Iron transformation mediates phosphate retention across a permafrost thaw gradient

Barczok, Maximilian; Smith, Chelsea; Kinsman-Costello, Lauren; Patzner, Monique; Bryce, Casey; Kappler, Andreas; Singer, David; Herndon, Elizabeth

doi:10.1038/s43247-024-01810-z

Iron transformation mediates phosphate retention across a permafrost thaw gradient

Journal Article · Tue Oct 29 00:00:00 EDT 2024 · Communications Earth & Environment

DOI:https://doi.org/10.1038/s43247-024-01810-z· OSTI ID:2475723

Barczok, Maximilian ^[1]; Smith, Chelsea ^[1]; Kinsman-Costello, Lauren ^[1]; Patzner, Monique ^[2]; ^[3]; ^[4]; Singer, David ^[1]; ^[5]

Kent State Univ., Kent, OH (United States)
Univ. of Tubingen (Germany)
Univ. of Tubingen (Germany); Univ. of Bristol (United Kingdom)
Univ. of Tubingen (Germany); Cluster of Excellence: EXC 2124: Controlling Microbes to Fight Infection, Tubingen (Germany)
Univ. of Tennessee, Knoxville, TN (United States); Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)

Phosphorus limits primary productivity in many (Sub-)Arctic ecosystems and may constrain biological carbon sequestration. Iron (III) oxides strongly bind phosphate in soils but can dissolve under flooded, reducing conditions induced by permafrost thaw and ground collapse. The ability for iron to regulate phosphate storage and solubility in thawing permafrost landscapes remains unclear. Here, iron-rich sediments containing iron oxides and organic-bound iron were incubated with or without added phosphate in soils along a permafrost thaw gradient to evaluate how iron-phosphate associations respond to thaw-induced redox shifts. Iron oxides partially dissolved and released sorbed phosphate when incubated in soils underlain by degraded permafrost. Iron complexed by organic matter remained stable but provided no phosphate binding capacity. Phosphate addition enhanced iron oxide dissolution and phosphorus concentrations in associated microbial biomass. Our study demonstrates that the capacity for iron oxides to immobilize and retain phosphate in permafrost peatlands decreases with permafrost thaw.

View Accepted Manuscript (DOE)

Research Organization:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES). Scientific User Facilities (SUF); National Science Foundation (NSF)

Grant/Contract Number:: AC05-00OR22725; AC02-06CH11357; EAR-1609027; OPP-2006194

OSTI ID:: 2475723

Journal Information:: Communications Earth & Environment, Vol. 5, Issue 1; ISSN 2662-4435

Publisher:: Springer NatureCopyright Statement

Country of Publication:: United States

Language:: English

References (67)

