacteria

FungalTraits:A user-friendly traits database of fungi and fungus-like stramenopiles

The cryptic lifestyle of most fungi necessitates molecular identification of the guild in environmental studies. Over the past decades, rapid development and affordability of molecular tools have tremendously improved insights of the fungal diversity in all ecosystems and habitats. Yet, in spite of the progress of molecular methods, knowledge about functional properties of the fungal taxa is vague and interpretation of environmental studies in an ecologically meaningful manner remains challenging. In order to facilitate functional assignments and ecological interpretation of environmental studies we introduce a user friendly traits and character database FungalTraits operating at genus and species hypothesis levels. Combining the information from previous efforts such as FUNGuild and Fun(Fun) together with involvement of expert knowledge, we reannotated 10,210 and 151 fungal and Stramenopila genera, respectively. This resulted in a stand-alone spreadsheet dataset covering 17 lifestyle related traits of fungal and Stramenopila genera, designed for rapid functional assignments of environmental studies. In order to assign the trait states to fungal species hypotheses, the scientific community of experts manually categorised and assigned available trait information to 697,413 fungal ITS sequences. On the basis of those sequences we were able to summarise trait and host information into 92,623 fungal species hypotheses at 1% dissimilarity threshold

Temporally variable geographical distance effects contribute to the assembly of root-associated fungal communities

Root-associated fungi are key contributors to ecosystem functioning, however, the factors which determine community assembly are still relatively poorly understood. This study simultaneously quantified the roles of geographical distance, environmental heterogeneity and time in determining root-associated fungal community composition at the local scale within a short rotation coppice (SRC) willow plantation. Culture independent molecular analyses of the root-associated fungal community suggested a strong but temporally variable effect of geographical distance among fungal communities in terms of composition at the local geographical level. Whilst these distance effects were most prevalent on October communities, soil pH had an effect on structuring of the communities throughout the sampling period. Given the temporal variation in the effects of geographical distance and the environment for shaping root-associated fungal communities, there is clearly need for a temporal component to sampling strategies in future investigations of fungal ecology

Connecting the multiple dimensions of global soil fungal diversity

How the multiple facets of soil fungal diversity vary worldwide remains virtually unknown, hindering the management of this essential species-rich group. By sequencing high-resolution DNA markers in over 4000 topsoil samples from natural and human-altered ecosystems across all continents, we illustrate the distributions and drivers of different levels of taxonomic and phylogenetic diversity of fungi and their ecological groups. We show the impact of precipitation and temperature interactions on local fungal species richness (alpha diversity) across different climates. Our findings reveal how temperature drives fungal compositional turnover (beta diversity) and phylogenetic diversity, linking them with regional species richness (gamma diversity). We integrate fungi into the principles of global biodiversity distribution and present detailed maps for biodiversity conservation and modeling of global ecological processes