Saprotrophic Fungus Induces Microscale Mineral Weathering to Source Potassium in a Carbon-Limited Environment

Richardson, Jocelyn A.; Anderton, Christopher R.; Bhattacharjee, Arunima

doi:10.3390/min13050641

Saprotrophic Fungus Induces Microscale Mineral Weathering to Source Potassium in a Carbon-Limited Environment

Journal Article · Fri May 05 00:00:00 EDT 2023 · Minerals

DOI:https://doi.org/10.3390/min13050641· OSTI ID:1972480

Richardson, Jocelyn A. ^[1]; Anderton, Christopher R. ^[2]; Bhattacharjee, Arunima ^[2]

SLAC National Accelerator Laboratory (SLAC), Menlo Park, CA (United States). Stanford Synchrotron Radiation Lightsource (SSRL); SLAC National Accelerator Laboratory
Pacific Northwest National Laboratory (PNNL), Richland, WA (United States). Environmental Molecular Sciences Laboratory (EMSL)

Plants rely on potassium for many critical biological processes, but most soils are potassium limited. Moving potassium from the inaccessible, mineral-bound pool to a more bioavailable form is crucial for sustainably increasing local potassium concentrations for plant growth and health. Here, we use a synthetic soil habitat (mineral doped micromodels) to study and directly visualize how the saprotrophic fungus, Fusarium sp. DS 682, weathers K-rich soil minerals. After 30 days of fungal growth, both montmorillonite and illite (secondary clays) had formed as surface coatings on primary K-feldspar, biotite, and kaolinite grains. The distribution of montmorillonite differed depending on the proximity to a carbon source, where montmorillonite was found to be associated with K-feldspar closer to the carbon (C) source, which the fungus was inoculated on, but associated with biotite at greater distances from the C source. The distribution of secondary clays is likely due to a change in the type of fungal exuded organic acids; from citric to tartaric acid dominated production with increasing distance from the C source. Thus, the main control on the ability of Fusarium sp. DS 682 to weather K-feldspar is proximity to a C source to produce citric acid via the TCA cycle.

View Accepted Manuscript (DOE)

Research Organization:: Pacific Northwest National Laboratory (PNNL), Richland, WA (United States); SLAC National Accelerator Laboratory (SLAC), Menlo Park, CA (United States)

Sponsoring Organization:: DOE-BER; National Institutes of Health (NIH); USDOE Office of Science (SC), Basic Energy Sciences (BES); USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC02-76SF00515; AC05-76RL01830

OSTI ID:: 1972480

Alternate ID(s):: OSTI ID: 2483887

Report Number(s):: PNNL-SA--190853

Journal Information:: Minerals, Journal Name: Minerals Journal Issue: 5 Vol. 13; ISSN 2075-163X

Publisher:: MDPICopyright Statement

Country of Publication:: United States

Language:: English

References (67)

