Moisture-mineral interactions drive bacterial and organic matter turnover in glacier-sourced riparian sediments undergoing pedogenesis

Smith, A. Peyton; Rod, Kenton A.; Campell, Tayte; Patel, Kaizad F.; Dohnalkova, Alice; Tfaily, Malak; Renteria, Lupita; Bailey, Vanessa L.; Renslow, Ryan

doi:10.1016/j.soilbio.2024.109617

Title: Moisture-mineral interactions drive bacterial and organic matter turnover in glacier-sourced riparian sediments undergoing pedogenesis

Journal Article · 09 October 2024 · Soil Biology and Biochemistry

DOI: https://doi.org/10.1016/j.soilbio.2024.109617 · OSTI ID:2514403

^[1];

^[2]; Campell, Tayte ^[2];

^[2]; Dohnalkova, Alice ^[3];

^[4]; Renteria, Lupita ^[2];

^[2]; Renslow, Ryan ^[2]

Texas A & M Univ., College Station, TX (United States)
Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)
Pacific Northwest National Laboratory (PNNL), Richland, WA (United States). Environmental Molecular Sciences Laboratory (EMSL)
Univ. of Arizona, Tucson, AZ (United States)

Glacial recession is occurring at unprecedented rates resulting in increased sediment accumula-tions in some riverine ecosystems. Increased sediment deposition has implications for ecosystem stability (e.g., floods and river paths) and environmental services (e.g., carbon sequestration). Soils and sediments have an enormous potential to retain carbon (C), predominantly due to sorp-tion to mineral surfaces. However, C persistence may be sensitive to climate-change induced temperature and moisture variations. We coupled ultrahigh resolution organic matter composition classification with bacterial characterization and respiration measurements to test the combined effects of temperature (4 vs 20°C) and moisture (50 vs 100% water-filled pore space) on C turn-over in sediments maintained under different mineralogical conditions (illite-amended vs non-amended). Here we show that the inhibition of CO₂ emissions from the combined effect of in-creased moisture content and illite was reflected in the turnover of key molecular signatures, such as the nominal oxidation state of C, often irrespective of temperature. However, shifts in bacteri-al communities from a coupled moisture-mineral interaction, were temperature-dependent. Our results highlight the importance of moisture in driving mineral-organic interactions and suggest that C in clay-rich, water-saturated sediments is both thermodynamically unfavorable and miner-al-protected from microbial consumption.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)

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

Grant/Contract Number:: AC05-76RL01830

OSTI ID:: 2514403

Report Number(s):: PNNL-SA--190100

Journal Information:: Soil Biology and Biochemistry, Journal Name: Soil Biology and Biochemistry Journal Issue: _ Vol. 199; ISSN 0038-0717

Publisher:: ElsevierCopyright Statement

Country of Publication:: United States

Language:: English

References (58)

