Fungal hyphae develop where titanomagnetite inclusions reach the surface of basalt grains

• Published in: Scientific reports Vol. 12; no. 1; pp. 3407 - 16
• Main Authors: Lybrand, Rebecca A., Qafoku, Odeta, Bowden, Mark E., Hochella, Michael F., Kovarik, Libor, Perea, Daniel E., Qafoku, Nikolla P., Schroeder, Paul A., Wirth, Mark G., Zaharescu, Dragos G.
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 01.03.2022; Nature Publishing Group; Nature Portfolio
• Subjects: 631/45/47; 704/2151; 704/47; Basalt; BASIC BIOLOGICAL SCIENCES; biochemistry; Biofilms; Carbon cycle; Carbon sequestration; Coniferous forests; Forests; Fungi; GEOSCIENCES; Hardwoods; Humanities and Social Sciences; Hyphae; Hyphae - metabolism; multidisciplinary; Nutrient cycles; Radioactive wastes; Science; Science (multidisciplinary); Silicates - metabolism; Soil; Soil formation; solid earth sciences; Waste disposal; Weathering
• ISSN: 2045-2322; 2045-2322
• DOI: 10.1038/s41598-021-04157-z

Nutrient foraging by fungi weathers rocks by mechanical and biochemical processes. Distinguishing fungal-driven transformation from abiotic mechanisms in soil remains a challenge due to complexities within natural field environments. We examined the role of fungal hyphae in the incipient weathering of granulated basalt from a three-year field experiment in a mixed hardwood-pine forest (S. Carolina) to identify alteration at the nanometer to micron scales based on microscopy-tomography analyses. Investigations of fungal-grain contacts revealed (i) a hypha-biofilm-basaltic glass interface coinciding with titanomagnetite inclusions exposed on the grain surface and embedded in the glass matrix and (ii) native dendritic and subhedral titanomagnetite inclusions in the upper 1–2 µm of the grain surface that spanned the length of the fungal-grain interface. We provide evidence of submicron basaltic glass dissolution occurring at a fungal-grain contact in a soil field setting. An example of how fungal-mediated weathering can be distinguished from abiotic mechanisms in the field was demonstrated by observing hyphal selective occupation and hydrolysis of glass-titanomagnetite surfaces. We hypothesize that the fungi were drawn to basaltic glass-titanomagnetite boundaries given that titanomagnetite exposed on or very near grain surfaces represents a source of iron to microbes. Furthermore, glass is energetically favorable to weathering in the presence of titanomagnetite. Our observations demonstrate that fungi interact with and transform basaltic substrates over a three-year time scale in field environments, which is central to understanding the rates and pathways of biogeochemical reactions related to nuclear waste disposal, geologic carbon storage, nutrient cycling, cultural artifact preservation, and soil-formation processes.