Stoichiometry and temperature sensitivity of methanogenesis and CO ₂ production from saturated polygonal tundra in Barrow, Alaska Roy Chowdhury, Taniya; Herndon, Elizabeth M.; Phelps, Tommy J. Global Change Biology, Vol. 21, Issue 2 https://doi.org/10.1111/gcb.12762	journal	November 2014
Climate change and the permafrost carbon feedback Schuur, E. A. G.; McGuire, A. D.; Schädel, C. Nature, Vol. 520, Issue 7546 https://doi.org/10.1038/nature14338	journal	April 2015
Large stocks of peatland carbon and nitrogen are vulnerable to permafrost thaw Hugelius, Gustaf; Loisel, Julie; Chadburn, Sarah Proceedings of the National Academy of Sciences, Vol. 117, Issue 34 https://doi.org/10.1073/pnas.1916387117	journal	August 2020
Biogeochemical Diversity Along a Riverside Toposequence in Arctic Alaska Giblin, A. E.; Nadelhoffer, K. J.; Shaver, G. R. Ecological Monographs, Vol. 61, Issue 4 https://doi.org/10.2307/2937049	journal	February 1991
Influence of contrasting redox conditions on iron (oxyhydr)oxide transformation and associated phosphate sorption Barczok, Maximilian; Smith, Chelsea; Di Domenico, Nicolle Biogeochemistry, Vol. 166, Issue 2 https://doi.org/10.1007/s10533-023-01094-z	journal	November 2023
Phosphate removal from aqueous solution using iron oxides: Adsorption, desorption and regeneration characteristics Ajmal, Zeeshan; Muhmood, Atif; Usman, Muhammad Journal of Colloid and Interface Science, Vol. 528 https://doi.org/10.1016/j.jcis.2018.05.084	journal	October 2018
The Arctic has warmed nearly four times faster than the globe since 1979 Rantanen, Mika; Karpechko, Alexey Yu.; Lipponen, Antti Communications Earth & Environment, Vol. 3, Issue 1 https://doi.org/10.1038/s43247-022-00498-3	journal	August 2022
Dark Formation of Hydroxyl Radical in Arctic Soil and Surface Waters Page, Sarah E.; Kling, George W.; Sander, Michael Environmental Science & Technology, Vol. 47, Issue 22 https://doi.org/10.1021/es4033265	journal	October 2013
Iron mineral dissolution releases iron and associated organic carbon during permafrost thaw Patzner, Monique S.; Mueller, Carsten W.; Malusova, Miroslava Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-020-20102-6	journal	December 2020
Changes in peat chemistry associated with permafrost thaw increase greenhouse gas production Hodgkins, S. B.; Tfaily, M. M.; McCalley, C. K. Proceedings of the National Academy of Sciences, Vol. 111, Issue 16 https://doi.org/10.1073/pnas.1314641111	journal	April 2014
An evolving view on biogeochemical cycling of iron Kappler, Andreas; Bryce, Casey; Mansor, Muammar Nature Reviews Microbiology, Vol. 19, Issue 6 https://doi.org/10.1038/s41579-020-00502-7	journal	February 2021
Iron-Phosphorus sediment incubation experiment in Stordalen Mire, Abisko, Sweden (2019) Herndon, Elizabeth; Barczok, Maximilian; Smith, Chelsea NSF Arctic Data Center https://doi.org/10.18739/A2PR7MW4N	dataset	January 2024
Element Redistribution along Hydraulic and Redox Gradients of Low-Centered Polygons, Lena Delta, Northern Siberia Fiedler, S.; Wagner, D.; Kutzbach, L. Soil Science Society of America Journal, Vol. 68, Issue 3 https://doi.org/10.2136/sssaj2004.1002	journal	January 2004
Terrestrial phosphorus limitation: mechanisms, implications, and nitrogen–phosphorus interactions Vitousek, Peter M.; Porder, Stephen; Houlton, Benjamin Z. Ecological Applications, Vol. 20, Issue 1 https://doi.org/10.1890/08-0127.1	journal	January 2010
Methane Production Pathway Regulated Proximally by Substrate Availability and Distally by Temperature in a High‐Latitude Mire Complex Chang, Kuang‐Yu; Riley, William J.; Brodie, Eoin L. Journal of Geophysical Research: Biogeosciences, Vol. 124, Issue 10 https://doi.org/10.1029/2019JG005355	journal	October 2019
Trajectory of the Arctic as an integrated system Hinzman, Larry D.; Deal, Clara J.; McGuire, A. David Ecological Applications, Vol. 23, Issue 8 https://doi.org/10.1890/11-1498.1	journal	December 2013
