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

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 ofmore » 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.« less

Authors:
 [1];  [2];  [2]; ORCiD logo [3];  [2]; ORCiD logo [2]; ORCiD logo [2];  [4];  [2];  [5]
  1. Oregon State Univ., Corvallis, OR (United States); Univ. of California, Davis, CA (United States)
  2. Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
  3. Pacific Northwest National Lab. (PNNL), Richland, WA (United States); Virginia Polytechnic Inst. and State Univ. (Virginia Tech), Blacksburg, VA (United States)
  4. Univ. of Georgia, Athens, GA (United States)
  5. Univ. of Wisconsin, Green Bay, WI (United States); Univ. of California, Davis, CA (United States)
Publication Date:
Research Org.:
Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
Sponsoring Org.:
USDOE Office of Science (SC); National Science Foundation (NSF)
OSTI Identifier:
1860251
Report Number(s):
PNNL-SA-163525; 49828; 51465; EAR-1945659; EAR-GEO-1331846; EAR-1023215
Journal ID: ISSN 2045-2322
Grant/Contract Number:  
AC05-76RL01830
Resource Type:
Accepted Manuscript
Journal Name:
Scientific Reports
Additional Journal Information:
Journal Volume: 12; Journal Issue: 1; Journal ID: ISSN 2045-2322
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 58 GEOSCIENCES; biochemistry; solid earth sciences

Citation Formats

Lybrand, Rebecca A., Qafoku, Odeta, Bowden, Mark E., Hochella, Michael F., Kovarik, Libor, Perea, Daniel E., Qafoku, Nikolla P., Schroeder, Paul, Wirth, Mark G., and Zaharescu, Dragos G. Fungal hyphae develop where titanomagnetite inclusions reach the surface of basalt grains. United States: N. p., 2022. Web. doi:10.1038/s41598-021-04157-z.
Lybrand, Rebecca A., Qafoku, Odeta, Bowden, Mark E., Hochella, Michael F., Kovarik, Libor, Perea, Daniel E., Qafoku, Nikolla P., Schroeder, Paul, Wirth, Mark G., & Zaharescu, Dragos G. Fungal hyphae develop where titanomagnetite inclusions reach the surface of basalt grains. United States. https://doi.org/10.1038/s41598-021-04157-z
Lybrand, Rebecca A., Qafoku, Odeta, Bowden, Mark E., Hochella, Michael F., Kovarik, Libor, Perea, Daniel E., Qafoku, Nikolla P., Schroeder, Paul, Wirth, Mark G., and Zaharescu, Dragos G. Tue . "Fungal hyphae develop where titanomagnetite inclusions reach the surface of basalt grains". United States. https://doi.org/10.1038/s41598-021-04157-z. https://www.osti.gov/servlets/purl/1860251.
@article{osti_1860251,
title = {Fungal hyphae develop where titanomagnetite inclusions reach the surface of basalt grains},
author = {Lybrand, Rebecca A. and Qafoku, Odeta and Bowden, Mark E. and Hochella, Michael F. and Kovarik, Libor and Perea, Daniel E. and Qafoku, Nikolla P. and Schroeder, Paul and Wirth, Mark G. and Zaharescu, Dragos G.},
abstractNote = {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.},
doi = {10.1038/s41598-021-04157-z},
journal = {Scientific Reports},
number = 1,
volume = 12,
place = {United States},
year = {Tue Mar 01 00:00:00 EST 2022},
month = {Tue Mar 01 00:00:00 EST 2022}
}

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