Separate effects of flooding and anaerobiosis on soil greenhouse gas emissions and redox sensitive biogeochemistry: Separate flooding effects on soil fluxes McNicol, Gavin; Silver, Whendee L. Journal of Geophysical Research: Biogeosciences, Vol. 119, Issue 4 https://doi.org/10.1002/2013JG002433	journal	April 2014
Geomorphic Controls on Floodplain Soil Organic Carbon in the Yukon Flats, Interior Alaska, From Reach to River Basin Scales Lininger, K. B.; Wohl, E.; Rose, J. R. Water Resources Research, Vol. 54, Issue 3 https://doi.org/10.1002/2017WR022042	journal	March 2018
Inland waters and their role in the carbon cycle of Alaska Stackpoole, Sarah M.; Butman, David E.; Clow, David W. Ecological Applications, Vol. 27, Issue 5 https://doi.org/10.1002/eap.1552	journal	July 2017
Organo-mineral associations in temperate soils: Integrating biology, mineralogy, and organic matter chemistry Kögel-Knabner, Ingrid; Guggenberger, Georg; Kleber, Markus Journal of Plant Nutrition and Soil Science, Vol. 171, Issue 1 https://doi.org/10.1002/jpln.200700048	journal	February 2008
From mass to structure: an aromaticity index for high-resolution mass data of natural organic matter Koch, B. P.; Dittmar, T. Rapid Communications in Mass Spectrometry, Vol. 30, Issue 1 https://doi.org/10.1002/rcm.7433	journal	December 2015
Water‐dispersible nanocolloids and higher temperatures promote the release of carbon from riparian soil Rod, Kenton A.; Smith, A. Peyton; Leng, Weinan Vadose Zone Journal, Vol. 19, Issue 1 https://doi.org/10.1002/vzj2.20077	journal	January 2020
Plumbing the Global Carbon Cycle: Integrating Inland Waters into the Terrestrial Carbon Budget Cole, J. J.; Prairie, Y. T.; Caraco, N. F. Ecosystems, Vol. 10, Issue 1 https://doi.org/10.1007/s10021-006-9013-8	journal	February 2007
Relationships between mineral surfaces and organic carbon concentrations in soils and sediments Mayer, Lawrence M. Chemical Geology, Vol. 114, Issue 3-4 https://doi.org/10.1016/0009-2541(94)90063-9	journal	June 1994
Dissolved organic matter in soil: challenging the paradigm of sorptive preservation Guggenberger, Georg; Kaiser, Klaus Geoderma, Vol. 113, Issue 3-4 https://doi.org/10.1016/S0016-7061(02)00366-X	journal	May 2003
Stabilization and destabilization of soil organic matter: mechanisms and controls Sollins, Phillip; Homann, Peter; Caldwell, Bruce A. Geoderma, Vol. 74, Issue 1-2 https://doi.org/10.1016/S0016-7061(96)00036-5	journal	November 1996
An inter-laboratory comparison of ten different ways of measuring soil microbial biomass C Beck, T.; Joergensen, R. G.; Kandeler, E. Soil Biology and Biochemistry, Vol. 29, Issue 7 https://doi.org/10.1016/S0038-0717(97)00030-8	journal	July 1997
Influence of sorption on the biological utilization of two simple carbon substrates Jones, D. L.; Edwards, A. C. Soil Biology and Biochemistry, Vol. 30, Issue 14 https://doi.org/10.1016/S0038-0717(98)00060-1	journal	December 1998
Role of the soil matrix and minerals in protecting natural organic materials against biological attack Baldock, J. A.; Skjemstad, J. O. Organic Geochemistry, Vol. 31, Issue 7-8 https://doi.org/10.1016/S0146-6380(00)00049-8	journal	July 2000
Life at the oxic–anoxic interface: microbial activities and adaptations Brune, A. FEMS Microbiology Reviews, Vol. 24, Issue 5 https://doi.org/10.1016/S0168-6445(00)00054-1	journal	December 2000
Effect of long-term fertilization on C mineralization and production of CH4 and CO2 under anaerobic incubation from bulk samples and particle size fractions of a typical paddy soil Zheng, Jufeng; Zhang, Xuhui; Li, Lianqing Agriculture, Ecosystems & Environment, Vol. 120, Issue 2-4 https://doi.org/10.1016/j.agee.2006.07.008	journal	May 2007
