The Importance of Nitric Oxide as the Molecular Basis of the Hydrogen Gas Fumigation-Induced Alleviation of Cd Stress on Ganoderma lucidum

Dyaaaldin Abdalmegeed,Qurban Ali,Javaid A Bhat,Wajid Ali Khattak,Ilyas Ali,Pengfei Cheng,Gan Zhao,Fawze Alnadari,Weiti Cui,Mostafa G Ali,Yehia A.-G Mahmoud,Sameh A Korma,Wenbiao Shen,Manar K Abd Elnabi

doi:10.3390/jof8010010

Abstract

Whether or not hydrogen gas (H2) can reduce cadmium (Cd) toxicity in Ganoderma lucidum has remained largely unknown. Here, we report that Cd-induced growth inhibition in G. lucidum was significantly alleviated by H2 fumigation or hydrogen-rich water (HRW), evaluated by lower oxidative damage and Cd accumulation. Moreover, the amelioration effects of H2 fumigation were better than of HRW in an optimum concentration of H2 under our experimental conditions. Further results showed that H2-alleviated growth inhibition in G. lucidum was accompanied by increased nitric oxide (NO) level and nitrate reductase (NR) activity under Cd stress. On the other hand, the mitigation effects were reversed after removing endogenous NO with its scavenger cPTIO or inhibiting H2-induced NR activity with sodium tungstate. The role of NO in H2-alleviated growth inhibition under Cd stress was proved to be achieved through a restoration of redox balance, an increase in cysteine and proline contents, and a reduction in Cd accumulation. In summary, these results clearly revealed that NR-dependent NO might be involved in the H2-alleviated Cd toxicity in G. lucidum through rebuilding redox homeostasis, increasing cysteine and proline levels, and reducing Cd accumulation. These findings may open a new window for H2 application in Cd-stressed economically important fungi.

Highlights

Ganoderma lucidum is one of the large basidiomycetous fungi with a highly significant medicinal importance [1]
Mycelial inocula were grown on solid complete yeast medium (CYM) media for 2 days; on the 3rd day, were either pre-treated with 1%, 2%, 3%, 5%, or 10% H2 fumigation or 50% hydrogen-rich water (HRW) for 24 h or not treated with either hydrogen forms (Con)
Under Cd stress, the activities of CAT, glutathione reductase (GR), and glutathione peroxidase (GPX) were decreased by 55.40%, 46.43%, and 43.67%, respectively; superoxide dismutase (SOD) activity was increased by 24.31%

Summary

Introduction

Ganoderma lucidum is one of the large basidiomycetous fungi with a highly significant medicinal importance [1]. Cadmium (Cd) is one of the most harmful heavy metals due to its carcinogenic and neurotoxic effects on animals and humans [2]. Excess Cd accumulation inside living organisms can disrupt physiological processes such as protein metabolism, respiration, and nutrients uptake [4], as it induces the production of reactive oxygen species (ROS) [5,6]. ROS, in turn, oxidize vital biological molecules such as proteins, lipids, and nucleic acids, leading to membrane damage, inactivation of enzymes, and lipid peroxidation [5]. G. lucidum accumulates Cd while consuming contaminated straw, leading to reduced mycelial growth and biomass. The contaminated mushrooms are eaten by humans, and their health is adversely affected

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