Calcareous organic matter coatings sequester siderophores in alkaline soils

Boiteau, Rene M.; Kukkadapu, Ravi K.; Cliff, John B.; Smallwood, Chuck R.; Kovarik, Libor; Wirth, Mark G.; Engelhard, Mark H.; Varga, Tamas; Dohnalkova, Alice; Perea, Daniel E.; Wietsma, Thomas W.; Moran, James J.; Hofmockel, Kirsten S.

doi:10.1016/j.scitotenv.2020.138250

Calcareous organic matter coatings sequester siderophores in alkaline soils

Journal Article · Thu Mar 26 00:00:00 EDT 2020 · Science of the Total Environment

DOI:https://doi.org/10.1016/j.scitotenv.2020.138250· OSTI ID:1631325

^[1]; ^[2]; Cliff, John B. ^[2]; ^[3]; Kovarik, Libor ^[2]; Wirth, Mark G. ^[2]; ^[2]; ^[2]; Dohnalkova, Alice ^[2]; ^[2]; Wietsma, Thomas W. ^[2]; ^[2]; ^[4]

Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Environmental Molecular Sciences Lab. (EMSL); Oregon State Univ., Corvallis, OR (United States)
Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Environmental Molecular Sciences Lab. (EMSL)
Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Environmental Molecular Sciences Lab. (EMSL); Sandia National Lab. (SNL-NM), Albuquerque, NM (United States)
Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Environmental Molecular Sciences Lab. (EMSL); Iowa State Univ., Ames, IA (United States)

Although most studies on organic matter stabilization in soils have focused on adsorption to aluminosilicate and iron oxide minerals due to their strong interactions with organic nucleophiles, stabilization within alkaline soils has been empirically correlated with exchangeable Ca concentrations. Yet the extent of competing processes within natural soil remain unclear. We employed sub-micron scale techniques to investigate the minerology and organic carbon on individual fine particles within an alkaline soil from Eastern Washington. XRD, Mössbauer spectroscopy, TEM-EDX-SAED, and XPS analysis demonstrated a mineral assemblage dominated by quartz, feldspars, iron oxides, and calcite. Although exposed Si, Al, and Fe accounted for ~30% of the surface elemental composition, most of the organic carbon and nitrogen was associated with Ca-rich coatings. Adsorption isotherms of two siderophores with the same soil showed greater adsorption of pyoverdine compared with less polar enterobactin. Using NanoSIMS to map the distribution of isotopically labeled siderophores across the surfaces of fine grains, we observed a preference for binding to surfaces heavily coated with organic matter. We propose a mechanism of adsorption by which organic molecules aggregate within calcareous soils via calcium bridging, favoring the stabilization of larger molecules with a greater number of nucleophilic functional groups.

View Accepted Manuscript (DOE)

Research Organization:: Pacific Northwest National Laboratory (PNNL), Richland, WA (United States). Environmental Molecular Sciences Laboratory (EMSL); Sandia National Laboratories (SNL-NM), Albuquerque, NM (United States)

Sponsoring Organization:: USDOE Laboratory Directed Research and Development (LDRD) Program; USDOE National Nuclear Security Administration (NNSA); USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC04-94AL85000; AC05-76RL01830

OSTI ID:: 1631325

Alternate ID(s):: OSTI ID: 1772024

Report Number(s):: PNNL-SA--147851; SAND--2021-2763J

Journal Information:: Science of the Total Environment, Journal Name: Science of the Total Environment Journal Issue: C Vol. 724; ISSN 0048-9697

Publisher:: ElsevierCopyright Statement

Country of Publication:: United States

Language:: English

References (51)