The effect of permafrost thaw on old carbon release and net carbon exchange from tundra Schuur, Edward A. G.; Vogel, Jason G.; Crummer, Kathryn G. Nature, Vol. 459, Issue 7246 https://doi.org/10.1038/nature08031	journal	May 2009
The two-species phosphate adsorption kinetics on goethite Arroyave, Jeison Manuel; Avena, Marcelo; Tan, Wenfeng Chemosphere, Vol. 307 https://doi.org/10.1016/j.chemosphere.2022.135782	journal	November 2022
Phosphorus Cycling in Alaskan Coastal Tundra: A Hypothesis for the Regulation of Nutrient Cycling Chapin, F. S.; Barsdate, R. J.; Barèl, D. Oikos, Vol. 31, Issue 2 https://doi.org/10.2307/3543562	journal	January 1978
Development of a sequential extraction procedure for iron: implications for iron partitioning in continentally derived particulates Poulton, Simon W.; Canfield, Donald E. Chemical Geology, Vol. 214, Issue 3-4 https://doi.org/10.1016/j.chemgeo.2004.09.003	journal	January 2005
Interactions between iron and carbon in permafrost thaw ponds Chauhan, Ankita; Patzner, Monique S.; Bhattacharyya, Amrita Science of The Total Environment, Vol. 946 https://doi.org/10.1016/j.scitotenv.2024.174321	journal	October 2024
Effect of pH on the Formation of Goethite and Hematite from Ferrihydrite Schwertmann, U. Clays and Clay Minerals, Vol. 31, Issue 4 https://doi.org/10.1346/CCMN.1983.0310405	journal	January 1983
Vegetation, climatic changes and net carbon sequestration in a North-Scandinavian subarctic mire over 30 years Malmer, Nils; Johansson, Torbjorn; Olsrud, Maria Global Change Biology, Vol. 0, Issue 0 https://doi.org/10.1111/j.1365-2486.2005.01042.x	journal	October 2005
From Fe(III) Ions to Ferrihydrite and then to Hematite Schwertmann, Udo; Friedl, Josef; Stanjek, Helge Journal of Colloid and Interface Science, Vol. 209, Issue 1 https://doi.org/10.1006/jcis.1998.5899	journal	January 1999
Influence of iron redox cycling on organo-mineral associations in Arctic tundra soil Herndon, Elizabeth; AlBashaireh, Amineh; Singer, David Geochimica et Cosmochimica Acta, Vol. 207 https://doi.org/10.1016/j.gca.2017.02.034	journal	June 2017
A modified single solution method for the determination of phosphate in natural waters Murphy, J.; Riley, J. P. Analytica Chimica Acta, Vol. 27 https://doi.org/10.1016/S0003-2670(00)88444-5	journal	January 1962
Microbial iron cycling is prevalent in water-logged Alaskan Arctic tundra habitats, but sensitive to disturbance Michaud, Alexander B.; Massé, Rémi O.; Emerson, David FEMS Microbiology Ecology, Vol. 99, Issue 3 https://doi.org/10.1093/femsec/fiad013	journal	February 2023
Global Carbon Budget 2019 Friedlingstein, Pierre; Jones, Matthew W.; O'Sullivan, Michael Earth System Science Data, Vol. 11, Issue 4 https://doi.org/10.5194/essd-11-1783-2019	journal	January 2019
Thermodynamic Characterization of Iron Oxide–Aqueous Fe ²⁺ Redox Couples Gorski, Christopher A.; Edwards, Rebecca; Sander, Michael Environmental Science & Technology, Vol. 50, Issue 16 https://doi.org/10.1021/acs.est.6b02661	journal	July 2016
Hydrologic Impacts of Thawing Permafrost—A Review Walvoord, Michelle A.; Kurylyk, Barret L. Vadose Zone Journal, Vol. 15, Issue 6 https://doi.org/10.2136/vzj2016.01.0010	journal	January 2016
Biological and Geochemical Sinks for Phosphorus in Soil from a Wet Tropical Forest Olander, Lydia P.; Vitousek, Peter M. Ecosystems, Vol. 7, Issue 4 https://doi.org/10.1007/s10021-004-0264-y	journal	April 2004
Iron (Oxyhydr)Oxides Serve as Phosphate Traps in Tundra and Boreal Peat Soils Herndon, Elizabeth M.; Kinsman‐Costello, Lauren; Duroe, Kiersten A. Journal of Geophysical Research: Biogeosciences, Vol. 124, Issue 2 https://doi.org/10.1029/2018JG004776	journal	February 2019
The long-term fate of permafrost peatlands under rapid climate warming Swindles, Graeme T.; Morris, Paul J.; Mullan, Donal Scientific Reports, Vol. 5, Issue 1 https://doi.org/10.1038/srep17951	journal	December 2015
Sorption and desorption of organic matter in soils as affected by phosphate Spohn, Marie; Diáková, Kateřina; Aburto, Felipe Geoderma, Vol. 405 https://doi.org/10.1016/j.geoderma.2021.115377	journal	January 2022
