Direct observation of Mn distribution/speciation within and surrounding a basidiomycete fungus in the production of Mn-oxides important in toxic element containment
Journal
Chemosphere
Journal Volume
313
Start Page
137526
ISSN
0045-6535
Date Issued
2023-02
Author(s)
Takeda, Ayaka
Oki, Takumi
Yokoo, Hiroki
Kawamoto, Keisuke
Nakano, Yuriko
Ochiai, Asumi
Winarni, Ilma Dwi
Kitahara, Mitsuki
Miyoshi, Kenta
Fukuyama, Kenjin
Ohara, Yoshiyuki
Yamaji, Keiko
Ohnuki, Toshihiko
Hochella, Michael F.
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.
Subjects
Basidiomycota
Fungi
Manganese Compounds
Oxidation-Reduction
Oxides
Superoxides
Chugoku
Honshu
Japan
Ningyo Pass
Okayama
Chlorine compounds
Energy dispersive X ray analysis
Fluorescence microscopy
Groundwater
Nanotechnology
Oxidation
pH
Water absorption
X ray diffraction analysis
chloride
cupric ion
diaminobenzidine
diphenyliodonium salt
manganese
manganese oxide
nanocrystal
nitroblue tetrazolium
peroxide
radium
superoxide
uranium
yeast extract
zinc ion
manganese derivative
oxide
Biogenic manganese oxides
Direct observations
Manganese distribution
Manganese oxidations
Nano scale
Oxide formation
Toxic elements
Zn 2+
fungus
oxidation
speciation (chemistry)
toxic substance
absorption
Article
Basidiomycetes
cell pH
Coprinopsis urticicola
electron microscopy
filamentous fungus
fluorescence microscopy
fungus growth
fungus hyphae
fungus isolation
measurement
mine tailings
nonhuman
precipitation
synchrotron radiation
water sampling
X ray absorption spectroscopy
X ray analysis
chemistry
oxidation reduction reaction
Publisher
Elsevier BV
Type
journal article