Direct observation of Mn distribution/speciation within and surrounding a basidiomycete fungus in the production of Mn-oxides important in toxic element containment

Ayaka Takeda, Takumi Oki, Hiroki Yokoo, Keisuke Kawamoto, Yuriko Nakano, Asumi Ochiai, Ilma Dwi Winarni, Mitsuki Kitahara, Kenta Miyoshi, Kenjin Fukuyama, Yoshiyuki Ohara, Keiko Yamaji, Toshihiko Ohnuki, Michael F. Hochella, Satoshi Utsunomiya

Research output: Contribution to journalArticlepeer-review

Abstract

Biogenic manganese (Mn) oxides occur ubiquitously in the environment including the uranium (U) mill tailings at the Ningyo-toge U mine in Okayama, Japan, being important in the sequestration of radioactive radium. To understand the nanoscale processes in Mn oxides formation at the U mill tailings site, Mn2+ absorption by a basidiomycete fungus, Coprinopsis urticicola, isolated from Ningyo-toge mine water samples, was investigated in the laboratory under controlled conditions utilizing electron microscopy, synchrotron-based X-ray analysis, and fluorescence microscopy with a molecular pH probe. The fungus’ growth was first investigated in an agar-solidified medium supplemented with 1.0 mmol/L Mn2+, and Cu2+ (0–200 μM), Zn2+ (0–200 μM), or diphenyleneiodonium (DPI) chloride (0–100 μM) at 25 °C. The results revealed that Zn2+ has no significant effects on Mn oxide formation, whereas Cu2+ and DPI significantly inhibit both fungal growth and Mn oxidation, indicating superoxide-mediated Mn oxidation. Indeed, nitroblue tetrazolium and diaminobenzidine assays on the growing fungus revealed the production of superoxide and peroxide. During the interaction of Mn2+ with the fungus in solution medium at the initial pH of 5.67, a small fraction of Mn2+ infiltrated the fungal hyphae within 8 h, forming a few tens of nm-sized concentrates of soluble Mn2+ in the intracellular pH of ∼6.5. After 1 day of incubation, Mn oxides began to precipitate on the hyphae, which were characterized as fibrous nanocrystals with a hexagonal birnessite-structure, these forming spherical aggregates with a diameter of ∼1.5 μm. These nanoscale processes associated with the fungal species derived from the Ningyo-toge mine area provide additional insights into the existing mechanisms of Mn oxidation by filamentous fungi at other U mill tailings sites under circumneutral pH conditions. Such processes add to the class of reactions important to the sequestration of toxic elements.

Original languageEnglish
Article number137526
JournalChemosphere
Volume313
DOIs
Publication statusPublished - Feb 2023

All Science Journal Classification (ASJC) codes

  • Environmental Engineering
  • Environmental Chemistry
  • Chemistry(all)
  • Pollution
  • Public Health, Environmental and Occupational Health
  • Health, Toxicology and Mutagenesis

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