XANES Investigation of Phosphate Sorption in Single and Binary Systems of Iron and Aluminum Oxide Minerals Khare, Nidhi; Hesterberg, Dean; Martin, James D. Environmental Science & Technology, Vol. 39, Issue 7 https://doi.org/10.1021/es049237b	journal	April 2005
Bioavailable Soil Phosphorus Decreases with Increasing Elevation in a Subarctic Tundra Landscape Vincent, Andrea G.; Sundqvist, Maja K.; Wardle, David A. PLoS ONE, Vol. 9, Issue 3 https://doi.org/10.1371/journal.pone.0092942	journal	March 2014
Redox-active antibiotics enhance phosphorus bioavailability McRose, Darcy L.; Newman, Dianne K. Science, Vol. 371, Issue 6533 https://doi.org/10.1126/science.abd1515	journal	March 2021
Rapid Nutrient Release from Permafrost Thaw in Arctic Aquatic Ecosystems Reyes, Francisco R.; Lougheed, Vanessa L. Arctic, Antarctic, and Alpine Research, Vol. 47, Issue 1 https://doi.org/10.1657/AAAR0013-099	journal	February 2015
Recent pause in the growth rate of atmospheric CO2 due to enhanced terrestrial carbon uptake Keenan, Trevor F.; Prentice, I. Colin; Canadell, Josep G. Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms13428	journal	November 2016
Sorption and desorption of dissolved organic phosphorus onto iron (oxyhydr)oxides in seawater Ruttenberg, K. C.; Sulak, D. J. Geochimica et Cosmochimica Acta, Vol. 75, Issue 15 https://doi.org/10.1016/j.gca.2010.10.033	journal	August 2011
Phosphorus Interactions with Iron in Undisturbed and Disturbed Arctic Tundra Ecosystems Berens, Matthew John; Michaud, Alexander Bryce; VanderJeugdt, Erin Environmental Science & Technology, Vol. 58, Issue 26 https://doi.org/10.1021/acs.est.3c09072	journal	June 2024
Seasonal Fluctuations in Iron Cycling in Thawing Permafrost Peatlands Patzner, Monique S.; Kainz, Nora; Lundin, Erik Environmental Science & Technology, Vol. 56, Issue 7 https://doi.org/10.1021/acs.est.1c06937	journal	March 2022
Chloroform fumigation and the release of soil nitrogen: A rapid direct extraction method to measure microbial biomass nitrogen in soil Brookes, P. C.; Landman, Andrea; Pruden, G. Soil Biology and Biochemistry, Vol. 17, Issue 6 https://doi.org/10.1016/0038-0717(85)90144-0	journal	January 1985
Adsorption of phosphorus on sediments from the Three-Gorges Reservoir (China) and the relation with sediment compositions Wang, Ying; Shen, Zhenyao; Niu, Junfeng Journal of Hazardous Materials, Vol. 162, Issue 1 https://doi.org/10.1016/j.jhazmat.2008.05.013	journal	February 2009
Geochemical drivers of organic matter decomposition in arctic tundra soils Herndon, Elizabeth M.; Yang, Ziming; Bargar, John Biogeochemistry, Vol. 126, Issue 3 https://doi.org/10.1007/s10533-015-0165-5	journal	December 2015
Decadal vegetation changes in a northern peatland, greenhouse gas fluxes and net radiative forcing Johansson, TorbjÖRn; Malmer, Nils; Crill, Patrick M. Global Change Biology, Vol. 12, Issue 12 https://doi.org/10.1111/j.1365-2486.2006.01267.x	journal	December 2006
The contribution of Fe(III) and humic acid reduction to ecosystem respiration in drained thaw lake basins of the Arctic Coastal Plain: Fe(III) AND HA REDUCTION IN THE ARCTIC Lipson, David A.; Raab, Theodore K.; Goria, Dominic Global Biogeochemical Cycles, Vol. 27, Issue 2 https://doi.org/10.1002/gbc.20038	journal	May 2013
Transformation of Two-Line Ferrihydrite to Goethite and Hematite as a Function of pH and Temperature Das, Soumya; Hendry, M. Jim; Essilfie-Dughan, Joseph Environmental Science & Technology, Vol. 45, Issue 1 https://doi.org/10.1021/es101903y	journal	January 2011
Impact of iron–organic matter complexes on aqueous phosphate concentrations Sundman, Anneli; Karlsson, Torbjörn; Sjöberg, Staffan Chemical Geology, Vol. 426 https://doi.org/10.1016/j.chemgeo.2016.02.008	journal	May 2016
Nutrients Alter Methane Production and Oxidation in a Thawing Permafrost Mire Kashi, N. Niloufar; Hobbie, Erik A.; Varner, Ruth K. Ecosystems, Vol. 26, Issue 2 https://doi.org/10.1007/s10021-022-00758-5	journal	April 2022
