Phylogenomics including new sequence data of phytoplankton-infecting chytrids reveals multiple independent lifestyle transitions across the phylum.

Parasitism is the most common lifestyle on Earth and has emerged many times independently across the eukaryotic tree of life. It is frequently found among chytrids (Chytridiomycota), which are early-branching unicellular fungi that feed osmotrophically via rhizoids as saprotrophs or parasites. Chytrids are abundant in most aquatic and terrestrial environments and fulfil important ecosystem functions. As parasites, they can have significant impacts on host populations. They cause global amphibian declines and influence the Earth's carbon cycle by terminating algal blooms. To date, the evolution of parasitism within the chytrid phylum remains unclear due to the low phylogenetic resolution of rRNA genes for the early diversification of fungi, and because few parasitic lineages have been cultured and genomic data for parasites is scarce. Here, we combine transcriptomics, culture-independent single-cell genomics and a phylogenomic approach to overcome these limitations. We newly sequenced 29 parasitic taxa and combined these with existing data to provide a robust backbone topology for the diversification of Chytridiomycota. Our analyses reveal multiple independent lifestyle transitions between parasitism and saprotrophy among chytrids and multiple host shifts by parasites. Based on these results and the parasitic lifestyle of other early-branching holomycotan lineages, we hypothesise that the chytrid last common ancestor was a parasite of phytoplankton.

Single-cell genomics reveals new rozellid lineages and supports their sister relationship to Microsporidia.

The phylum Rozellomycota has been proposed for a group of early-branching holomycotan lineages representing obligate parasites and hyperparasites of zoosporic fungi, oomycotes or phytoplankton. Given their predominantly intracellular lifestyle, rozellids are typically known from environmental ribosomal DNA data, except for the well-studied Rozella species. To date, the phylogenetic relationship between rozellids and microsporidians (Microsporidia) is not fully understood and most reliable hypotheses are based on phylogenomic analyses that incorporate the only publicly available rozellid genome of Rozella allomycis. Here, we provide genomic data of three new rozellid lineages obtained by single-cell sequencing from environmental samples and show with a phylogenomic approach that rozellids form a monophyletic group that is sister to microsporidians, corroborating the previously proposed phylum Rozellomycota. Whereas no mitochondrial genes coding for the respiratory Complex I could be found, we discovered a gene coding for a nucleotide phosphate transporter in one of the three draft genomes. The scattered absence of Complex I genes and scattered presence of nucleotide transporter genes across diverse microsporidian and rozellid lineages suggest that these adaptations to a parasitic lifestyle, which reduce the parasite's capability to synthesize ATP but enables it to steal ATP from its host, evolved independently in microsporidians and rozellids.

Biogeographic gradients of picoplankton diversity indicate increasing dominance of prokaryotes in warmer Arctic fjords.

Climate change is opening the Arctic Ocean to increasing human impact and ecosystem changes. Arctic fjords, the region's most productive ecosystems, are sustained by a diverse microbial community at the base of the food web. Here we show that Arctic fjords become more prokaryotic in the picoplankton (0.2-3 µm) with increasing water temperatures. Across 21 fjords, we found that Arctic fjords had proportionally more trophically diverse (autotrophic, mixotrophic, and heterotrophic) picoeukaryotes, while subarctic and temperate fjords had relatively more diverse prokaryotic trophic groups. Modeled oceanographic connectivity between fjords suggested that transport alone would create a smooth gradient in beta diversity largely following the North Atlantic Current and East Greenland Current. Deviations from this suggested that picoeukaryotes had some strong regional patterns in beta diversity that reduced the effect of oceanographic connectivity, while prokaryotes were mainly stopped in their dispersal if strong temperature differences between sites were present. Fjords located in high Arctic regions also generally had very low prokaryotic alpha diversity. Ultimately, warming of Arctic fjords could induce a fundamental shift from more trophic diverse eukaryotic- to prokaryotic-dominated communities, with profound implications for Arctic ecosystem dynamics including their productivity patterns.