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Abstract
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.
Highlights
Nutrient foraging by fungi weathers rocks by mechanical and biochemical processes
We investigated three-dimensional elemental distribution within a basaltic glass matrix and across an interfacial boundary with titanomagnetite crystals at near atomic scale resolution provided by Atom Probe Tomography (APT)
High-resolution microscopy surveys of five grains revealed strands of fungal hyphae adhering to grain surfaces and growing along grain edges (Figs. 1, S1)
Summary
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. Assessing the biotic and abiotic drivers of basalt and glass weathering in natural Earth systems, including soils, remains of paramount importance for recognizing and predicting long-term ecosystem response to changes in global c limate[11,12], identifying lithologic controls on global carbon cycling[2,13], or detecting mineralogical biosignatures that may provide evidence for past, present, and future life on other p lanets[14–16]. Three substrate types were set up for the study including (1) quartz sand as a nutrient-poor, in-situ control to assess background levels of fungal foraging; (2) granite extracted from a granitic rock quarry in southern Arizona to provide a fresh supply of coarse-grained minerals[27,50]; and (3) basalt, given its importance as a silicate rock for global carbon and nutrient cycling[46]. Results provided evidence for fungal-driven biomechanical weathering of the granite and basalt in all three ecosystems after one year of field burial[41], and highlighted the need for more in-depth assessments of biotic-mineral interfaces, on basaltic surfaces inhabited by fungi and containing mineral coatings presumably from microbial activity[51]
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