The mitochondrial alternative oxidase Aox1 is needed to cope with respiratory stress but dispensable for pathogenic development in Ustilago maydis

Abstract

The mitochondrial alternative oxidase is an important enzyme that allows respiratory activity and the functioning of the Krebs cycle upon disturbance of the respiration chain. It works as a security valve in transferring excessive electrons to oxygen, thereby preventing potential damage by the generation of harmful radicals. A clear biological function, besides the stress response, has so far convincingly only been shown for plants that use the alternative oxidase to generate heat to distribute volatiles. In fungi it was described that the alternative oxidase is needed for pathogenicity. Here, we investigate expression and function of the alternative oxidase at different stages of the life cycle of the corn pathogen Ustilago maydis (Aox1). Interestingly, expression of Aox1 is specifically induced during the stationary phase suggesting a role at high cell density when nutrients become limiting. Studying deletion strains as well as overexpressing strains revealed that Aox1 is dispensable for normal growth, for cell morphology, for response to temperature stress as well as for filamentous growth and plant pathogenicity. However, during conditions eliciting respiratory stress yeast-like growth as well as hyphal growth is strongly affected. We conclude that Aox1 is dispensable for the normal biology of the fungus but specifically needed to cope with respiratory stress.

Hypoxia Promotes Immune Evasion by Triggering β-Glucan Masking on the Candida albicans Cell Surface via Mitochondrial and cAMP-Protein Kinase A Signaling

“…AOX1A and AOX1B are nonsynonymous alleles which encode alternative oxidases that protect the C. albicans mitochondrion against oxidative damage ( 60 – 62 ), as do their homologues in other fungi and plants ( 63 , 64 ). We observed that, like pop2 Δ cells, a C. albicans aox1A Δ/ aox1B Δ (hereafter aox1 Δ) mutant that lacks both isoforms of Aox1, display significantly enhanced β-glucan masking in response to hypoxia compared to the wild-type control ( Fig.…”

“…Normoxic aox1 Δ cells displayed high basal levels of β-glucan exposure, relative to the wild-type control ( Fig. 6 ), potentially because of abnormally high levels of mitochondrial ROS ( 60 – 64 ).…”

Alternative Oxidase: A Potential Target for Controlling Aflatoxin Contamination and Propagation of Aspergillus flavus

“…Furthermore, aflatoxin synthesis requires considerable amounts of ATP and NADPH (Yabe and Nakajima, 2004). However, after the initial growth phase, the energy demand of fungal cells is reduced and carbon catabolism is inhibited through oxidative phosphorylation (Cárdenas-Monroy et al, 2017;Molnár et al, 2018a). To maintain cellular homeostasis, fungal cells may rely on alternative respiratory pathways for reoxidation of NADH for aflatoxin synthesis without concomitant ATP production.…”

Fungal seed pathogens of wild chili peppers possess multiple mechanisms to tolerate capsaicinoids

“…Alternative oxidases have been described in the filamentous fungi Neurospora crassa (Descheneau et al 2005), Aspergillus fumigatus (Tudella et al 2004), Fusarium oxysporom (Pereira et al 1997) and others. In fungi such as Ustilago maydis, the alternative oxidase is not necessary for normal growth, but confers a fitness advantage in the presence of respiratory stress (Cárdenas-Monroy et al 2017). Fungi that associate with spicy chili pepper fruits experience a substantial degree of respiratory stress induced by capsaicinoids, but that stress may be alleviated by an alternative oxidase.…”