K-Edge X-Ray Absorption Spectra from Potassium Compounds Sugiura, C.; Muramatsu, S. physica status solidi (b), Vol. 132, Issue 2 https://doi.org/10.1002/pssb.2221320249	journal	December 1985
In vitro weathering of phlogopite by ectomycorrhizal fungi Paris, Fabienne; Bonnaud, Pascal; Ranger, Jacques Plant and Soil, Vol. 177, Issue 2 https://doi.org/10.1007/BF00010125	journal	December 1995
In vitro weathering of phlogopite by ectomycorrhizal fungi Paris, Fabienne; Botton, Bernard; Lapeyrie, Fr�d�ric Plant and Soil, Vol. 179, Issue 1 https://doi.org/10.1007/BF00011651	journal	February 1996
Co-inoculation of potassium solubilizing and nitrogen fixing bacteria on solubilization of waste mica and their effect on growth promotion and nutrient acquisition by a forage crop Basak, Biraj Bandhu; Biswas, Dipak Ranjan Biology and Fertility of Soils, Vol. 46, Issue 6 https://doi.org/10.1007/s00374-010-0456-x	journal	April 2010
Effect of arbuscular mycorrhizal colonization and two levels of compost supply on nutrient uptake and flowering of pelargonium plants Perner, Henrike; Schwarz, Dietmar; Bruns, Christian Mycorrhiza, Vol. 17, Issue 5 https://doi.org/10.1007/s00572-007-0116-7	journal	February 2007
Biotite and microcline as potassium sources in ectomycorrhizal and non-mycorrhizal Pinus sylvestris seedlings Wallander, H.; Wickman, Tonie Mycorrhiza, Vol. 9, Issue 1 https://doi.org/10.1007/s005720050259	journal	June 1999
Potassium coordination in trioctahedral micas investigated by K-edge XANES spectroscopy Cibin, G.; Mottana, A.; Marcelli, A. Mineralogy and Petrology, Vol. 85, Issue 1-2 https://doi.org/10.1007/s00710-005-0099-z	journal	November 2005
Fischer–Tropsch Synthesis: XANES Spectra of Potassium in Promoted Precipitated Iron Catalysts as a Function of Time On-stream Jacobs, Gary; Pendyala, Venkat Ramana Rao; Martinelli, Michela Catalysis Letters, Vol. 147, Issue 8 https://doi.org/10.1007/s10562-017-2090-9	journal	June 2017
Innovation in Resourcing Geological Materials as Crop Nutrients Manning, David A. C. Natural Resources Research, Vol. 27, Issue 2 https://doi.org/10.1007/s11053-017-9347-2	journal	June 2017
Research on potassium in agriculture: needs and prospects Römheld, Volker; Kirkby, Ernest A. Plant and Soil, Vol. 335, Issue 1-2 https://doi.org/10.1007/s11104-010-0520-1	journal	August 2010
Two Phosphate- and Potassium-solubilizing Bacteria Isolated from Tianmu Mountain, Zhejiang, China Hu, Xiufang; Chen, Jishuang; Guo, Jiangfeng World Journal of Microbiology and Biotechnology, Vol. 22, Issue 9 https://doi.org/10.1007/s11274-006-9144-2	journal	May 2006
A study of potassium dynamics and mineralogy in soils from subtropical Brazilian lowlands Britzke, Darines; da Silva, Leandro Souza; Moterle, Diovane Freire Journal of Soils and Sediments, Vol. 12, Issue 2 https://doi.org/10.1007/s11368-011-0431-7	journal	September 2011
Clay Minerals as the key to the Sequestration of Carbon in Soils Churchman, Gordon Jock; Singh, Mandeep; Schapel, Amanda Clays and Clay Minerals, Vol. 68, Issue 2 https://doi.org/10.1007/s42860-020-00071-z	journal	April 2020
Forms of potassium in coal and its combustion products Spiro, C. L.; Wong, J.; Lytle, F. W. Fuel, Vol. 65, Issue 3 https://doi.org/10.1016/0016-2361(86)90291-7	journal	March 1986
The effect of organic acids on plagioclase dissolution rates and stoichiometry Welch, Susan A.; Ullman, William J. Geochimica et Cosmochimica Acta, Vol. 57, Issue 12 https://doi.org/10.1016/0016-7037(93)90386-B	journal	June 1993
rates of feldspar dissolution at pH 3–7 with 0–8 m M oxalic acid Stillings, Lisa L.; Drever, James I.; Brantley, Susan L. Chemical Geology, Vol. 132, Issue 1-4 https://doi.org/10.1016/S0009-2541(96)00043-5	journal	October 1996
X-ray absorption study of the potassium coordination environment in glasses from the NaAlSi3O8-KAlSi3O8 binary Jackson, W. E.; Brown, G. E.; Ponader, C. W. Journal of Non-Crystalline Solids, Vol. 93, Issue 2-3 https://doi.org/10.1016/S0022-3093(87)80177-1	journal	September 1987
Fungal Production of Citric and Oxalic Acid: Importance in Metal Speciation, Physiology and Biogeochemical Processes Gadd, Geoffrey M. Advances in Microbial Physiology https://doi.org/10.1016/S0065-2911(08)60165-4	book	January 1999
