Microbe-mineral interactions play a crucial role in driving geological and geochemical processes. In these processes, mineral supply energy and nutrients essential for microbial growth and metabolism, while microbes influence mineral dissolution, transformation, and formation processes through their metabolic activities. These interactions occur at microscopic interfaces at the single-cell level, shaping both microbe and mineral evolution while profoundly influencing geological events, biogeochemical cycles, and ore formation. Fungi, one of Earth's oldest and most diverse life forms, are unique due to apical growth mode of the hyphae. This growth mode enables hyphal tips to exert biophysical forces of up to 10−20 μN/μM², allowing them to explore and penetrate substrates. The study of fungi’s roles in geological and geochemical processes has emerged as a distinct field called Geomycology. Increasing evidence highlights the critical role of fungi play in soil formation, ore genesis, biogeochemical cycling of elements, and the evolution and reproduction of terrestrial plants.
In 1997, Jongmans et al. discovered that fungi significantly accelerate the weathering of silicate minerals, leading to the formaiton of tunnels. In 2009, Bonneville et al. demonstrated that biophysical forces excerted by fungal hyphal tips directly distort the crystal structure of silicate mineral, while subsequent biochemical actions derived from metabolites (e.g., proton, organic acids, and siderophores) dissolve and mobilize elements. These biophysical and biochmeical mechanisms act synergistically to enhance mineral weathering. Our previous studies showed that fungal hyphae instantly initiate mineral weathering upon contact (Li et al., 2022) and highlighted the critical role of biophysical forces generated at hyphal tips in the fungal weathering process (Li et al., 2016). However, most studies to date have focused on freshly prepared silicate minerals, leaving the fungal weathering of aged minerals with altered layers (Si-rich deposits) laygely unexplored. Altered layers form rapidly during silicate mineral dissolution and significantly inhibit further dissolution under abiotic conditions. Thus far, only Wild et al. (2018) have reported on bacterial activity on aged silicates (olivine and labradorite), showing only a 30% enhancement compared to abiotic conditions. Notably, fungal weathering of aged silicate minerals remains unstudied.
To bridge this knowledge gap, Dr. Zibo Li from the Nanjing Institute of Geology and Paleontology, Chinese Academy of Sciences, collaborated with Professor Xiancai Lu from Nanjing University and a team of researchers, including Professors Maoyan Zhu and Zongjun Yin (Nanjing Institute of Geology and Paleontology), Professors Jun Chen and Gaojun Li (Nanjing University), Professor Zhangdong Jin (Institute of Earth Environment, CAS), and Professor Hui Teng (Tianjin University). Their study explored fungal interactions with aged olivine and lizardite, demonstrating that fungal hyphae can degrade altered layers and continuously promote silicate mineral weathering. The study was recently published in Geophysical Research Letters.
Key Findings:
1. Fungi significantly enhance the dissolution rates of aged silicate minerals. Aged olivine and lizardite, pretreated in acidic solutions, developed Si-rich altered layers. As pretreatment duration increased, the thickness of these altered layer grew, and mineral dissolution rates under abiotic condition gradually declined. Under fungal influence, the dissolution rates of aged silicate minerals increased by 1−2 orders of magnitude, with olivine dissolution rates enhanced by 9−14 times and lizardite dissolution rates by 71−123 times compared to abiotic conditons.
2. Fungal hyphae penetrate altered layers and etch underlying fresh minerals. Within 24 hours of cultivation, fungal hyphae produced dissolution channels on the surfaces of both fresh and aged silicate minerals, with channel depths ranging from 18−65 nm on olivine and 10−32 nm on lizardite. After 20 days, the hyphae penetrated the altered layers, facilitating further elemental dissolution from the fresh minerals beneath.
3. Fungi facilitate matter and energy diffusion within altered layers. For olivine pretreated for 480 hours, the thickness of the altered layer increased from ~110 nm to ~230 nm at the hyphal tip-mineral interface and from ~20 nm to ~380 nm at the hyphal end-mineral interface. Beneath the altered layers, fungi oxidized structual Fe(II). For lizardite pretreated for 96 hours, fungal hyphae dissolved elements within altered layers and the thickness of altered layers at hypha-mineral interface expanded from ~3.3 μm to 6.2 μm. Although fungi had a weaker effect on dissolving altered layers with normalized Mg/Si molar ratios below 0.65, prolonged contact between fungi and minerals eventurally led to further dissolution of the fresh minerals below.
This study reveals that fungi actively regulate their growth behavior in response to the bioavailability of nutrients in the envirments, effectively degrading altered layers through etching and penetration. Biophysical forces exerted by fungal tips disrupt altered layers, while the enhanced interdiffusion of metabolic byproducts (e.g., protons, small-molecule complexes, and reactive oxygen species) and released cations across altered layers continuously prmote the weathering of silicate mineral. These findings not only deepen our understanding of microbially-mediated geological and geochemical processes but also provide a theoretical framework for searching mineralogical biosignatures.
This study was funded by the National Natural Science Foundation of China.
Citations:
AG Jongmans, N Van Breemen, U Lundström, PAW Van Hees, RD Finlay, M Srinivasan, T Unestam, R Giesler, P-A Melkerud, and M Olsson. 1997. Rock-eating fungi, Nature, 389: 682-83. https://doi.org/10.1038/39493
S. Bonneville*, M. M. Smits, A. Brown, J. Harrington, J. R. Leake, R. Brydson, and L. G. Benning. 2009. Plant-driven fungal weathering: Early stages of mineral alteration at the nanometer scale, Geology, 37: 615-18. https://doi.org/10.1130/G25699A.1
Zi-Bo Li*, Lianwen Liu, Xiancai Lu, Yi Cao, Junfeng Ji, and Jun Chen. 2022. Hyphal tips actively develop strong adhesion with nutrient-bearing silicate to promote mineral weathering and nutrient acquisition, Geochimica et Cosmochimica Acta, 318: 55-69. https://doi.org/10.1016/j.gca.2021.11.017
Zibo Li, Lianwen Liu, Jun Chen, and H. Henry Teng*. 2016. Cellular dissolution at hypha- and spore-mineral interfaces revealing unrecognized mechanisms and scales of fungal weathering, Geology, 44: 319-22. https://doi.org/10.1130/G37561.1
Bastien Wild, Gwenaël Imfeld, François Guyot, and Damien Daval. 2018. Early stages of bacterial community adaptation to silicate aging, Geology, 46: 555-58. https://doi.org/10.1130/G40283.1
Figure 1: The concentration of dissolved Fe in fungal and abiotic weathering experiments over a 20‐day period. Values within square brackets denote the enhancement factor (Fefungal,max/Feabiotic,max).
Figure 2: The lengths of T. flavus hyphae on olivine and lizardite and hyphal etching and penetration.
Figure 3: The normalized Mg/Si molar ratios beneath T. flavus hypha- and solution-olivine/lizardite interfaces as determined by TEM-EDS after 24 h of cultivation.
Figure 4: T. flavus hypha-induced transformation of the crystal structure and the oxidation of Fe(II) in olivine pretreated for 480 h after 24 h of cultivation.
Article informaiton:
Zi-Bo Li*, Xiancai Lu*, Gaojun Li, Zhangdong Jin, Lianwen Liu, Zongjun Yin, Maoyan Zhu, Hui Henry Teng, Junfeng Ji, and Jun Chen. 2024. Continuable Weathering of Silicate Minerals Driven by Fungal Plowing, Geophysical Research Letters, 51: e2024GL111197. https://doi.org/10.1029/2024GL111197
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