Genomic analysis reveals cryptic diversity in aphelids and sheds light on the emergence of Fungi

Mikhailov, Kirill V.; Karpov, Sergey A.; Letcher, Peter M.; Lee, Philip A.; Logacheva, Maria D.; Penin, Aleksey A.; Nesterenko, Maksim A.; Pozdnyakov, Igor R.; Potapenko, Evgenii; Sherbakov, D. Yu.; Panchin, Yu. V.; Aleoshin, Vladimir V.

doi:10.1016/j.cub.2022.08.071

Cited by 15 publications

(29 citation statements)

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“…Mikhailov et al [ 18 ] recently published the genome of A. protococcorum and Amoeboaphelidium occidentale . The ancestor of Aphelidiomycota was flagellated, and in some cases, a reduction in flagellum occurred as in A. occidentale and A. protococcorum , while, in other species, it was retained (e.g., P. tribonematis ) [ 18 ].…”

Section: Resultsmentioning

confidence: 99%

Tubulin Polymerization Promoting Proteins (TPPPs) of Aphelidiomycota: Correlation between the Incidence of p25alpha Domain and the Eukaryotic Flagellum

Orosz

2023

JoF

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The seven most early diverging lineages of the 18 phyla of fungi are the non-terrestrial fungi, which reproduce through motile flagellated zoospores. There are genes/proteins that are present only in organisms with flagellum or cilium. It was suggested that TPPP-like proteins (proteins containing at least one complete or partial p25alpha domain) are among them, and a correlation between the incidence of the p25alpha domain and the eukaryotic flagellum was hypothesized. Of the seven phyla of flagellated fungi, six have been known to contain TPPP-like proteins. Aphelidiomycota, one of the early-branching phyla, has some species (e.g., Paraphelidium tribonematis) that retain the flagellum, whereas the Amoeboaphelidium genus has lost the flagellum. The first two Aphelidiomycota genomes (Amoeboaphelidium protococcorum and Amoeboaphelidium occidentale) were sequenced and published last year. A BLASTP search revealed that A. occidentale does not have a TPPP, but A. protococcorum, which possesses pseudocilium, does have a TPPP. This TPPP is the ‘long-type’ which occurs mostly in animals as well as other Opisthokonta. P. tribonematis has a ‘fungal-type’ TPPP, which is found only in some flagellated fungi. These data on Aphelidiomycota TPPP proteins strengthen the correlation between the incidence of p25alpha domain-containing proteins and that of the eukaryotic flagellum/cilium.

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Section: Resultsmentioning

confidence: 99%

Tubulin Polymerization Promoting Proteins (TPPPs) of Aphelidiomycota: Correlation between the Incidence of p25alpha Domain and the Eukaryotic Flagellum

Orosz

2023

JoF

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“…The 540 HGs included all gene families previously reported to be lost in EDF: subunits of WASH and VASP (lost in LUFA), WAVE 14 , the CyclOP 26 light sensing system (lost after Blastocladiomycota), flagellar genes 22 (lost across the branching of Chytridiomycota, Blastocladiomycota, and Olpidium , see Supplementary Data 3), cobalamin synthesis proteins 25 , the replacement of the E2F cell cycle regulator by the SBF complex 24 . However, different taxon sampling updated the inferred time point of these loss events in several cases.…”

Section: Resultsmentioning

confidence: 99%

“…The retention of protist genes and the lack of clear synapomorphies for fungi blur lines between fungi and related protists and may explain why the taxonomic limits of fungi have been challenging to define and are still a matter of debate 14 . In other words, taxonomically defined Fungi don't match with any clade we could define, based on gene content, as 'genomic Fungi', a situation that would not change with the exclusion of Opisthosporidia from fungi.…”

Section: Discussionmentioning

confidence: 99%

“…For highly duplicated gene groups, a dominant functional signal was related to extracellular proteins (e.g. secreted CAZymes) and transporters which can be linked to the transition from phagotrophy to osmotrophy and the subsequent sophistication of extracellular digestive and uptake mechanisms 11,14,15,20,34,48 . These also explained a considerable portion of the duplication events in the chytrid and Dikarya ancestors, though it should be noted that a myriad other functions were also represented among the most expanding families.…”

Section: Discussionmentioning

confidence: 99%

“…Irrespective of significant flux in the taxonomic definition of Fungi 11 , how the earliest fungal ancestors are characterised and how they evolved from a unicellular opisthokont ancestor has been the subject of intense research. Reconstructions of the last universal fungal ancestor (LUFA) became more and more nuanced with the inclusion of newly discovered and/or classified early diverging lineages 8,10,[12][13][14][15][16] . These results contributed to our current understanding of LUFA as a unicellular phagotrophic parasite of microalgae, possessing motile cell stages with amoeboid and flagellar motility and a chitinous cell wall, at least in part of its life cycle 9,15 .…”

Section: Introductionmentioning

confidence: 99%

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

Merényi

Krizsán

Sahu

et al. 2022

Preprint

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Fungi are among the most ecologically important heterotrophs that have radiated into most niches on Earth and fulfil key ecological services. However, despite intense interest in their origins, major genomic trends characterising the evolutionary route from a unicellular opisthokont ancestor to derived multicellular fungi remain poorly known. Here, we reconstructed gene family evolution across 123 genomes of fungi and relatives and show that a dominant trend in early fungal evolution has been the gradual shedding of protist genes and highly episodic innovation via gene duplication. We find that the gene content of early-diverging fungi is protist-like in many respects, owing to the conservation of protist genes in early fungi. While gene loss has been constant and gradual during early fungal evolution, our reconstructions show that gene innovation showed two peaks. Gene groups with the largest contribution to genomic change included extracellular proteins, transcription factors, as well as ones linked to the coordination of nutrient uptake with growth, highlighting the transition to a sessile osmotrophic feeding strategy and subsequent lifestyle evolution as important elements of early fungal evolution. Taken together, this work provided a highly resolved genome-wide catalogue of gene family changes across fungal evolution. This suggests that the genome of pre-fungal ancestors may have been transformed into the archetypal fungal genome by a combination of gradual gene loss, turnover and two large duplication events rather than by abrupt changes, and consequently, that the taxonomically defined fungal kingdom does not represent a genomically uniform assemblage of extant species characterized by diagnostic synapomorphies.

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Marine parasite Protaphelidium rhizoclonii gen. et sp. nov. designates the basal environmental cluster at the aphelid phylogenetic tree

Seliuk,

Karpov

2024

Mycol Progress

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Genomic analysis reveals cryptic diversity in aphelids and sheds light on the emergence of Fungi

Cited by 15 publications

References 120 publications

Tubulin Polymerization Promoting Proteins (TPPPs) of Aphelidiomycota: Correlation between the Incidence of p25alpha Domain and the Eukaryotic Flagellum

Tubulin Polymerization Promoting Proteins (TPPPs) of Aphelidiomycota: Correlation between the Incidence of p25alpha Domain and the Eukaryotic Flagellum

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

Marine parasite Protaphelidium rhizoclonii gen. et sp. nov. designates the basal environmental cluster at the aphelid phylogenetic tree

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