95 / 2025-03-31 17:41:09

Nanoplastics-Mediated Metabolic Alterations in Manganese-Oxidizing Fungi

Nanoplastics,Manganese oxides,Biomineralization,Metabolism

Theme 2: Geobiology of Modern Habitable Earth > Session 2c: Geomicrobiology of Hazardous Elements Generated by Anthropogenic Activities

Manganese (Mn) oxides are highly reactive mineral phases that play important roles in elemental biogeochemical cycles. Unlike other metallic elements, although the oxidation of soluble Mn (II) is thermodynamically feasible, its oxidation rate is very slow. Some studies suggest that the biological oxidation rate of manganese can be 10⁵ times faster than non-biological oxidation. Therefore, it is widely believed that Mn (IV) oxide minerals in terrestrial and aquatic environments are precipitated through microbial mineralization or through catalytic action on the surface of highly reactive manganese/iron oxides^[1-3]. However, since the beginning of the Anthropocene, human productive activities have had a significant impact on microbial activities. For example, primary and secondary nanoplastics (NPs), as landmark products of human activities, are now ubiquitous in the environment, and they may affect the metabolic activities of microorganisms and related element cycling^[4]. However, the effects of NPs on the metabolic activity and environmental behavior of manganese oxidizing microorganisms have not been reported.

This study explored the effects of NPs on the metabolic function of the manganese oxidizing fungus Acremonium strictum strain KR21-2, which is significant for understanding the interaction between microorganisms and the earth environment since the Anthropocene. The main conclusions are as follows:

(1) The dry weight analysis of hyphae showed NPs had no significant effect on the growth of strain KR21-2. But TEM images revealed that a large number of NPs adhered to the hydrophobic surface of cell membrane. The MDA, LDH, CAT, TSOD and Calcein-AM/PI double staining results indicated that the adherence of NPs might induce cellular damage caused by unbalanced oxidative stress in the presence of 50 and 100 mg/L NPs.

(2) Strain KR21-2 might trigger some mechanisms to repair injured cells and result in a series of changes in carbon metabolism and extracellular metabolites. The Biolog FF results suggested that the addition of different concentrations of NPs significantly increased the utilization of all types of carbon sources. The markedly enhanced utilization of D-Malic acid, L-Malic acid, L-Aspartic acid, L-Glutamic acid and Succinamic acid showed the enhancement of microbial TCA cycle and mitochondrial respiration. As a barrier in protecting microorganisms from external stimuli, the content of extracellular polymeric substance (EPS) was also significantly increased. Furthermore, transcriptomic analysis suggested that transcription processes, phospholipid synthesis, protein metabolism and transport were enhanced in the presence of 1 and 10 mg/L NPs, which are the repair strategies of microorganisms.

(3) High concentration of NPs inhibited the biomineralization process. When 50 and 100 mg/L NPs were added, the concentration of Mn²⁺ in the culture medium hardly decreased after 96 h incubation, and only yellow hyphae without Mn oxides were observed. We propose that the metabolic energy of strain KR21-2 only supports cell growth and repair under the high stress of 50 and 100 mg/L NPs, and strain KR21-2 ceases the secretion of manganese oxidase because manganese oxidation is a non-essential process.

(4) Low concentration of NPs modulates the crystal structure of manganese oxide by changing the chemical composition of EPS. The concentration and visualization analyses of polysaccharide showed that the presence of NPs resulted in a significant increase in polysaccharide, and it was tightly distributed on the surface of hyphae. EEM-PARAFAC analysis showed that tyrosine protein-like substances and tryptophan protein-like substances in B-EPS increased in the presence of NPs. Therefore, we inferred that in the presence of 1 and 10 mg/L NPs, manganese oxidation process became slower due to the increased hydrophobicity of EPS attenuated the complexation ability of Mn²⁺, which resulted in the crystallinity increase of BMOs.



References

[1] Thomas G. Spiro J R B G. Bacteriogenic manganese oxides.[J]. Accounts of Chemical Research. 2010, 43(1): 2-9.

[2] Tebo B M, Bargar J R, Clement B G, et al. BIOGENIC MANGANESE OXIDES: Properties and Mechanisms of Formation[J]. Annu.rev.earth Planet. 2004, 32(1): 287-328.

[3] Webb S M, Dick G J, Bargar J R, et al. Evidence for the presence of Mn(III) intermediates in the bacterial oxidation of Mn(II)[J]. Proceedings of the National Academy of Sciences of the United States of America. 2005, 102(15).

[4] Larue C, Sarret G, Michel H C, et al. A Critical Review on the Impacts of Nanoplastics and Microplastics on Aquatic and Terrestrial Photosynthetic Organisms[J]. Small. 2021.