The Role of Osmolytes and Membrane Lipids in the Adaptation of Acidophilic Fungi

Abstract

Acidophiles maintain near-neutral intracellular pH using proton pumps. We have suggested the protective role of osmolytes and membrane lipids in the adaptation to an acidic environment. Previously we have observed, for the first time, high levels of trehalose in acidophilic basidiomycete Sistotrema brinkmannii. Here, we have studied the composition of both osmolytes and membrane lipids of two more acidophilic fungi. Trehalose and polyols were among the main osmolytes during growth under optimal conditions (pH 4.0) in basidiomycete Phlebiopsis gigantea and ascomycete Mollisia sp. Phosphatidic acids, phosphatidylethanolamines, phosphatidylcholines, and sterols, were predominant membrane lipids in both fungi. P. gigantea had a narrow optimum of growth at pH 4.0, resulting in a sharp decline of growth rate at pH 2.6 and 5.0, accompanied by a decrease in the number of osmolytes and significant changes in the composition of membrane lipids. In contrast, Mollisia sp. had a broad optimal growth range (pH 3.0–5.0), and the number of osmolytes either stayed the same (at pH 6.0) or increased (at pH 2.6), while membrane lipids composition remained unchanged. Thus, the data obtained indicate the participation of osmolytes and membrane lipids in the adaptation of acidophilic fungi.

Membrane Lipids and Osmolytes in the Response of the Acidophilic Basidiomycete Phlebiopsis gigantea to Heat, Cold, and Osmotic Shocks

“…Thus, a high degree of unsaturation of the phospholipid fraction can be observed (about 1.5), which is usually characteristic of psychrophilic fungi [ 42 , 43 ]. It has also been previously shown that in P. gigantea , the degree of unsaturation remained constant both in growth dynamics and under unfavorable pH conditions [ 25 ]. The data obtained suggest that the mechanism for changing the degree of unsaturation is not involved in the adaptation of P. gigantea to either the pH factor or HS, CS, or OS.…”

“…In our studies, we have shown that PAs, which are minor components in non-extremophiles [ 44 ], are present in extremophiles, either as predominant or as one of the main membrane lipids [ 24 , 25 , 45 , 46 , 47 ]. PAs are multifunctional and poorly studied compounds, being a key metabolite of lipogenesis and performing regulatory and structural functions [ 48 , 49 ].…”

“…It is assumed that PAs can control transport from the Golgi apparatus and EPR, endocytosis, and exocytosis due to the ability to aggregate into microdomains, which leads to bending of membranes, resulting in vesicle formation. Previously, we have shown for the first time a high proportion of PA in various extremophilic fungi: thermophiles [ 45 ], alkaliphiles [ 46 ], acidophiles [ 24 , 25 ], and xerophiles [ 47 ]. Acidophiles, unlike neutrophils, are also characterized by the presence of PA as one of the main phospholipids, along with PE, PC, and sterols, which also confirms their role in extremophilia [ 24 , 25 ].…”

“…Previously, we have shown for the first time a high proportion of PA in various extremophilic fungi: thermophiles [ 45 ], alkaliphiles [ 46 ], acidophiles [ 24 , 25 ], and xerophiles [ 47 ]. Acidophiles, unlike neutrophils, are also characterized by the presence of PA as one of the main phospholipids, along with PE, PC, and sterols, which also confirms their role in extremophilia [ 24 , 25 ]. These data suggest that extremophile membranes have a special structure compared with non-extremophile membranes.…”

“…Acidophiles, like all other fungi, are exposed to additional stress factors (heat, cold, osmotic) under natural conditions. Previous data on the effects of trehalose protection [ 24 , 25 ] suggest that acidophiles can use the cell membrane and osmolytic systems to adapt to a variety of abiotic stressors.…”