Olga A Grum Grzhimaylo

Estimates suggest that more than 40-50% of the area of the northern hemisphere of our planet is covered by Sphagnum bogs, which act as a reservoir for storing planetary carbon stocks in peat, with polar and high mountain regions underlain by permafrost. In the boreal zone, permafrost also underlies some of the peatlands. Both the cold polar and high mountain regions, as well as the acidic flooded Sphagnum bogs, represent poly-extreme conditions for existence. However, even in these ecotopes, actively functioning microorganisms (bacteria, archaea, protists, and fungi) are known. In this work, I focused on studying the mycelial fungi of boreal peatlands, the Arctic, and Antarctica.

In peatlands, fungi mainly play an important role as decomposers of recalcitrant tissues of Sphagnum mosses, initiating this process. Fungi break down the most complex phenolic components into simpler ones, making them available to bacterial enzymes. Being mostly aerobic organisms, fungi are predominantly active in the upper aerated layers of peat, while in deeper peat deposits, the main role of decomposers shifts to anaerobic prokaryotic organisms. With global warming, the thawing of permafrost is occurring, resulting in the expansion of the area of boreal peatlands. This process is accompanied by the loss of thriving fungal species in permafrost and the activation of species that are preserved in frozen substrate as spores. At the same time, the upper layers of boreal peatlands are heating up and drying out, enhancing the activity of resident fungi. These transformations affect the intensity of global biogeochemical cycles, and therefore, the rate of peat accumulation and greenhouse gas emissions. Currently, the description of fungal communities in peatlands and permafrost soils is lacking. Furthermore, the issue with current understanding of fungal communities in permafrost and peat is that it is unknown which of the detected fungi are active and which are present as spores. Without information on the species composition of fungi in these locations and the extent of their activity, it is impossible to predict changes in the functioning of fungal communities and substance cycling under the impact of global warming.

The objectives of my dissertation were to describe the diversity of fungi in Sphagnum bogs located in the Arctic region on the coast of the White Sea, compare the obtained fungal communities with the fungal community of three Sphagnum bogs in the temperate zone, and analyze the existing literature on terrestrial mycelial fungi in the Arctic and Antarctica.

To expand the information on the species composition of fungi in boreal peat bogs, in Chapter 2, I present the results of the study of peat deposits and bottom sediments of five near-coastal peatlands. These peatlands are located at different elevations relative to sea level, and they were formed at different times after the retreat of the sea due to post-glacial land uplift from the White Sea. In this study, I used culture methods to identify fungi, so it is not possible to determine whether they are active or preserved as spores. In this chapter, I present a list of identified fungal species, a comparative characterization of the fungal communities of Sphagnum mosses and peat at different depths, as well as the studied peatlands. Marine fungal species were found in bottom sediments, while they were absent in peat deposits. The highest number of fungi and their diversity were found in the surface aerated layers of peatland, such as living and dying parts of Sphagnum, as well as at the maximum depth of the peat deposit (in the underlying rock), which can be explained by the leaching of fungal spores and their accumulation in waterproof underlying substrate.

The object of study in Chapter 3 was the brackish lake Kislo-Sladkoe, which is currently in the process of becoming isolated from the White Sea and gradually becoming peatified. In this work, as in the previous chapter, culture methods were used to identify fungi. The result of this study was the discovery of mosaicism in the fungal community in this ecosystem. I collected samples from different components of this lake, such as bottom mud from different depths, littoral deposits from the shore where periodic influx of seawater occurs, Sphagnum from the opposite shore where a freshwater stream flows into the lake and peatification has begun, as well as soil from the costal forest. These samples differed in pH and salinity values, and corresponding differences in fungal species composition were found.

In Chapter 4, I present a brief comparison of fungal communities of three boreal and three temperate Sphagnum peatlands. Culture methods were used in both regions, however, the methods of storing samples differed, which could have influenced the results. Nevertheless, extremely low similarity was noted in the fungal communities of northern and temperate peatlands at the species level. Strong differences in fungal communities are presumably explained by the climatic differences between these regions, as well as by different methodological approaches.

Chapter 5 provides a review dedicated to the description of terrestrial mycelial fungi of the Arctic and Antarctic regions. As a result of this research, I compiled a list of known fungi in polar regions, provided maps of their occurrences, analyzed the substrates of fungal discovery, compared methodological approaches, and attempted to determine the presence of endemic fungal species in the Arctic and Antarctic. I found that nearly 1300 species of mycelial fungi are known in polar regions, isolated from various substrates. In the Arctic, fungal species diversity is higher than in Antarctica, with approximately 20% of fungal species overlapping between the two regions. Different studies used different methods for collecting and storing specimens, fungal discovery, and identification. Therefore, it is very difficult to analyze results obtained using such diverse methods. Nevertheless, I showed that endemic species may be more prevalent in Antarctica compared to the Arctic. However, with increasing research in polar and high-altitude regions, a growing similarity in fungal species composition in these regions is being observed. The question of the presence of endemic fungal species in polar regions remains debatable.

Chapter 6 focuses on two isolates of the fungus species Psychrophilomyces antarctius, discovered in Antarctica and the Tibetan Plateau in 2015, and described as a new fungal species. We isolated it from samples of littoral deposits of Shokalsky Island (Kara Sea, Arctic), identified it based on morphology and four sequences of conservative genes, and conducted experimental work to determine the optimal values of temperature, pH, and salinity for growth of this fungus. We demonstrated that this fungus belongs to the species P. antarctius with the highest similarities in morphology, physiology, and DNA sequences. Thus, I discovered another fungal species shared between polar and high-altitude regions, confirming my hypothesis that with increasing research in these regions, differences in fungal communities are diminishing.

In Chapter 7, I discuss all the material of this thesis, as well as provide and discuss statistical processing. In main conclusions, I summarize the main questions of this thesis and possible future research directions. Additionally, I present unpublished results of an experiment showing the ability of over 200 tested fungal cultures from peatlands to decompose Sphagnum mosses. I found that fungi can be divided into three groups: those growing only on Sphagnum and actively decomposing its tissues, those growing on and around Sphagnum, and those growing around Sphagnum but not decomposing it.