Divergent genomic trajectories predate the origin of animals and fungi

Abstract

Animals and fungi have radically distinct morphologies, yet both evolved within the same eukaryotic supergroup: Opisthokonta1,2. Here we reconstructed the trajectory of genetic changes that accompanied the origin of Metazoa and Fungi since the divergence of Opisthokonta with a dataset that includes four novel genomes from crucial positions in the Opisthokonta phylogeny. We show that animals arose only after the accumulation of genes functionally important for their multicellularity, a tendency that began in the pre-metazoan ancestors and later accelerated in the metazoan root. By contrast, the pre-fungal ancestors experienced net losses of most functional categories, including those gained in the path to Metazoa. On a broad-scale functional level, fungal genomes contain a higher proportion of metabolic genes and diverged less from the last common ancestor of Opisthokonta than did the gene repertoires of Metazoa. Metazoa and Fungi also show differences regarding gene gain mechanisms. Gene fusions are more prevalent in Metazoa, whereas a larger fraction of gene gains were detected as horizontal gene transfers in Fungi and protists, in agreement with the long-standing idea that transfers would be less relevant in Metazoa due to germline isolation3–5. Together, our results indicate that animals and fungi evolved under two contrasting trajectories of genetic change that predated the origin of both groups. The gradual establishment of two clearly differentiated genomic contexts thus set the stage for the emergence of Metazoa and Fungi.

Taxonomic vs genomic fungi: contrasting evolutionary loss of protistan genomic heritage and emergence of fungal novelties

“…Taken together, our analyses revealed that early-diverging fungi possess a large number of HGs shared specifically with protists, and that these were gradually lost during evolution. The broad conservation of protist HGs may explain the morphological and genetic similarities between EDF and protists reported in previous studies 16,23,24,31,32 and also clarifies why the genome content of fungi reflects that of ancestral opisthokonts more than metazoan gene content does 33 . However, our data revealed that the retention of protist genes is not restricted to certain gene families, but is a genomewide trend in early-diverging fungi.…”

“…We think this explains why EDF gravitate towards protists in gene content-based analyses (See Fig. 1) and provides a genomewide explanation for sporadic evidence for the similarity of EDFs to protists from analyses of single genes 24,25 , individual genomes 33 or TF-omes 45 . At the same time, we detected a limited number of gene families that could be considered synapomorphic for fungi, in agreement with previous conjectures on the lack of synapomorphies in the kingdom 11,22 .…”

A highly contiguous genome assembly reveals sources of genomic novelty in the symbiotic fungusRhizophagus irregularis

“…Similarly in plants, the genetic basis for symbiont perception, nodule organogenesis and nitrogen-fixation genes already existed in the common ancestor of nitrogen-fixing legumes, and diversified in downstream nitrogen-fixing lineages (Libourel et al, 2022). Such macroevolutionary transitions punctuate the eukaryotic tree of life, where the acquisition of new molecular functions accompanies major evolutionary and ecological transitions, but precedes divergence and lifestyle specialisation in downstream lineages (Domazet-Lošo et al, 2022; Ocana-Pallares et al, 2022).…”

Evolution and phylogenetic distribution ofendo-α-mannosidase

“…In none of the GH99 sequences from CRuMS (4 taxa sampled) Y189 was present, but a significant proportion (4 sequences, 27%) of hits from Amoebozoa have this feature (Supplementary File S11). Within Obazoa, a sister clade to Amoebozoa, only Opisthokonta retained Y189 and among the opisthokonts, the only nucletmycean that contains it is the recently sequenced Parvularia atlantis 46 . No true fungi possess the GH99 domain.…”