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Abstract
Reductions in genome size and complexity are a hallmark of obligate symbioses. The mitochondrial genome displays clear examples of these reductions, with the ancestral alpha‐proteobacterial genome size and gene number having been reduced by orders of magnitude in most descendent modern mitochondrial genomes. Here, we examine patterns of mitochondrial evolution specifically looking at intron size, number, and position across 58 species from 21 genera of lichenized Ascomycete fungi, representing a broad range of fungal diversity and niches. Our results show that the cox1gene always contained the highest number of introns out of all the mitochondrial protein‐coding genes, that high intron sequence similarity (>90%) can be maintained between different genera, and that lichens have undergone at least two instances of complete, genome‐wide intron loss consistent with evidence for genome streamlining via loss of parasitic, noncoding DNA, in Phlyctis boliviensisand Graphis lineola. Notably, however, lichenized fungi have not only undergone intron loss but in some instances have expanded considerably in size due to intron proliferation (e.g., Alectoria fallacina and Parmotrema neotropicum), even between closely related sister species (e.g., Cladonia). These results shed light on the highly dynamic mitochondrial evolution that is occurring in lichens and suggest that these obligate symbiotic organisms are in some cases undergoing recent, broad‐scale genome streamlining via loss of protein‐coding genes as well as noncoding, parasitic DNA elements.
Highlights
Genome expansions and contractions are prominent, repeated oc‐ currences across the tree of life, but the underlying mechanisms and selective regimes driving these changes are often unclear, limiting our ability to understand commonalities and differences across major domains (Adams & Palmer, 2003; Gray, Burger, & Lang, 1999; Jeffares, Mourier, & Penny, 2006; Khachane, Timmis, & Santos, 2007)
We documented differences in the number and variabil‐ ity of introns within 21 genera of lichens that are on par with the total variation present among major subdomains of the tree of life, such as metazoa, fungi, and plants
Previous research has demonstrated that intron number is variable between different species of nonli‐ chenized Ascomycete fungi (e.g., S. cerevisiae is relatively intron‐poor in comparison with Aspergillus nidulans; Paquin et al, 1997; Nielsen et al, 2004) and can drive major differences in genome size in these organisms (Sandor, Zhang, & Xu, 2018)
Summary
Genome expansions and contractions are prominent, repeated oc‐ currences across the tree of life, but the underlying mechanisms and selective regimes driving these changes are often unclear, limiting our ability to understand commonalities and differences across major domains (Adams & Palmer, 2003; Gray, Burger, & Lang, 1999; Jeffares, Mourier, & Penny, 2006; Khachane, Timmis, & Santos, 2007). Group I introns typically encode for homing endonucleases (HEGs) types LAGLIDADG and GIY‐YIG, while group II introns usually encode for reverse transcriptase genes (RT) (Lang, Laforest, & Burger, 2007) These genetic elements and other retrotransposable elements are often considered selfish as they pose no obvious value to their host genome (Edgell, Chalamcharla, & Belfort, 2011). Because of their frequent replication and transposition throughout the ge‐ nome, these genetic elements have the capability of introducing mutations within the host genome upon their insertion (Cambareri, Foss, Rowtree, Selker, & Kinsey, 1996; Nagy & Chandler, 2004). We (a) re‐ cord genome‐wide intron presence and sequence similarity in an evolutionary framework by inferring gains and losses through
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