Organic matter in small mesopores in sediments and soils Mayer, Lawrence M.; Schick, Linda L.; Hardy, Kathleen R. Geochimica et Cosmochimica Acta, Vol. 68, Issue 19 https://doi.org/10.1016/j.gca.2004.03.019	journal	October 2004
Biogeochemistry of dissolved organic matter in an anoxic intertidal creek bank Seidel, Michael; Beck, Melanie; Riedel, Thomas Geochimica et Cosmochimica Acta, Vol. 140 https://doi.org/10.1016/j.gca.2014.05.038	journal	September 2014
Characterization of dissolved organic matter in Lake Superior and its watershed using ultrahigh resolution mass spectrometry Minor, Elizabeth C.; Steinbring, Carla J.; Longnecker, Krista Organic Geochemistry, Vol. 43 https://doi.org/10.1016/j.orggeochem.2011.11.007	journal	February 2012
Lactovum miscens gen. nov., sp. nov., an aerotolerant, psychrotolerant, mixed-fermentative anaerobe from acidic forest soil Matthies, Carola; Gößner, Anita; Acker, Georg Research in Microbiology, Vol. 155, Issue 10 https://doi.org/10.1016/j.resmic.2004.06.006	journal	December 2004
Response of fermenting bacterial and methanogenic archaeal communities in paddy soil to progressing rice straw degradation Ji, Yang; Liu, Pengfei; Conrad, Ralf Soil Biology and Biochemistry, Vol. 124 https://doi.org/10.1016/j.soilbio.2018.05.029	journal	September 2018
Soil carbon dynamics during drying vs. rewetting: Importance of antecedent moisture conditions Patel, Kaizad F.; Myers-Pigg, Allison; Bond-Lamberty, Ben Soil Biology and Biochemistry, Vol. 156 https://doi.org/10.1016/j.soilbio.2021.108165	journal	May 2021
Automated Analysis of Electrospray Ionization Fourier Transform Ion Cyclotron Resonance Mass Spectra of Natural Organic Matter Kujawinski, Elizabeth B.; Behn, Mark D. Analytical Chemistry, Vol. 78, Issue 13 https://doi.org/10.1021/ac0600306	journal	July 2006
Formularity: Software for Automated Formula Assignment of Natural and Other Organic Matter from Ultrahigh-Resolution Mass Spectra Tolić, Nikola; Liu, Yina; Liyu, Andrey Analytical Chemistry, Vol. 89, Issue 23 https://doi.org/10.1021/acs.analchem.7b03318	journal	November 2017
Molecular Fractionation of Dissolved Organic Matter with Metal Salts Riedel, Thomas; Biester, Harald; Dittmar, Thorsten Environmental Science & Technology, Vol. 46, Issue 8 https://doi.org/10.1021/es203901u	journal	March 2012
Methane oxidation activity in various soils and freshwater sediments: Occurrence, characteristics, vertical profiles, and distribution on grain size fractions Bender, Martin; Conrad, Ralf Journal of Geophysical Research, Vol. 99, Issue D8 https://doi.org/10.1029/94JD00266	journal	January 1994
Sorptive preservation of labile organic matter in marine sediments Keil, Richard G.; Montluçon, Daniel B.; Prahl, Fredrick G. Nature, Vol. 370, Issue 6490 https://doi.org/10.1038/370549a0	journal	August 1994
Stabilizing feedbacks in glacier-bed erosion Alley, R. B.; Lawson, D. E.; Larson, G. J. Nature, Vol. 424, Issue 6950 https://doi.org/10.1038/nature01839	journal	August 2003
Methane oxidation by an extremely acidophilic bacterium of the phylum Verrucomicrobia Dunfield, Peter F.; Yuryev, Anton; Senin, Pavel Nature, Vol. 450, Issue 7171 https://doi.org/10.1038/nature06411	journal	November 2007
Persistence of soil organic matter as an ecosystem property Schmidt, Michael W. I.; Torn, Margaret S.; Abiven, Samuel Nature, Vol. 478, Issue 7367 https://doi.org/10.1038/nature10386	journal	October 2011
The contentious nature of soil organic matter Lehmann, Johannes; Kleber, Markus Nature, Vol. 528, Issue 7580 https://doi.org/10.1038/nature16069	journal	November 2015
