Generation, Transfer, and Loss of Alternative Oxidase Paralogues in the <i>Aspergillaceae</i> Family
2023
Michel Flipphi | Alexandra Márton | Vivien Bíró | Norbert Ág | Erzsébet Sándor | Erzsébet Fekete | Levente Karaffa
Alternative oxidase (Aox) is a terminal oxidase operating in branched electron transport. The activity correlates positively with overflow metabolisms in certain <i>Aspergilli</i>, converting intracellular glucose by the shortest possible path into organic acids, like citrate or itaconate. Aox is nearly ubiquitous in fungi, but <i>aox</i> gene multiplicity is rare. Nevertheless, within the family of the <i>Aspergillaceae</i> and among its various species of industrial relevance—<i>Aspergillus niger</i>, <i>A. oryzae</i>, <i>A. terreus</i>, <i>Penicillium rubens</i>—paralogous <i>aox</i> genes coexist. Paralogous genes generally arise from duplication and are inherited vertically. Here, we provide evidence of four independent duplication events along the lineage that resulted in <i>aox</i> paralogues (<i>aoxB</i>) in contemporary <i>Aspergillus</i> and <i>Penicillium</i> taxa. In some species, three <i>aox</i> genes are co-expressed. The origin of the <i>A. niger</i> paralogue is different than that of the <i>A. terreus</i> paralogue, but all paralogous clades ultimately arise from ubiquitous <i>aoxA</i> parent genes. We found different patterns of uncorrelated gene losses reflected in the <i>Aspergillus</i> pedigree, albeit the original <i>aoxA</i> orthologues persist everywhere and are never replaced. The loss of acquired paralogues co-determines the contemporary <i>aox</i> gene content of individual species. In <i>Aspergillus calidoustus</i>, the two more ancient paralogues have, in effect, been replaced by two <i>aoxB</i> genes of distinct origins.
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