Climate change is altering Arctic ecosystem structure by changing weather patterns and reducing sea ice coverage. These changes are increasing light penetration into the Arctic Ocean that are forecasted to increase primary production; however, increased light can also induce photoinhibition and cause physiological stress in algae and phytoplankton that can favour disease development. Fungi are voracious parasites in many ecosystems that can modulate the flow of carbon through food webs, yet are poorly characterized in the marine environment. We provide the first data from any marine ecosystem in which fungi in the Chytridiomycota dominate fungal communities and are linked in their occurrence to light intensities and algal stress. Increased light penetration stresses ice algae and elevates disease incidence under reduced snow cover. Our results show that chytrids dominate Arctic marine fungal communities and have the potential to rapidly change primary production patterns with increased light penetration.
Fungi are important parasites of primary producers and nutrient cyclers in aquatic ecosystems. In the Pacific-Arctic domain, fungal parasitism is linked to light intensities and algal stress that can elevate disease incidence on algae and reduce diatom concentrations. Fungi are vastly understudied in the marine realm and knowledge of their function is constrained by the current understanding of fungal distribution and drivers on global scales. To investigate the spatial distribution of fungi in the western Arctic and sub-Arctic, we used high throughput methods to sequence 18S rRNA, cloned and sequenced 28S rRNA and microscopically counted chytrid-infected diatoms. We identified a broad distribution of fungal taxa predominated by Chytridiomycota and Dikarya. Phylogenetic analysis of our Chytridiomycota clones placed Arctic marine fungi sister to the order Lobulomycetales. This clade of fungi predominated in fungal communities under ice with low snowpack. Microscopic examination of fixed seawater and sea ice samples revealed chytrids parasitizing diatoms collected across the Arctic that notably infected 25% of a single diatom species in the Bering Sea. The Pezizomycotina comprised > 95% of eukaryotic sequence reads in Greenland, providing preliminary evidence for osmotrophs being a substitute for algae as the base of food webs.
Growing interest in understanding the relevance of marine fungi to food webs, biogeochemical cycling, and biological patterns necessitates establishing a context for interpreting future findings. To help establish this context, we summarize the diversity of cultured and observed marine planktonic fungi from across the world. While exploring this diversity, we discovered that only half of the known marine fungal species have a publicly available DNA locus, which we hypothesize will likely hinder accurate highthroughput sequencing classification in the future, as it does currently. Still, we reprocessed >600 high-throughput datasets and analyzed 4.9 × 10 9 sequences (4.8 × 10 9 shotgun metagenomic reads and 1.0 × 10 8 amplicon sequences) and found that every fungal phylum is represented in the global marine planktonic mycobiome; however, this mycobiome is generally predominated by three phyla: the Ascomycota, Basidiomycota, and Chytridiomycota. We hypothesize that these three clades are the most abundant due to a combination of evolutionary histories, as well as physical processes that aid in their dispersal. We found that environments with atypical salinity regimes (>5 standard deviations from the global mean: Red Sea, Baltic Sea, sea ice) hosted higher proportions of the Chytridiomycota, relative to open oceans that are dominated by Dikarya. The Baltic Sea and Mediterranean Sea had the highest fungal richness of all areas explored. An analysis of similarity identified significant differences between oceanographic regions. There were no latitudinal gradients of marine fungal richness and diversity observed. As more high-throughput sequencing data become available, expanding the collection of reference loci and genomes will be essential to understanding the ecology of marine fungi.
Recent molecular evidence suggests a global-distribution of marine fungi; however, the ecological relevance and corresponding biological contributions of fungi to marine ecosystems remains largely unknown. We assessed fungal biomass from the open Arctic Ocean by applying novel biomass conversion factors from cultured-isolates to environmental sterol and CARD-FISH data. We found an average of 16.54 nmol m -3 of ergosterol in sea ice and seawater, which corresponds to 1.74 mg C m -3 (444.56 mg C m -2 in seawater). Using Chytridiomycota-specific probes, we observed freeliving and particulate-attached cells that averaged 34.07 µg C m -3 in sea ice and seawater (11.66 mg C m -2 in seawater). Summed CARD-FISH and ergosterol values approximate 1.77 mg C m -3 in sea ice and seawater (456.23 mg C m -2 in seawater), which is similar to biomass estimates of other marine taxa generally considered integral to marine food webs and ecosystem processes. Using the GeoChip microarray, we detected evidence for fungal viruses within the Partitiviridae in sediment, as well as fungal genes involved in the degradation of biomass and the assimilation of nitrate. To bridge our observations of fungi on particulate and the detection of degradative genes, we germinated fungal conidia in zooplankton fecal pellets and grew fungal conidia after eight months incubation in sterile seawater. Ultimately, these data suggest that fungi could be as important in oceanic ecosystems as they are in freshwater environments. Significance Statement:The oceans cover 71% of the world's surface; however, the contributions of marine fungi to these environments remain a gap to understanding marine ecosystem processes and associated biogeochemical cycling. Here we provide the first biomass estimates of fungi from the Arctic Ocean, supplemented with a functional gene inventory, and experiment-based ecological data demonstrating putative niches occupied by fungi in the marine environment. We provide evidence that marine fungi comprise a comparable quantity of biomass relative to other taxonomic groups that are generally considered to be essential ecosystem components.
Fungi have evolved mechanisms to function in the harsh conditions of the Arctic Ocean and its adjacent seas. Despite the ecological and industrial potential of these fungi and the unique species discovered in the cold seas, Arctic marine fungi remain poorly characterised, with only 33 publications available to date. In this review, we present a list of 100 morphologically identified species of marine fungi detected in the Arctic. Independent molecular studies, applying Sanger or high-throughput sequencing (HTS), have detected hundreds of fungal operational taxonomic units (OTUs) in single substrates, with no evidence for decreased richness of marine fungi towards northern latitudes. The dominant fungal phyla may be substrate-specific, as sea-ice and seawater seem to host more Chytridiomycota and Basidiomycota than Ascomycota-dominated driftwood and sediments. Molecular studies have revealed the presence of the Chytridiomycota and Leotiomycetes in Arctic waters, with mounting evidence suggesting a significant role in nutrient and carbon cycling. The high detection frequency of Leotiomycetes is partly due to OTUs from marine
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