Isolation and identification of potassium-solubilizing bacteria from tobacco rhizospheric soil and their effect on tobacco plants Zhang, Chengsheng; Kong, Fanyu Applied Soil Ecology, Vol. 82 https://doi.org/10.1016/j.apsoil.2014.05.002	journal	October 2014
Perspectives of potassium solubilizing microbes in sustainable food production system: A review Sattar, Annum; Naveed, Muhammad; Ali, Mohsin Applied Soil Ecology, Vol. 133 https://doi.org/10.1016/j.apsoil.2018.09.012	journal	January 2019
Different mechanisms driving the preferential adsorption of dissolved organic matter by goethite and montmorillonite Han, Lanfang; Yang, Yan; Sun, Ke Chemical Geology, Vol. 585 https://doi.org/10.1016/j.chemgeo.2021.120560	journal	December 2021
A review of feldspar alteration and its geological significance in sedimentary basins: From shallow aquifers to deep hydrocarbon reservoirs Yuan, Guanghui; Cao, Yingchang; Schulz, Hans-Martin Earth-Science Reviews, Vol. 191 https://doi.org/10.1016/j.earscirev.2019.02.004	journal	April 2019
Scale matters? Exploring the effect of scale on fungal–mineral interactions Smits, Mark M. Fungal Biology Reviews, Vol. 23, Issue 4 https://doi.org/10.1016/j.fbr.2009.11.002	journal	November 2009
Microbial release of potassium from K-bearing minerals by thermophilic fungus Aspergillus fumigatus Lian, Bin; Wang, Bin; Pan, Mu Geochimica et Cosmochimica Acta, Vol. 72, Issue 1 https://doi.org/10.1016/j.gca.2007.10.005	journal	January 2008
Specificity of low molecular weight organic acids on the release of elements from lizardite during fungal weathering Li, Zi-bo; Lu, Xiancai; Teng, H. Henry Geochimica et Cosmochimica Acta, Vol. 256 https://doi.org/10.1016/j.gca.2018.09.029	journal	July 2019
In-situ dissolution rates of silicate minerals and associated bacterial communities in the critical zone (Strengbach catchment, France) Wild, Bastien; Daval, Damien; Beaulieu, Emilie Geochimica et Cosmochimica Acta, Vol. 249 https://doi.org/10.1016/j.gca.2019.01.003	journal	March 2019
Fungal strategies of potassium extraction from silicates of different resistance as manifested in differential weathering and gene expression Pinzari, Flavia; Cuadros, Javier; Jungblut, Anne D. Geochimica et Cosmochimica Acta, Vol. 316 https://doi.org/10.1016/j.gca.2021.10.010	journal	January 2022
Mobilization and fractionation of rare earth elements during experimental bio-weathering of granites He, Yilin; Ma, Lingya; Li, Xurui Geochimica et Cosmochimica Acta, Vol. 343 https://doi.org/10.1016/j.gca.2022.12.027	journal	February 2023
Potassium isotopic fractionation in a humid and an arid soil–plant system in Hawai‘i Li, Wenshuai; Liu, Xiao-Ming; Hu, Yan Geoderma, Vol. 400 https://doi.org/10.1016/j.geoderma.2021.115219	journal	October 2021
Soil chemical extractions can alter potassium coordination in agricultural soils: A combined wet chemical and X-ray absorption spectroscopic approach Schmidt, Emma J.; Zanoni, Giovanni; Bumguardner, Amee Geoderma, Vol. 422 https://doi.org/10.1016/j.geoderma.2022.115914	journal	September 2022
Dissolution of kaolinite induced by citric, oxalic, and malic acids Wang, Xingxiang; Li, Qingman; Hu, Huafeng Journal of Colloid and Interface Science, Vol. 290, Issue 2 https://doi.org/10.1016/j.jcis.2005.04.066	journal	October 2005
A XANES investigation of the network-modifier cations environment before and after the Na + /K + ion-exchange in silicate glasses Ragoen, C.; Cormier, L.; Bidegaray, A. -I. Journal of Non-Crystalline Solids, Vol. 479 https://doi.org/10.1016/j.jnoncrysol.2017.10.021	journal	January 2018
Growth promotion and increased potassium uptake of cotton and rape by a potassium releasing strain of Bacillus edaphicus Sheng, X. F. Soil Biology and Biochemistry, Vol. 37, Issue 10 https://doi.org/10.1016/j.soilbio.2005.02.026	journal	October 2005
Plant- or microbial-derived? A review on the molecular composition of stabilized soil organic matter Angst, Gerrit; Mueller, Kevin E.; Nierop, Klaas G. J. Soil Biology and Biochemistry, Vol. 156 https://doi.org/10.1016/j.soilbio.2021.108189	journal	May 2021