Differentiating calcium carbonate polymorphs by surface analysis techniques-an XPS and TOF-SIMS study Ni, Ming; Ratner, Buddy D. Surface and Interface Analysis, Vol. 40, Issue 10 https://doi.org/10.1002/sia.2904	journal	October 2008
Surface Complexation at the TiO2(anatase)/Aqueous Solution Interface: Chemisorption of Catechol Rodrı́guez, Raul; Blesa, Miguel A.; Regazzoni, Alberto E. Journal of Colloid and Interface Science, Vol. 177, Issue 1 https://doi.org/10.1006/jcis.1996.0012	journal	January 1996
Calcium-mediated stabilisation of soil organic carbon Rowley, Mike C.; Grand, Stéphanie; Verrecchia, Éric P. Biogeochemistry, Vol. 137, Issue 1-2 https://doi.org/10.1007/s10533-017-0410-1	journal	December 2017
Beyond clay: towards an improved set of variables for predicting soil organic matter content Rasmussen, Craig; Heckman, Katherine; Wieder, William R. Biogeochemistry, Vol. 137, Issue 3 https://doi.org/10.1007/s10533-018-0424-3	journal	February 2018
The fate of siderophores: antagonistic environmental interactions in exudate-mediated micronutrient uptake Harrington, James M.; Duckworth, Owen W.; Haselwandter, Kurt BioMetals, Vol. 28, Issue 3 https://doi.org/10.1007/s10534-015-9821-4	journal	January 2015
Adsorption by goethite (α-FeOOH) of humic substances from three different lakes Tipping, E. Chemical Geology, Vol. 33, Issue 1-4 https://doi.org/10.1016/0009-2541(81)90086-3	journal	January 1981
The adsorption of aquatic humic substances by iron oxides Tipping, E. Geochimica et Cosmochimica Acta, Vol. 45, Issue 2 https://doi.org/10.1016/0016-7037(81)90162-9	journal	February 1981
Solution stability constants of some metal complexes of derivatives of catechol Athavale, V. T.; Prabhu, L. H.; Vartak, D. G. Journal of Inorganic and Nuclear Chemistry, Vol. 28, Issue 5 https://doi.org/10.1016/0022-1902(66)80450-5	journal	May 1966
Reaction of forest floor organic matter at goethite, birnessite and smectite surfaces Chorover, Jon; Amistadi, Mary Kay Geochimica et Cosmochimica Acta, Vol. 65, Issue 1 https://doi.org/10.1016/S0016-7037(00)00511-1	journal	January 2001
Assessing the surface composition of soil particles from some Podzolic soils by X-ray photoelectron spectroscopy Yuan, G.; Soma, M.; Seyama, H. Geoderma, Vol. 86, Issue 3-4 https://doi.org/10.1016/S0016-7061(98)00049-4	journal	November 1998
The role of DOM sorption to mineral surfaces in the preservation of organic matter in soils Kaiser, Klaus; Guggenberger, Georg Organic Geochemistry, Vol. 31, Issue 7-8 https://doi.org/10.1016/S0146-6380(00)00046-2	journal	July 2000
Coordination of calcium by iron enterobactin Hider, R. C.; Mohd-Nor, A. Rahim; Silver, Jack Journal of Inorganic Biochemistry, Vol. 17, Issue 3 https://doi.org/10.1016/S0162-0134(00)80099-9	journal	January 1982
TEM-EDX investigation on Zn- and Pb-contaminated soils Buatier, Martine D.; Sobanska, Sophie; Elsass, Françoise Applied Geochemistry, Vol. 16, Issue 9-10 https://doi.org/10.1016/S0883-2927(01)00015-4	journal	July 2001
In situ infrared spectroscopic analysis of the adsorption of aromatic carboxylic acids to TiO2, ZrO2, Al2O3, and Ta2O5 from aqueous solutions Dobson, Kevin D.; McQuillan, A. James Spectrochimica Acta Part A: Molecular and Biomolecular Spectroscopy, Vol. 56, Issue 3 https://doi.org/10.1016/S1386-1425(99)00154-7	journal	February 2000
Mineral–Organic Associations: Formation, Properties, and Relevance in Soil Environments Kleber, Markus; Eusterhues, Karin; Keiluweit, Marco https://doi.org/10.1016/bs.agron.2014.10.005	book	December 2014
Biodegradation of forest floor organic matter bound to minerals via different binding mechanisms Mikutta, Robert; Mikutta, Christian; Kalbitz, Karsten Geochimica et Cosmochimica Acta, Vol. 71, Issue 10 https://doi.org/10.1016/j.gca.2007.03.002	journal	May 2007
Properties and reactivity of Fe-organic matter associations formed by coprecipitation versus adsorption: Clues from arsenate batch adsorption Mikutta, Robert; Lorenz, Dennis; Guggenberger, Georg Geochimica et Cosmochimica Acta, Vol. 144 https://doi.org/10.1016/j.gca.2014.08.026	journal	November 2014
Root-driven weathering impacts on mineral-organic associations in deep soils over pedogenic time scales Garcia Arredondo, Mariela; Lawrence, Corey R.; Schulz, Marjorie S. Geochimica et Cosmochimica Acta, Vol. 263 https://doi.org/10.1016/j.gca.2019.07.030	journal	October 2019
