Evolution and codon usage bias of mitochondrial and nuclear genomes in Aspergillus section Flavi

Abstract

The fungal genus Aspergillus contains a diversity of species divided into taxonomic sections of closely related species. Section Flavi contains 33 species, many of industrial, agricultural, or medical relevance. Here, we analyze the mitochondrial genomes (mitogenomes) of 20 Flavi species--including 18 newly assembled mitogenomes--and compare their evolutionary history and codon usage bias (CUB) patterns to their nuclear counterparts. CUB refers to variable frequencies of synonymous codons in coding DNA and is shaped by a balance of neutral processes and natural selection. All mitogenomes were circular DNA molecules with highly conserved gene content and order. As expected, genomic content, including GC content, and genome size differed greatly between mitochondrial and nuclear genomes. Phylogenetic analysis based on 14 concatenated mitochondrial genes predicted evolutionary relationships largely consistent with those predicted by a phylogeny constructed from 2,422 nuclear genes. Comparing similarities in interspecies patterns of CUB between mitochondrial and nuclear genomes showed that species grouped differently by patterns of CUB depending on whether analyses were performed using mitochondrial or nuclear relative synonymous usage values. We found that patterns of CUB at gene-level are more similar between mitogenomes of different species than the mitogenome and nuclear genome of the same species. Finally, we inferred that, although most genes--both nuclear and mitochondrial--deviated from the neutral expectation for codon usage, mitogenomes were not under translational selection while nuclear genomes were under moderate translational selection. These results contribute to the study of mitochondrial genome evolution in filamentous fungi.