Biophysical controls on organic carbon fluxes in fluvial networks Battin, Tom J.; Kaplan, Louis A.; Findlay, Stuart Nature Geoscience, Vol. 1, Issue 2 https://doi.org/10.1038/ngeo101	journal	January 2008
Biogeochemically diverse organic matter in Alpine glaciers and its downstream fate Singer, Gabriel A.; Fasching, Christina; Wilhelm, Linda Nature Geoscience, Vol. 5, Issue 10 https://doi.org/10.1038/ngeo1581	journal	September 2012
Microbially driven export of labile organic carbon from the Greenland ice sheet Musilova, Michaela; Tranter, Martyn; Wadham, Jemma Nature Geoscience, Vol. 10, Issue 5 https://doi.org/10.1038/ngeo2920	journal	April 2017
River piracy and drainage basin reorganization led by climate-driven glacier retreat Shugar, Daniel H.; Clague, John J.; Best, James L. Nature Geoscience, Vol. 10, Issue 5 https://doi.org/10.1038/ngeo2932	journal	April 2017
The boundless carbon cycle Battin, Tom J.; Luyssaert, Sebastiaan; Kaplan, Louis A. Nature Geoscience, Vol. 2, Issue 9 https://doi.org/10.1038/ngeo618	journal	September 2009
DADA2: High-resolution sample inference from Illumina amplicon data Callahan, Benjamin J.; McMurdie, Paul J.; Rosen, Michael J. Nature Methods, Vol. 13, Issue 7 https://doi.org/10.1038/nmeth.3869	journal	May 2016
Shifts in pore connectivity from precipitation versus groundwater rewetting increases soil carbon loss after drought Smith, A. Peyton; Bond-Lamberty, Ben; Benscoter, Brian W. Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/s41467-017-01320-x	journal	November 2017
Anaerobic microsites have an unaccounted role in soil carbon stabilization Keiluweit, Marco; Wanzek, Tom; Kleber, Markus Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/s41467-017-01406-6	journal	November 2017
Elevated temperature and CO2 strongly affect the growth strategies of soil bacteria Ruan, Yang; Kuzyakov, Yakov; Liu, Xiaoyu Nature Communications, Vol. 14, Issue 1 https://doi.org/10.1038/s41467-023-36086-y	journal	January 2023
Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2 Bolyen, Evan; Rideout, Jai Ram; Dillon, Matthew R. Nature Biotechnology, Vol. 37, Issue 8 https://doi.org/10.1038/s41587-019-0209-9	journal	July 2019
Effects of flooding and redox conditions on solute diffusion in soil Kirk, G. J. D.; Solivas, J. L.; Alberto, M. C. European Journal of Soil Science, Vol. 54, Issue 3 https://doi.org/10.1046/j.1365-2389.2003.00532.x	journal	September 2003
Mineral surfaces and soil organic matter Kaiser, K.; Guggenberger, G. European Journal of Soil Science, Vol. 54, Issue 2 https://doi.org/10.1046/j.1365-2389.2003.00544.x	journal	June 2003
Detection of abundant sulphate‐reducing bacteria in marine oxic sediment layers by a combined cultivation and molecular approach Wieringa, Elze B. A.; Overmann, Jörg; Cypionka, Heribert Environmental Microbiology, Vol. 2, Issue 4 https://doi.org/10.1046/j.1462-2920.2000.00123.x	journal	August 2000
Regulation of soil organic C mineralisation at the pore scale Ruamps, Léo S.; Nunan, Naoise; Pouteau, Valérie FEMS Microbiology Ecology, Vol. 86, Issue 1 https://doi.org/10.1111/1574-6941.12078	journal	February 2013
Spatial location of carbon decomposition in the soil pore system Strong, D. T.; Wever, H. De; Merckx, R. European Journal of Soil Science, Vol. 55, Issue 4 https://doi.org/10.1111/j.1365-2389.2004.00639.x	journal	December 2004
Effect of low temperature on microbial growth: lowered affinity for substrates limits growth at low temperature Nedwell, D. B. FEMS Microbiology Ecology, Vol. 30, Issue 2 https://doi.org/10.1111/j.1574-6941.1999.tb00639.x	journal	October 1999