Distinguishing black carbon from biogenic humic substances in soil clay fractions Laird, David A.; Chappell, Mark A.; Martens, Dean A. Geoderma, Vol. 143, Issue 1-2 https://doi.org/10.1016/j.geoderma.2007.10.025	journal	January 2008
Edaphic controls on soil organic carbon stocks in restored grasslands O'Brien, Sarah L.; Jastrow, Julie D.; Grimley, David A. Geoderma, Vol. 251-252 https://doi.org/10.1016/j.geoderma.2015.03.023	journal	August 2015
Submicron scale imaging of soil organic matter dynamics using NanoSIMS – From single particles to intact aggregates Mueller, Carsten W.; Kölbl, Angelika; Hoeschen, Carmen Organic Geochemistry, Vol. 42, Issue 12 https://doi.org/10.1016/j.orggeochem.2011.06.003	journal	January 2012
Effect of exchangeable cation concentration on sorption and desorption of dissolved organic carbon in saline soils Setia, Raj; Rengasamy, Pichu; Marschner, Petra Science of The Total Environment, Vol. 465 https://doi.org/10.1016/j.scitotenv.2013.01.010	journal	November 2013
Iron mineralogy and uranium-binding environment in the rhizosphere of a wetland soil Kaplan, Daniel I.; Kukkadapu, Ravi; Seaman, John C. Science of The Total Environment, Vol. 569-570 https://doi.org/10.1016/j.scitotenv.2016.06.120	journal	November 2016
Carbon and nitrogen mineralization in acidic, limed and calcareous agricultural soils: Apparent and actual effects Bertrand, Isabelle; Delfosse, Olivier; Mary, Bruno Soil Biology and Biochemistry, Vol. 39, Issue 1 https://doi.org/10.1016/j.soilbio.2006.07.016	journal	January 2007
Cycling downwards – dissolved organic matter in soils Kaiser, Klaus; Kalbitz, Karsten Soil Biology and Biochemistry, Vol. 52 https://doi.org/10.1016/j.soilbio.2012.04.002	journal	September 2012
Solid-Phase Fe Speciation along the Vertical Redox Gradients in Floodplains using XAS and Mössbauer Spectroscopies Chen, Chunmei; Kukkadapu, Ravi K.; Lazareva, Olesya Environmental Science & Technology, Vol. 51, Issue 14 https://doi.org/10.1021/acs.est.7b00700	journal	June 2017
Microbial Iron Acquisition: Marine and Terrestrial Siderophores Sandy, Moriah; Butler, Alison Chemical Reviews, Vol. 109, Issue 10 https://doi.org/10.1021/cr9002787	journal	October 2009
Molecular Structure in Soil Humic Substances: The New View Sutton, Rebecca; Sposito, Garrison Environmental Science & Technology, Vol. 39, Issue 23 https://doi.org/10.1021/es050778q	journal	December 2005
NanoSIMS Study of Organic Matter Associated with Soil Aggregates: Advantages, Limitations, and Combination with STXM Remusat, Laurent; Hatton, Pierre-Joseph; Nico, Peter S. Environmental Science & Technology, Vol. 46, Issue 7 https://doi.org/10.1021/es203745k	journal	March 2012
Soft X-ray Spectromicroscopy Study of Mineral-Organic Matter Associations in Pasture Soil Clay Fractions Chen, Chunmei; Dynes, James J.; Wang, Jian Environmental Science & Technology, Vol. 48, Issue 12 https://doi.org/10.1021/es405485a	journal	May 2014
Geochemical Processes Constraining Iron Uptake in Strategy II Fe Acquisition Schenkeveld, W. D. C.; Schindlegger, Y.; Oburger, E. Environmental Science & Technology, Vol. 48, Issue 21 https://doi.org/10.1021/es5031728	journal	October 2014
Solution equilibria of enterobactin and metal-enterobactin complexes Loomis, Lawrence D.; Raymond, Kenneth N. Inorganic Chemistry, Vol. 30, Issue 5 https://doi.org/10.1021/ic00005a008	journal	March 1991
Computational Studies of Catechol and Water Interactions with Titanium Oxide Nanoparticles Redfern, P. C.; Zapol, P.; Curtiss, L. A. The Journal of Physical Chemistry B, Vol. 107, Issue 41 https://doi.org/10.1021/jp0303669	journal	October 2003
Adsorption of Enterobactin to Metal Oxides and the Role of Siderophores in Bacterial Adhesion to Metals Upritchard, Hamish G.; Yang, Jing; Bremer, Philip J. Langmuir, Vol. 27, Issue 17 https://doi.org/10.1021/la202352j	journal	September 2011
Adsorption to Metal Oxides of the Pseudomonas aeruginosa Siderophore Pyoverdine and Implications for Bacterial Biofilm Formation on Metals Upritchard, Hamish G.; Yang, Jing; Bremer, Philip J. Langmuir, Vol. 23, Issue 13 https://doi.org/10.1021/la7004024	journal	June 2007