Microscale soil structures foster organic matter stabilization in permafrost soils Mueller, Carsten W.; Hoeschen, Carmen; Steffens, Markus Geoderma, Vol. 293 https://doi.org/10.1016/j.geoderma.2017.01.028	journal	May 2017
Thawing permafrost and thicker active layers in sub-arctic Sweden Åkerman, H. Jonas; Johansson, Margareta Permafrost and Periglacial Processes, Vol. 19, Issue 3 https://doi.org/10.1002/ppp.626	journal	July 2008
Permafrost soils and carbon cycling Ping, C. L.; Jastrow, J. D.; Jorgenson, M. T. SOIL, Vol. 1, Issue 1 https://doi.org/10.5194/soil-1-147-2015	journal	January 2015
Divergent responses of permafrost peatlands to recent climate change Sim, Thomas G.; Swindles, Graeme T.; Morris, Paul J. Environmental Research Letters, Vol. 16, Issue 3 https://doi.org/10.1088/1748-9326/abe00b	journal	February 2021
Biological Phosphorus Cycling in Arctic and Alpine Soils Weintraub, Michael N. Phosphorous in Action: Biological Processes in Soil Phosphorous Cycling, p. 295-316 https://doi.org/10.1007/978-3-642-15271-9_12	book	October 2010
Soil redox dynamics under dynamic hydrologic regimes - A review Zhang, Zengyu; Furman, Alex Science of The Total Environment, Vol. 763 https://doi.org/10.1016/j.scitotenv.2020.143026	journal	April 2021
Vegetation Succession, Carbon Accumulation and Hydrological Change in Subarctic Peatlands, Abisko, Northern Sweden Gałka, Mariusz; Szal, Marta; Watson, Elizabeth J. Permafrost and Periglacial Processes, Vol. 28, Issue 4 https://doi.org/10.1002/ppp.1945	journal	April 2017
In situ Methane Production from Acid Peat in Plant Communities with Different Moisture Regimes in a Subarctic Mire Svensson, Bo H.; Rosswall, Thomas Oikos, Vol. 43, Issue 3 https://doi.org/10.2307/3544151	journal	December 1984
Microbial iron cycling during palsa hillslope collapse promotes greenhouse gas emissions before complete permafrost thaw Patzner, Monique S.; Logan, Merritt; McKenna, Amy M. Communications Earth & Environment, Vol. 3, Issue 1 https://doi.org/10.1038/s43247-022-00407-8	journal	April 2022
Phosphorus Fractionation Responds to Dynamic Redox Conditions in a Humid Tropical Forest Soil Lin, Yang; Bhattacharyya, Amrita; Campbell, Ashley N. Journal of Geophysical Research: Biogeosciences, Vol. 123, Issue 9 https://doi.org/10.1029/2018JG004420	journal	September 2018
Iron:phosphorus ratio in surface sediment as an indicator of phosphate release from aerobic sediments in shallow lakes Jensen, H. S.; Kristensen, P.; Jeppesen, E. Hydrobiologia, Vol. 235-236, Issue 1 https://doi.org/10.1007/BF00026261	journal	July 1992
Investigation of phosphate adsorption onto ferrihydrite by X-ray Photoelectron Spectroscopy Mallet, M.; Barthélémy, K.; Ruby, C. Journal of Colloid and Interface Science, Vol. 407 https://doi.org/10.1016/j.jcis.2013.06.049	journal	October 2013
Characterization of Iron(III) in Organic Soils Using Extended X-ray Absorption Fine Structure Spectroscopy Karlsson, Torbjörn; Persson, Per; Skyllberg, Ulf Environmental Science & Technology, Vol. 42, Issue 15 https://doi.org/10.1021/es800322j	journal	August 2008
Differential controls by climate and substrate over the heterotrophic and rhizospheric components of soil respiration Scott-Denton, Laura E.; Rosenstiel, Todd N.; Monson, Russell K. Global Change Biology, Vol. 12, Issue 2 https://doi.org/10.1111/j.1365-2486.2005.01064.x	journal	February 2006
Future productivity and carbon storage limited by terrestrial nutrient availability Wieder, William R.; Cleveland, Cory C.; Smith, W. Kolby Nature Geoscience, Vol. 8, Issue 6 https://doi.org/10.1038/ngeo2413	journal	April 2015
Phosphate Imposed Limitations on Biological Reduction and Alteration of Ferrihydrite Borch, Thomas; Masue, Yoko; Kukkadapu, Ravi K. Environmental Science & Technology, Vol. 41, Issue 1 https://doi.org/10.1021/es060695p	journal	January 2007
A comparison of lignin-degrading enzyme activities in forest floor layers across a global climatic gradient Fujii, Kazumichi; Nakada, Yuji; Umezawa, Kiwamu Soil Ecology Letters, Vol. 2, Issue 4 https://doi.org/10.1007/s42832-020-0042-6	journal	July 2020

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