Fermentation pattern of methanogenic degradation of rice straw in anoxic paddy soil Glissmann, Kristin; Conrad, Ralf FEMS Microbiology Ecology, Vol. 31, Issue 2 https://doi.org/10.1111/j.1574-6941.2000.tb00677.x	journal	February 2000
Verrucomicrobia Are Candidates for Polysaccharide-Degrading Bacterioplankton in an Arctic Fjord of Svalbard Cardman, Z.; Arnosti, C.; Durbin, A. Applied and Environmental Microbiology, Vol. 80, Issue 12 https://doi.org/10.1128/AEM.00899-14	journal	April 2014
Oxygen-dependent growth of the obligate anaerobe Desulfovibrio vulgaris Hildenborough Johnson, M. S.; Zhulin, I. B.; Gapuzan, M. E. Journal of Bacteriology, Vol. 179, Issue 17 https://doi.org/10.1128/jb.179.17.5598-5601.1997	journal	September 1997
SEDIMENT BACTERIA: Who's There, What Are They Doing, and What's New? Nealson, Kenneth H. Annual Review of Earth and Planetary Sciences, Vol. 25, Issue 1 https://doi.org/10.1146/annurev.earth.25.1.403	journal	May 1997
Oxygen Respiration by Desulfovibrio Species Cypionka, Heribert Annual Review of Microbiology, Vol. 54, Issue 1 https://doi.org/10.1146/annurev.micro.54.1.827	journal	October 2000
Metagenomic biomarker discovery and explanation Segata, Nicola; Izard, Jacques; Waldron, Levi Genome Biology, Vol. 12, Issue 6 https://doi.org/10.1186/gb-2011-12-6-r60	journal	January 2011
Optimizing taxonomic classification of marker-gene amplicon sequences with QIIME 2’s q2-feature-classifier plugin Bokulich, Nicholas A.; Kaehler, Benjamin D.; Rideout, Jai Ram Microbiome, Vol. 6, Issue 1 https://doi.org/10.1186/s40168-018-0470-z	journal	May 2018
Millennial-aged organic carbon subsidies to a modern river food web Caraco, Nina; Bauer, James E.; Cole, Jonathan J. Ecology, Vol. 91, Issue 8 https://doi.org/10.1890/09-0330.1	journal	August 2010
A Unified Multiscale Model for Pore-ScaleFlow Simulations in Soils Yang, Xiaofan; Liu, Chongxuan; Shang, Jianying Soil Science Society of America Journal, Vol. 78, Issue 1 https://doi.org/10.2136/sssaj2013.05.0190	journal	January 2014
Soil CO ₂ and O ₂ Concentrations Illuminate the Relative Importance of Weathering and Respiration to Seasonal Soil Gas Fluctuations Hodges, Caitlin; Kim, Hyojin; Brantley, Susan L. Soil Science Society of America Journal, Vol. 83, Issue 4 https://doi.org/10.2136/sssaj2019.02.0049	journal	July 2019
Dispersible Colloid Facilitated Release of Organic Carbon From Two Contrasting Riparian Sediments Rod, Kenton A.; Patel, Kaizad F.; Kumar, Swatantar Frontiers in Water, Vol. 2 https://doi.org/10.3389/frwa.2020.560707	journal	December 2020
Maximum respiration rates in hyporheic zone sediments are primarily constrained by organic carbon concentration and secondarily by organic matter chemistry Stegen, James C.; Garayburu-Caruso, Vanessa A.; Danczak, Robert E. Biogeosciences, Vol. 20, Issue 14 https://doi.org/10.5194/bg-20-2857-2023	journal	July 2023

Similar Records

Water-dispersible nanocolloids and higher temperatures promote the release of carbon from riparian soil

Journal Article · 2020 · Vadose Zone Journal · OSTI ID:1735604

Rod, Kenton A.; Smith, A. Peyton; Leng, Weinan; +8 more

Methane oxidation in a neutral landfill cover soil: Influence of moisture content, temperature, and nitrogen-turnover

Journal Article · 1995 · Journal of Environmental Quality · OSTI ID:245361

Boeckx, P; Van Cleemput, O

Pedogenesis of black shale-influenced soils of the Knobs region of eastern Kentucky

Thesis/Dissertation · 1988 · OSTI ID:5884300

Sobecki, T M

Related Subjects

58 GEOSCIENCES
59 BASIC BIOLOGICAL SCIENCES

Title: Moisture-mineral interactions drive bacterial and organic matter turnover in glacier-sourced riparian sediments undergoing pedogenesis

Citation Formats

References (58)

Similar Records

Related Subjects