Submicron structures provide preferential spots for carbon and nitrogen sequestration in soils Vogel, Cordula; Mueller, Carsten W.; Höschen, Carmen Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms3947	journal	January 2014
Soil wettability can be explained by the chemical composition of particle interfaces - An XPS study Woche, Susanne K.; Goebel, Marc-O.; Mikutta, Robert Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/srep42877	journal	February 2017
Siderophore profiling of co-habitating soil bacteria by ultra-high resolution mass spectrometry Boiteau, Rene M.; Fansler, Sarah J.; Farris, Yuliya Metallomics, Vol. 11, Issue 1 https://doi.org/10.1039/C8MT00252E	journal	January 2019
Association of desferrioxamine with humic substances and their interaction with cadmium(II) as studied by pyrolysis–gas chromatography–mass spectrometry and nuclear magnetic resonance spectroscopy† Higashi, Richard. M.; Fan, Teresa. W-M.; Lane, Andrew N. The Analyst, Vol. 123, Issue 5 https://doi.org/10.1039/a708177d	journal	January 1998
Chemistry and biology of siderophores Hider, Robert C.; Kong, Xiaole Natural Product Reports, Vol. 27, Issue 5 https://doi.org/10.1039/b906679a	journal	January 2010
Surface analysis of soil material by X-ray photoelectron spectroscopy Gerin, P. A.; Genet, M. J.; Herbillon, A. J. European Journal of Soil Science, Vol. 54, Issue 3 https://doi.org/10.1046/j.1365-2389.2003.00537.x	journal	September 2003
The role of Ca-organic interactions in soil aggregate stability .III. Mechanisms and models Muneer, M.; Oades, Jm Soil Research, Vol. 27, Issue 2 https://doi.org/10.1071/SR9890411	journal	January 1989
Physical and chemical protection of soil organic carbon in three agricultural soils with different contents of calcium carbonate Clough, A.; Skjemstad, J. O. Soil Research, Vol. 38, Issue 5 https://doi.org/10.1071/SR99102	journal	January 2000
Complexation of Humic Substances with Oxides of Iron and Aluminum Varadachari, Chandrika; Chattopadhyay, Tarit; Ghosh, Kunal Soil Science, Vol. 162, Issue 1 https://doi.org/10.1097/00010694-199701000-00005	journal	January 1997
Clay-sized organo-mineral complexes in a cultivation chronosequence: revisiting the concept of the 'primary organo-mineral complex' Chenu, C.; Plante, A. F. European Journal of Soil Science, Vol. 57, Issue 4 https://doi.org/10.1111/j.1365-2389.2006.00834.x	journal	August 2006
Effects of organic matter and calcium on soil structural stability Wuddivira, M. N.; Camps-Roach, G. European Journal of Soil Science, Vol. 58, Issue 3 https://doi.org/10.1111/j.1365-2389.2006.00861.x	journal	June 2007
Molecular dynamics simulation of cationic complexation with natural organic matter Kalinichev, A. G.; Kirkpatrick, R. J. European Journal of Soil Science, Vol. 58, Issue 4 https://doi.org/10.1111/j.1365-2389.2007.00929.x	journal	August 2007
Mineral control of organic carbon mineralization in a range of temperate conifer forest soils Rasmussen, Craig; Southard, Randal J.; Horwath, William R. Global Change Biology, Vol. 12, Issue 5 https://doi.org/10.1111/j.1365-2486.2006.01132.x	journal	May 2006
Vacuum Cleaved Calcium Carbonate by XPS Engelhard, Mark; Baer, Don Surface Science Spectra, Vol. 6, Issue 2 https://doi.org/10.1116/1.1247917	journal	April 1999
Mineral Surface Control of Organic Carbon in Black Shale Kennedy, M. J. Science, Vol. 295, Issue 5555 https://doi.org/10.1126/science.1066611	journal	January 2002
Molecular and Microscopic Insights into the Formation of Soil Organic Matter in a Red Pine Rhizosphere Dohnalkova, Alice; Tfaily, Malak; Smith, A. Soils, Vol. 1, Issue 1 https://doi.org/10.3390/soils1010004	journal	August 2017

Similar Records

Corrosion inhibition of iron in acid solutions by biological siderophores

Journal Article · Mon May 01 00:00:00 EDT 1995 · Journal of the Electrochemical Society · OSTI ID:63186

Siderophore profiling of co-habitating soil bacteria by ultra-high resolution mass spectrometry

Journal Article · Tue Nov 13 19:00:00 EST 2018 · Metallomics · OSTI ID:1507754

Related Subjects

54 ENVIRONMENTAL SCIENCES

Calcareous organic matter coatings sequester siderophores in alkaline soils

Citation Formats

References (51)

Similar Records

Related Subjects