Giant Starship Elements Mobilize Accessory Genes in Fungal Genomes

Abstract

Accessory genes are variably present among members of a species and are a reservoir of adaptive functions. In bacteria, differences in gene distributions among individuals largely result from mobile elements that acquire and disperse accessory genes as cargo. In contrast, the impact of cargo-carrying elements on eukaryotic evolution remains largely unknown. Here, we show that variation in genome content within multiple fungal species is facilitated by Starships, a newly discovered group of massive mobile elements that are 110 kb long on average, share conserved components, and carry diverse arrays of accessory genes. We identified hundreds of Starship-like regions across every major class of filamentous Ascomycetes, including 28 distinct Starships that range from 27-393 kb and last shared a common ancestor ca. 400 mya. Using new long-read assemblies of the plant pathogen Macrophomina phaseolina, we characterize 4 additional Starships whose activities contribute to standing variation in genome structure and content. One of these elements, Voyager, inserts into 5S rDNA and contains a candidate virulence factor whose increasing copy number has contrasting associations with pathogenic and saprophytic growth, suggesting Voyager’s activity underlies an ecological trade-off. We propose that Starships are eukaryotic analogs of bacterial integrative and conjugative elements based on parallels between their conserved components and may therefore represent the first dedicated agents of active gene transfer in eukaryotes. Our results suggest that Starships have shaped the content and structure of fungal genomes for millions of years and reveal a new concerted route for evolution throughout an entire eukaryotic phylum.

Global patterns and rates of habitat transitions across the eukaryotic tree of life

“…These different gene contents may be due, at least in part, to lateral gene transfers (LGT) that could facilitate successful crossing of the salt barrier, as proposed for other environmental adaptations 68 – 73 . Interestingly, for two of the most frequently transitioning eukaryotic groups (diatoms and ascomycetes), it has been shown that gene transfer is an important driver of evolution 74 , 75 . However, the precise role of LGT in facilitating the crossing of the salt barrier remains unclear, as is our understanding of how protists in general acquire the necessary genes for osmoregulation.…”

The pangenome of the wheat pathogen Pyrenophora tritici-repentis reveals novel transposons associated with necrotrophic effectors ToxA and ToxB

“…Edge analysis and review of gene content within the 143-kb segment indicated target site duplications (or short direct repeats) at the edges and a tyrosine recombinase (gene_09853; DUF3435 domain) at the 5′ end, initially suggesting this element is a crypton [ 33 ]. Recently, however, a new class of large mobile elements called Starships have been defined [ 34 ]. An examination of other genes present within the transposon suggests that this element is also a Starship with many similarities, including the DUF3435 tyrosine recombinase ‘captain’, DUF3273 domains, ferric reductase, ankyrin repeats, heterokaryon incompatibility, NACHT nucleoside triphosphatase, and target site duplications (Fig.…”

“…An examination of other genes present within the transposon suggests that this element is also a Starship with many similarities, including the DUF3435 tyrosine recombinase ‘captain’, DUF3273 domains, ferric reductase, ankyrin repeats, heterokaryon incompatibility, NACHT nucleoside triphosphatase, and target site duplications (Fig. 4 B) [ 34 ]. A full list of genes present is available in Additional file 4 .…”

“…Fungi are known to display high variability in their genomes, and the ability of plant pathogenic species to gain virulence genes embedded in a ‘pathogenicity island’ and carried on supernumerary chromosomes that transfer horizontally as whole or in part is well described [ 36 ]. Recently, more reports have emerged on the ability of virulence genes to transfer on large transposons among plant pathogens [ 34 ]. Overall, the ability of pathogenic fungi to evolve rapidly to invade their hosts or cause outbreaks is illustrated through their ability to recombine, mutate, and shuffle their genetic components either vertically or horizontally.…”

Percepção sobre fungos em quintais urbanos de Benjamim Constant (Amazonas) e seus potenciais biotecnológicos

“…Estimativas sugerem que apenas 5-10% dos fungos existentes foram até então descobertos e descritos (Hawksworth, 2001). Neste sentido, muitos pesquisadores têm se dedicado à Micologia que, em suma, é o ramo da biologia especializado no estudo dos fungos: sistemática, taxonomia, fisiologia, morfologia, bioquímica, genética, toxicidade, biorremediação, aplicações biotecnológicas, dentre outras inúmeras linhas de atuação (Barbosa et al, 2012;Gluck-Thaler et al, 2022;Lacaz et al, 2002).…”