X-ray photon-in/photon-out methods for chemical imaging Marcus, Matthew A. TrAC Trends in Analytical Chemistry, Vol. 29, Issue 6 https://doi.org/10.1016/j.trac.2010.02.013	journal	June 2010
Chemical kinetics of water-rock interactions Lasaga, Antonio C. Journal of Geophysical Research: Solid Earth, Vol. 89, Issue B6 https://doi.org/10.1029/JB089iB06p04009	journal	June 1984
Organic Acids as Agents of Chemical Weathering of Silicate Minerals Huang, W. H.; Keller, W. D. Nature Physical Science, Vol. 239, Issue 96 https://doi.org/10.1038/physci239149a0	journal	October 1972
A coupled microscopy approach to assess the nano-landscape of weathering Lybrand, Rebecca A.; Austin, Jason C.; Fedenko, Jennifer Scientific Reports, Vol. 9, Issue 1 https://doi.org/10.1038/s41598-019-41357-0	journal	March 2019
Oxalate secretion by ectomycorrhizal Paxillus involutus is mineral-specific and controls calcium weathering from minerals Schmalenberger, A.; Duran, A. L.; Bray, A. W. Scientific Reports, Vol. 5, Issue 1 https://doi.org/10.1038/srep12187	journal	July 2015
Aqueous alteration of potassium-bearing aluminosilicate minerals: from mechanism to processing Skorina, Taisiya; Allanore, Antoine Green Chemistry, Vol. 17, Issue 4 https://doi.org/10.1039/C4GC02084G	journal	January 2015
The promotion effect of isolated potassium atoms with hybridized orbitals in catalytic oxidation Xu, Fei; Huang, Zhiwei; Hu, Pingping Chemical Communications, Vol. 51, Issue 48 https://doi.org/10.1039/C5CC02476E	journal	January 2015
Operando potassium K-edge X-ray absorption spectroscopy: investigating potassium catalysts during soot oxidation Davies, Catherine J.; Mayer, Alexander; Gabb, Jess Physical Chemistry Chemical Physics, Vol. 22, Issue 34 https://doi.org/10.1039/D0CP01227K	journal	January 2020
Carbon availability triggers fungal nitrogen uptake and transport in arbuscular mycorrhizal symbiosis Fellbaum, C. R.; Gachomo, E. W.; Beesetty, Y. Proceedings of the National Academy of Sciences, Vol. 109, Issue 7 https://doi.org/10.1073/pnas.1118650109	journal	January 2012
K-Extraction from Muscovite by the Isolated Fungi Song, Miao; Pedruzzi, Israel; Peng, Yunxiang Geomicrobiology Journal, Vol. 32, Issue 9 https://doi.org/10.1080/01490451.2014.985409	journal	April 2015
Prospects and challenges in utilization of indigenous rocks and minerals as source of potassium in farming Shirale, Abhay Omprakash; Meena, Bharat Prakash; Gurav, Priya Pandurang Journal of Plant Nutrition, Vol. 42, Issue 19 https://doi.org/10.1080/01904167.2019.1659353	journal	September 2019
Dissolution of Feldspars by Low-Molecular-Weight Aliphatic and Aromatic Acids Manley, E. P.; Evans, L. J. Soil Science, Vol. 141, Issue 2 https://doi.org/10.1097/00010694-198602000-00002	journal	February 1986
K-Edge Absorption Spectra of Ionic Potassium and ItsZ+1Analogy Dutta, C. M.; Huang, H. W. Physical Review Letters, Vol. 44, Issue 10 https://doi.org/10.1103/PhysRevLett.44.643	journal	March 1980
ATHENA , ARTEMIS , HEPHAESTUS : data analysis for X-ray absorption spectroscopy using IFEFFIT Ravel, B.; Newville, M. Journal of Synchrotron Radiation, Vol. 12, Issue 4 https://doi.org/10.1107/S0909049505012719	journal	June 2005
Quantitative local structure determination in mica crystals: ab initio simulations of polarization XANES at the potassium K -edge Xu, Wei; Chen, Dongliang; Chu, Wangsheng Journal of Synchrotron Radiation, Vol. 18, Issue 3 https://doi.org/10.1107/S0909049511002949	journal	March 2011
Potassium and Calcium K ‐Edge XANES in Chemical Compounds and Minerals: Implications for Geological Phase Identification Li, Wenshuai; Liu, Xiao‐Ming; Hu, Yongfeng Geostandards and Geoanalytical Research, Vol. 44, Issue 4 https://doi.org/10.1111/ggr.12351	journal	August 2020
Ectomycorrhizal weathering of the soil minerals muscovite and hornblende van Scholl, Laura; Smits, Mark M.; Hoffland, Ellis New Phytologist, Vol. 171, Issue 4 https://doi.org/10.1111/j.1469-8137.2006.01790.x	journal	September 2006
Aspergillus aculeatus enhances potassium uptake and photosynthetic characteristics in perennial ryegrass by increasing potassium availability Li, Xiaoning; Yin, Yanling; Fan, Shugao Journal of Applied Microbiology, Vol. 132, Issue 1 https://doi.org/10.1111/jam.15186	journal	July 2021
