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Characterization of newly discovered but poorly understood fungal-driven trophic processes in freshwater lake ecosystems by metatranscriptomic

Periodic Reporting for period 1 - CRYPTRANS (Characterization of newly discovered but poorly understood fungal-driven trophic processes in freshwater lake ecosystems by metatranscriptomic)

Reporting period: 2015-07-01 to 2017-06-30

Fungi are the primary degraders of plant matter and are globally important for the oxygen/carbon dioxide balance, among many other things. The origin of fungi is clearly aquatic, since we find most of the early diverging fungal lineages in freshwater and marine ecosystems, where they show specific adaptations such as motile spores. Thus, these aquatic fungal lineages can shed light on the origin of the terrestrial fungi and the unique enzymes that allow them to degrade plant polymers efficiently. Despite this knowledge, early diverging waterborne fungi are rarely investigated due to their microscopic size, their indistinguishable features, and the difficulty associated with keeping them in culture in the laboratory.

Our aim with this project was to shed light on the very poorly understood aquatic fungi (notably the phyla Chytridiomycota and Cryptomycota), many lineages of which are new or even unknown to science. We investigated these new fungi and detailed their taxonomy, functional processes, and ecological services in a range of freshwater systems. The overarching questions were: (1) What fungi are there in these systems? (2) What are their functions and roles? (3) What are the implications for the study of fungi, freshwater ecosystems, and ecology at large?

This EU project started in the beginning of July 2015 by an extensive sampling campaign of approximately 150 – mainly Swedish – lakes spanning the substantial national latitudinal gradient. We used state of the art DNA sequence analysis methods to establish what types of fungi were present in these freshwater systems. We found that several early diverging fungal lineages dominated the lake ecosystems, and it gradually became clear that approximately 25% of these fungal species were new, undescribed species that awaited formal description and scientific recognition. This opens up new perspectives for biodiversity research by showing that many important ecological processes are driven by organisms we know next to nothing about,
We processed the DNA samples of 144 boreal lakes. We extracted the DNA of all samples and screened the material for fungi by DNA metabarcoding of fungal and universal markers. This allowed us to examine the influence of environmental parameters on the fungal community, and we were able to estimate the proportion of the early diverging fungal lineages and unknown fungi in lakes and even in watery permafrost regions. In addition, we subjected an extensive single lake to intense screening to investigate the vertical distribution of fungi within the lake. In doing so we found a biodiversity stratification of fungi along the depth gradient of the lake – taking a single sample from a lake will not be enough. We were frustrated to find many fungi that could not be identified at any meaningful taxonomic level at all. To remedy this, we devised a software tool that the scientific community can use to single out these unknown/new lineages for further examination and formal description. We further explored the metadata for available fungal DNA sequence data and found it to be severely wanting. We assembled the missing metadata by hosting an international workshop, and the results of the workshop were disseminated to the scientific community through the international DNA sequence databases. In the process we found an intriguing case of a hidden RNA gene in a set of fungal sequences, which warranted a separate scientific publication. We started to approach the new fungal lineages by cultivation in mixed-model communities from lakes, and we described a species from an early diverging fungal lineage (Nephridiophagidae) as new to science.
During the EU project we seized the opportunity to further work on aquatic fungi and the methods needed to characterize these fungi properly. We did important work improving the support for early diverging fungal lineages and aquatic fungi in the largest fungal reference DNA sequence database (UNITE). UNITE is the standard database for molecular identification of fungi, which guarantees that our improvements will automatically reach the scientific community at large. Molecular identification of aquatic fungi is now easier and more precise for everyone, owing to our project. Our frustration with the neglected nature of aquatic fungi lead us to write no less than three perspectives/review paper where we pointed out the bewildering diversity of water-associated fungi from various points of view. In total we were able to publish 14 open access scientific, peer-reviewed papers during this MSCA fellowship. Europe has for a long time lacked a research line on the early evolution of fungi, but we feel confident that our efforts and results are strong and noteworthy enough to stimulate further research on this topic on our continent.
A – Example of aquatic fungi recovered during the course of the MSCA project. B – 2015 field work