Mitochondrial genome, comparative analysis and evolutionary insights into the entomopathogenic fungus Hirsutella thompsonii

Abstract

Nuclear genomes of two isolates of Hirsutella thompsonii, a pathogen causing epizootics among mites, have been reported; in contrast, its mitochondrial genome (mitogenome) has remained unknown, limiting our understanding of its evolution. Herein, we annotated the first complete mitogenome of H. thompsonii, which encoded all standard fungal mitochondrial genes plus three free-standing ORFs. Transcriptional analyses validated the expression of most conserved genes and revealed some interesting transcription patterns of mitochondrial genes. Phylogenetic analyses confirmed its placement in Ophiocordycipitaceae. Comparison of five different isolates originally collected from different locations revealed mitogenome size variations (60.3-66.4 kb) mainly due to different numbers of introns. A total of 15 intron loci were identified, with 11 existing in all 5 isolates and 4 showing presence/absence dynamics. These introns were most likely obtained through horizontal transfer from other fungal organisms. Those common introns might have been in H. thompsonii mitogenomes since the divergence of the fungus from its putative sister species H. minnesotensis, whereas those dynamic introns might have experienced 1-2 gain or loss events. We also detected evidence of degeneration for some introns. Overall, our study shed new insights into the mitochondrial evolution of the acaropathogenic fungus H. thompsonii.

The complete mitochondrial genome of the Chan‐hua fungus Isaria cicadae: a tale of intron evolution in Cordycipitaceae

“…These introns were most likely obtained by horizontal transfer from related fungal species (Supporting Information Table S6), while evidence of degeneration was also obvious for several introns. Similar results were also documented in many other fungi (Zhang et al ., ; Wang et al ., ). Mitochondrial introns are sometimes referred to as selfish genetic elements since they seem not to benefit host genomes and thus tend to degenerate rapidly due to a lack of natural selection (Edgell, ).…”

“…Mobile introns and HE‐encoding genes (HEGs) are neutral elements that go through a cycle of intron invasion, followed by ORF degeneration resulting in both ORF and possibly intron loss (Goddard and Burt, ). This explains why many studies (including the current study) detected extensive presence/absence variations and widespread horizontal transfer for mitochondrial introns (Zhang et al ., ; Wang et al ., ). Group I introns mobilize via intron homing powered by their own encoded HEs after horizontal transfer or via reverse splicing through an RNA intermediate (Belfort and Perlman, ).…”

Genome streamlining via complete loss of introns has occurred multiple times in lichenized fungal mitochondria

“…The extent of mitochondrial genome reduction varies substantially among taxa and can even vary between closely related sister species (Dibb, 1993;Jo & Choi, 2015;Lynch, Koskella, & Schaack, 2006;Signorovitch, Buss, & Dellaporta, 2007;Simmons et al, 2015;Wang, Zhang, Li, & Zhang, 2018). Bilateral metazoan mitochondrial genomes are highly consistent in size (16-20 kbp in length), usually contain the same 37 coding features, and lack introns or retrotransposable elements (Beagley, Okada, & Wolstenholme, 1996;Saccone, Giorgi, Gissi, Pesole, & Reyes, 1999).…”

“…Intron presence is well established in fungal mitochondrial genomes, but can vary widely among taxa (Giroux et al, 1994;Guha, Wai, Mullineux, & Hausner, 2017;Jeffares et al, 2006;Logsdon, 1998). Variation in intron number, which can occur even between different populations or strains of the same species, has the potential for widespread implications including impacting genome size and gene regulation or expression through alternative splicing mechanisms (Dibb, 1993;Jo & Choi, 2015;Lynch et al, 2006;Simmons et al, 2015;Wang et al, 2018). Among fungi, species can vary remarkably in intron content as well as genome size (Hensgens, Bonen, Haan, Horst, & Grivell, 1983;van der Veen et al, 1986;Fink, 1987;Derr, Strathern, & Garfinkel, 1991;Nielsen, Friedman, Birren, Burge, & Galagan, 2004;Guha et al, 2017;Wang et al, 2018;e.g., 18.9 kbp in Schizosaccharomyces pombe; Anziano, Perlman, Lang, & Wolf, 1983 and 235 kbp in Rhizoctonia solani; Losada et al, 2014).…”

“…Variation in intron number, which can occur even between different populations or strains of the same species, has the potential for widespread implications including impacting genome size and gene regulation or expression through alternative splicing mechanisms (Dibb, 1993;Jo & Choi, 2015;Lynch et al, 2006;Simmons et al, 2015;Wang et al, 2018). Among fungi, species can vary remarkably in intron content as well as genome size (Hensgens, Bonen, Haan, Horst, & Grivell, 1983;van der Veen et al, 1986;Fink, 1987;Derr, Strathern, & Garfinkel, 1991;Nielsen, Friedman, Birren, Burge, & Galagan, 2004;Guha et al, 2017;Wang et al, 2018;e.g., 18.9 kbp in Schizosaccharomyces pombe; Anziano, Perlman, Lang, & Wolf, 1983 and 235 kbp in Rhizoctonia solani; Losada et al, 2014). However, the study of intron evolution in fungi has been limited primarily to nonlichenized systems (Derr et al, 1991;Fink, 1987;Guha et al, 2017;Hensgens et al, 1983;Nielsen et al, 2004;van der Veen et al, 1986), despite the fact that tens of thousands of species of fungi are lichenized and have symbiotic lifestyles (Hawksworth & Hill, 1984).…”