Facultative symbiosis with a saprotrophic soil fungus promotes potassium uptake in American sweetgum trees Peng, Long; Shan, Xiaoliang; Yang, Yuzhan Plant, Cell & Environment, Vol. 44, Issue 8 https://doi.org/10.1111/pce.14053	journal	May 2021
Draft Genome Sequence of Fusarium sp. Strain DS 682, a Novel Fungal Isolate from the Grass Rhizosphere Bhattacharjee, Arunima; Anderson, Lindsey N.; Alfaro, Trinidad Microbiology Resource Announcements, Vol. 10, Issue 1 https://doi.org/10.1128/MRA.00884-20	journal	January 2021
A Mineral-Doped Micromodel Platform Demonstrates Fungal Bridging of Carbon Hot Spots and Hyphal Transport of Mineral-Derived Nutrients Bhattacharjee, Arunima; Qafoku, Odeta; Richardson, Jocelyn A. mSystems, Vol. 7, Issue 6 https://doi.org/10.1128/msystems.00913-22	journal	December 2022
Solubilization of potassium-bearing minerals by a wild-type strain of Bacillus edaphicus and its mutants and increased potassium uptake by wheat Sheng, Xia Fang; He, Lin Yan Canadian Journal of Microbiology, Vol. 52, Issue 1 https://doi.org/10.1139/w05-117	journal	January 2006
Climate Change and Food Systems Vermeulen, Sonja J.; Campbell, Bruce M.; Ingram, John S. I. Annual Review of Environment and Resources, Vol. 37, Issue 1 https://doi.org/10.1146/annurev-environ-020411-130608	journal	November 2012
Weathering of the primary rock-forming minerals: processes, products and rates Wilson, M. J. Clay Minerals, Vol. 39, Issue 3 https://doi.org/10.1180/0009855043930133	journal	September 2004
Sustainable carbon sources for microbial organic acid production with filamentous fungi Dörsam, Stefan; Fesseler, Jana; Gorte, Olga Biotechnology for Biofuels, Vol. 10, Issue 1 https://doi.org/10.1186/s13068-017-0930-x	journal	October 2017
SIXPack a Graphical User Interface for XAS Analysis Using IFEFFIT Webb, S. M. Physica Scripta https://doi.org/10.1238/Physica.Topical.115a01011	journal	January 2005
High Resolution Electron Microscopy of Feldspar Weathering Eggleton, Richard A. Clays and Clay Minerals, Vol. 28, Issue 3 https://doi.org/10.1346/CCMN.1980.0280302	journal	January 1980
Managing Potassium for Organic Crop Production Mikkelsen, Robert L. HortTechnology, Vol. 17, Issue 4 https://doi.org/10.21273/HORTTECH.17.4.455	journal	January 2007
Angular dependence of potassium K-edge XANES spectra of trioctahedral micas: Significance for the determination of the local structure and electronic behavior of the interlayer site Cibin, G. American Mineralogist, Vol. 91, Issue 7 https://doi.org/10.2138/am.2006.2041	journal	July 2006
Interlayer potassium and its neighboring atoms in micas: Crystal-chemical modeling and XANES spectroscopy Brigatti, M. F.; Malferrari, D.; Poppi, M. American Mineralogist, Vol. 93, Issue 5-6 https://doi.org/10.2138/am.2008.2644	journal	May 2008
The role of mycorrhizal associations in plant potassium nutrition Garcia, Kevin; Zimmermann, Sabine D. Frontiers in Plant Science, Vol. 5 https://doi.org/10.3389/fpls.2014.00337	journal	July 2014
Soil Type Affects Organic Acid Production and Phosphorus Solubilization Efficiency Mediated by Several Native Fungal Strains from Mexico Zúñiga-Silgado, Dorcas; Rivera-Leyva, Julio C.; Coleman, Jeffrey J. Microorganisms, Vol. 8, Issue 9 https://doi.org/10.3390/microorganisms8091337	journal	September 2020
Reviews and syntheses: Biological weathering and its consequences at different spatial levels – from nanoscale to global scale Finlay, Roger D.; Mahmood, Shahid; Rosenstock, Nicholas Biogeosciences, Vol. 17, Issue 6 https://doi.org/10.5194/bg-17-1507-2020	journal	March 2020

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54 ENVIRONMENTAL SCIENCES
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XANES spectroscopy
bio-induced mineral transformation
mineral-microbe interactions
simulated soil
synchrotron-XRF imaging
synthetic soil habitat

Saprotrophic Fungus Induces Microscale Mineral Weathering to Source Potassium in a Carbon-Limited Environment

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