Shared Signatures of Parasitism and Phylogenomics Unite Cryptomycota and Microsporidia

Abstract

Fungi grow within their food, externally digesting it and absorbing nutrients across a semirigid chitinous cell wall. Members of the new phylum Cryptomycota were proposed to represent intermediate fungal forms, lacking a chitinous cell wall during feeding and known almost exclusively from ubiquitous environmental ribosomal RNA sequences that cluster at the base of the fungal tree [1, 2]. Here, we sequence the first Cryptomycotan genome (the water mold endoparasite Rozella allomycis) and unite the Cryptomycota with another group of endoparasites, the microsporidia, based on phylogenomics and shared genomic traits. We propose that Cryptomycota and microsporidia share a common endoparasitic ancestor, with the clade unified by a chitinous cell wall used to develop turgor pressure in the infection process [3, 4]. Shared genomic elements include a nucleotide transporter that is used by microsporidia for stealing energy in the form of ATP from their hosts [5]. Rozella harbors a mitochondrion that contains a very rapidly evolving genome and lacks complex I of the respiratory chain. These degenerate features are offset by the presence of nuclear genes for alternative respiratory pathways. The Rozella proteome has not undergone major contraction like microsporidia; instead, several classes have undergone expansion, such as host-effector, signal-transduction, and folding proteins.

Evolution of a morphological novelty occurred before genome compaction in a lineage of extreme parasites

“…A phylogenetic analysis of 53 conserved concatenated genes supports a topology in which microsporidia is the most basal branch in the fungal tree (5). Another phylogenetic analysis based on 200 genes included the endoparasite Rozella allomycis, a representative of the recently discovered basal fungal lineage Cryptomycota (15,16), and placed microsporidia and Cryptomycota together on the most basal fungal branch (4). One of the shared genomic elements between microsporidia and R. allomycis is the nucleotide transporter that is used by microsporidia for stealing energy in the form of ATP from their hosts; Significance Intracellular obligate parasitism results in extreme adaptations, whose evolutionary history is difficult to understand, because intermediate forms are hardly ever found.…”

“…There are more than 1,200 described microsporidia species (2), with several having an economic impact by causing disease in animals such as fish and honey bees, and are a problem to human health, in particular since the AIDS pandemic. Microsporidia are currently placed on an ancestral branch within the fungi, although this placement has only recently been worked out, due to the absence of clear morphological and physiological connections to other eukaryotes and the profound changes resulting from adaptations to an intracellular lifestyle (3)(4)(5)(6). The evolutionary history of microsporidia is marked by the loss of several eukaryotic features, such as mitochondria (7), a typical Golgi apparatus (8), a flagellum (3), and the evolutionary innovation of an infection apparatus, the polar tube.…”

Miniaturized mitogenome of the parasitic plant Viscum scurruloideum is extremely divergent and dynamic and has lost all nad genes

“…With the notable exceptions of four lineages, all respiring eukaryotes contain complex I, a multisubunit, rotenone-sensitive NADH dehydrogenase that is encoded by 5-12 mitochondrial genes and a few dozen nuclear nad genes. The four exceptions, in which all mitochondrial and nuclear nad genes have vanished, include two distinct lineages of yeasts (28), the cryptomycotan fungus Rozella (29), and the lineage comprising dinoflagellates, apicomplexans, Chromera, and Oxyrrhis (30). That these are all unicellular makes the case in Viscum particularly notable.…”

“…The gene repertoire of the Viscum mitogenome may be so specialized to parasitic life that, unlike all other multicellular organisms investigated so far, it can survive without a mitochondrial-encoded respiratory complex I. Recently the intracellular parasitic fungus Rozella allomycis also was found to harbor a very rapidly evolving genome that lacks complex I of the respiratory chain (29). This discovery raises the tantalizing possibility that shared genomic signatures of parasitism may be present in mitogenomes both within and beyond the bounds of the angiosperm clade.…”

A genome Tree of Life for the Fungi kingdom

“…The current narrative is that the very small genome sizes of Microsporidia have resulted from one or more steps of extreme reduction of much larger genomes of fungal origin (16). Most of these "evidences" are based on the sequence similarity of the proteins coded by one or limited number of genes (4,5,17,18). However, the proteome tree suggests another narrative that the genomes of the Microsporidia may have a protistan origin rather than fungal origin [marked "(a)" in Figs.…”