Diversity, composition, and functional interactions between the moss metabolome and fungal communities in Alaska

Megan Nickerson

Non-vascular plants, such as mosses (Bryophyta), are abundant and ecologically important members of the vegetation in boreal and Arctic ecosystems, which span an expansive area (>4 million km²) globally. In northern ecosystems, mosses play critical roles in regulating carbon and hydrological cycles. For example, the slow decomposition of Sphagnum mosses results in the formation of peat that sequesters large amounts of carbon. Slow rates of Sphagnum decomposition are attributed to abiotic factors, such as low temperatures and a lack of oxygen necessary for microbial decomposition. Sphagnum may also directly inhibit microbial decomposition through high cation exchange that acidifies the surrounding area and the production of antimicrobial metabolites. Increasing temperatures, especially in northern regions, are predicted to accelerate microbial decomposition, thereby releasing stored carbon into the atmosphere. Although recent studies have investigated the role of moss-associated bacteria and protists in shaping Sphagnum’s response to climate change, fungi are the primary microorganisms involved in lignocellulose decomposition. Despite this, the diversity, taxonomic composition, and functional roles of fungal communities in Sphagnum remain largely unknown. It has been predicted that Sphagnum harbors low fungal diversity due to metabolites that inhibit fungal colonization and decomposition; however, to date, this has not been empirically tested across multiple Sphagnum spp. and geographic locations. As previous studies of moss-associated fungi in boreal and Arctic regions have revealed that moss genera harbor higher fungal diversity in living tissues compared to co-occurring vascular plants, I hypothesized that Sphagnum also contains diverse fungal communities that may play a significant role in decomposition. To address this critical knowledge gap, I characterized fungal communities in the living and senescing tissues of Sphagnum and two other co-occurring mosses at four boreal sites in Alaska, using both traditional culture-based methods and culture-free high-throughput sequencing. From the same tissues, I employed liquid chromatography tandem mass spectrometry to characterize moss metabolites and used statistical approaches to assess the impact of moss chemistry on fungal communities. As predicted, Sphagnum living and senesced tissues harbored a similar diversity and taxonomic composition of fungi when compared to co-occurring moss genera Pleurozium and Aulacomnium. Metabolomes of all mosses also contained similar compound classes. However, examination of fungal species and individual metabolites revealed significant differences among moss genera, regardless of tissue type. Mosses with more similar metabolomes harbored more similar fungal communities, suggesting that moss fungal communities may be highly adapted to host metabolites, similar to patterns observed for symbionts of vascular plants. Next, I collected living and senescing tissues of three Sphagnum species, along with adjacent soils, at two additional sites in northern Alaska. Using similar microbiome and metabolome methods, I examined the relationship between fungal taxonomic shifts during decomposition and chemical changes to substrate complexity and composition. Rather than a linear process, my results are consistent with a model in which changes to the metabolome by early colonizing fungi in living tissues generates an interacting feedback loop that influences the presence of subsequent fungi. Unlike predictions based on litter decomposition, the taxonomic composition of moss fungal communities was not structured solely by substrate complexity or bioavailability. Lastly, I used in vitro assays of phylogenetically diverse moss-associated Ascomycota species isolated in Alaska to determine whether moss metabolites directly inhibit fungal growth. My results suggest moss-associated fungi are adapted to moss metabolites, which is consistent with microbiome and metabolome results from my field-collected samples. Although I observed differences among fungal species and with different compounds, overall, results show that the growth of moss-associated fungal species in vitro is not universally inhibited by polyphenolic compounds. Overall, the results of my dissertation reveal an unexpectedly high diversity of fungi in Sphagnum, consistent with observations from other boreal mosses. Furthermore, while the fungal composition in mosses is influenced by host chemistry, Sphagnum metabolites do not appear to inhibit fungal colonization or growth, even at higher concentrations. As such, moss-associated fungi, including numerous Ascomycota species, may play a greater role in Sphagnum decomposition than previously recognized. A greater understanding of the fungal diversity of Sphagnum and the potential for fungal-mediated moss decomposition is necessary, as increased microbial activity and carbon release into the atmosphere are predicted as northern ecosystems continue to warm at unprecedented rates.

Diversity, composition, and functional interactions between the moss metabolome and fungal communities in Alaska

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