Peroxisomal metabolism is regulated by an oxygen‐recognition system through organelle crosstalk between the mitochondria and peroxisomes

Abstract

In the present study using Pichia methanolica, it was found that expressions of methanol-metabolic enzymes were strictly regulated by the presence of oxygen, and that induction of alcohol oxidase (AOD) isozymes was completely dependent on oxygen concentrations. A proportion of AOD-isozyme species responded to oxygen conditions, e.g. in a low oxygen condition, Mod1p was dominant, but with an increase in the oxygen concentration, the ratio of Mod2p increased. The K m value of Mod1p for oxygen was ca. one-seventh lower than that of Mod2p (0.47 and 3.51 mM, respectively). This shows that Mod1p is suitable at low oxygen concentrations and Mod2p at high oxygen concentrations. Also, zymogram changes for AOD isozymes were observed by inhibition of respiratory chain activity. These indicated that P. methanolica has the ability to recognize oxygen conditions and the respiratory chain should participate in the sensor for available oxygen. These facts indicate that there is organelle crosstalk between mitochondria and peroxisomes through nucleus gene regulation in order to control the consumption balance of available oxygen between the mitochondrial respiratory chain and peroxisomal AODs.

Peroxisomal ABC transporters and β-oxidation during the life cycle of the filamentous fungus Podospora anserina

“…Crosstalks between peroxisomes and mitochondria have been described in various organisms such as yeasts (Chelstowska and Butow, 1995;Fujimura et al, 2007;Liao et al, 1991;Petrova et al, 2004), filamentous fungi (Ruprich-Robert et al, 2002b), plants (Cooper and Beevers, 1969;Dieuaide et al, 1993) and mammals (Dirkx et al, 2005;Goldfisher et al, 1973;Hughes et al, 1990) but our knowledge of a possible link between peroxisomal ABC transporters and mitochondria is still very poor. In mammals, ALDP deficiencies lead to mitochondrial morphological abnormalities (McGuinness et al, 2003;Oezen et al, 2005).…”

Mitochondria and peroxisomes: Are the ‘Big Brother’ and the ‘Little Sister’ closer than assumed?

“…(28) Very recently, it has been demonstrated that peroxisomal metabolism in the yeast Pichia methanolica is regulated by an oxygen-recognition system through organelle crosstalk between the mitochondria and peroxisomes. (29) Furthermore, extensive metabolic interactions between peroxisomes, mitochondria and chloroplasts are described in plant leaves where the organelles tightly cooperate in the diversion of glycolate, produced by photosynthesis, into glycine and serine production, resulting in photo-respiration. (30) Such a metabolic communication renders peroxisomes and mitochondria dependent upon each other for their function (Fig.…”

Expression level of methanol-inducible peroxisomal proteins and peroxisome morphology are affected by oxygen conditions and mitochondrial respiratory pathway function in the methylotrophic yeastCandida boidinii

“…In a previous report, we showed that the induction patterns of AOD isozymes in P. methanolica were controlled by oxygen concentration (Fujimura et al, 2007). Therefore, the cell has to control the oxygen consumption balance between the peroxisomes and mitochondria.…”

“…Indeed, the P. methanolica AOD isozymes, which are octameric enzymes consisting of two different subunits with different affinities for oxygen, Mod1p, and Mod2p (Nakagawa et al, 1996(Nakagawa et al, , 1999(Nakagawa et al, , 2001, are induced only under aerobic conditions, with the ratio of the two subunits in the AOD octamer depending on oxygen concentration and respiratory chain activity (Nakagawa et al, 2006;Fujimura et al, 2007). Therefore, the yeast cells must have a mechanism for controlling the methanol metabolism, which responds to oxygen levels, to balance the oxygen needs between these two organelles.…”

“…Therefore, the yeast cells must have a mechanism for controlling the methanol metabolism, which responds to oxygen levels, to balance the oxygen needs between these two organelles. Indeed, the P. methanolica AOD isozymes, which are octameric enzymes consisting of two different subunits with different affinities for oxygen, Mod1p, and Mod2p (Nakagawa et al, 1996(Nakagawa et al, , 1999(Nakagawa et al, , 2001, are induced only under aerobic conditions, with the ratio of the two subunits in the AOD octamer depending on oxygen concentration and respiratory chain activity (Nakagawa et al, 2006;Fujimura et al, 2007). We believe that the regulation of methanol metabolism responding to oxygen conditions is an important system common to all methylotrophic yeast strains, and that maintenance of the oxygen consumption balance between peroxisomes and mitochondria is one of the key points for regulation of methanol metabolism.…”