Biomolecular budget of persistent, microbial-derived soil organic carbon: The importance of underexplored pools

Rempfert, Kaitlin R.; Bell, Sheryl L.; Kasanke, Christopher P.; Zhao, Qian; Zhao, Xiaodong; Lipton, Andrew S.; Hofmockel, Kirsten S.

doi:10.1016/j.scitotenv.2024.172916

Biomolecular budget of persistent, microbial-derived soil organic carbon: The importance of underexplored pools

Journal Article · Wed May 01 00:00:00 EDT 2024 · Science of the Total Environment

DOI:https://doi.org/10.1016/j.scitotenv.2024.172916· OSTI ID:2350963

Rempfert, Kaitlin R. ^[1]; ^[1]; Kasanke, Christopher P. ^[1]; ^[1]; Zhao, Xiaodong ^[1]; ^[1]; ^[2]

Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)
Pacific Northwest National Laboratory (PNNL), Richland, WA (United States); Iowa State University, Ames, IA (United States)

The details of how soil microorganisms contribute to stable soil organic carbon pools are a pressing knowledge gap with direct implications for soil health and climate mitigation. It is now recognized that microbial necromass contributes substantially to the formation of stable soil carbon. However, the quantification of necromass in soils has largely been limited to model molecules such as aminosugar biomarkers. The abundance and chemical composition of other persistent microbial residues remain unresolved, particularly concerning how these pools may vary with microbial community structure, soil texture, and management practices. We use yearlong soil incubation experiments with an isotopic tracer to quantify the composition of persistent residues derived from microbial communities inhabiting sand or silt dominated soil with annual (corn) or perennial (switchgrass) monocultures. Persistent microbial residues were recovered in diverse soil biomolecular pools including metabolites, proteins, lipids, and mineral-associated organic matter (MAOM). The relative abundances of microbial contributions to necromass pools were consistent across cropping systems and soil textures. The greatest residue accumulation was not recovered in MAOM but in the light density fraction of soil debris that persisted after extraction by chemical fractionation using organic solvents. Necromass abundance was positively correlated with microbial biomass abundance and revealed a possible role of cell wall morphology in enhancing microbial carbon persistence; while gram-negative bacteria accounted for the greatest contribution to microbial-derived carbon by mass at one year, residues from gram-positive Actinobacteria and Firmicutes showed greater durability. Together these results offer a quantitative assessment of the relative importance of diverse molecular classes for generating durable soil carbon.

View Accepted Manuscript (DOE)

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

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC05-76RL01830

OSTI ID:: 2350963

Report Number(s):: PNNL-SA--193775

Journal Information:: Science of the Total Environment, Journal Name: Science of the Total Environment Journal Issue: 2024 Vol. 932; ISSN 0048-9697

Publisher:: ElsevierCopyright Statement

Country of Publication:: United States

Language:: English

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Soil Respiration and Bacterial Structure and Function after 17 Years of a Reciprocal Soil Transplant Experiment Bond-Lamberty, Ben; Bolton, Harvey; Fansler, Sarah PLOS ONE, Vol. 11, Issue 3 https://doi.org/10.1371/journal.pone.0150599	journal	March 2016
Associative nitrogen fixation (ANF) in switchgrass (Panicum virgatum) across a nitrogen input gradient Roley, Sarah S.; Duncan, David S.; Liang, Di PLOS ONE, Vol. 13, Issue 6 https://doi.org/10.1371/journal.pone.0197320	journal	June 2018
Fourier Transform Infrared Spectroscopy of Clay Size Fraction of Cretaceous-Tertiary Kaolins in the Douala Sub-Basin, Cameroon Bukalo, Nenita N.; Ekosse, Georges-Ivo E.; Odiyo, John O. Open Geosciences, Vol. 9, Issue 1 https://doi.org/10.1515/geo-2017-0031	journal	August 2017
How enzymes are adsorbed on soil solid phase and factors limiting its activity: A Review Datta, Rahul; Anand, Swati; Moulick, Amitava International Agrophysics, Vol. 31, Issue 2 https://doi.org/10.1515/intag-2016-0049	journal	April 2017
Kinetic and Mechanistic Investigations on Oxidation of L-tryptophan by Diperiodatocuprate(III) in Aqueous Alkaline Medium Shetti, Nagaraj P.; Nandibewoor, Sharanappa T. Zeitschrift für Physikalische Chemie, Vol. 223, Issue 3 https://doi.org/10.1524/zpch.2009.5432	journal	March 2009
Slower growth of Escherichia coli leads to longer survival in carbon starvation due to a decrease in the maintenance rate Biselli, Elena; Schink, Severin Josef; Gerland, Ulrich Molecular Systems Biology, Vol. 16, Issue 6 https://doi.org/10.15252/msb.20209478	journal	June 2020
Toward an Ecological Classification of soil Bacteria Fierer, Noah; Bradford, Mark A.; Jackson, Robert B. Ecology, Vol. 88, Issue 6 https://doi.org/10.1890/05-1839	journal	June 2007
Chemical and Biological Characteristics of Physically Uncomplexed Organic Matter Gregorich, E. G.; Beare, M. H.; McKim, U. F. Soil Science Society of America Journal, Vol. 70, Issue 3 https://doi.org/10.2136/sssaj2005.0116	journal	January 2006
Organo-mineral interactions in contrasting soils under natural vegetation Jones, Edward; Singh, Balwant Frontiers in Environmental Science, Vol. 2 https://doi.org/10.3389/fenvs.2014.00002	journal	January 2014
Soil Properties Control Microbial Carbon Assimilation and Its Mean Residence Time Ali, Rana Shahbaz; Poll, Christian; Kandeler, Ellen Frontiers in Environmental Science, Vol. 8 https://doi.org/10.3389/fenvs.2020.00033	journal	March 2020
Microbial Necromass in Soils—Linking Microbes to Soil Processes and Carbon Turnover Kästner, M.; Miltner, A.; Thiele-Bruhn, S. Frontiers in Environmental Science, Vol. 9 https://doi.org/10.3389/fenvs.2021.756378	journal	December 2021
Site and Bioenergy Cropping System Similarly Affect Distinct Live and Total Soil Microbial Communities Leichty, Sarah I.; Kasanke, Christopher P.; Bell, Sheryl L. Frontiers in Microbiology, Vol. 12 https://doi.org/10.3389/fmicb.2021.725756	journal	October 2021
Persistent Activities of Extracellular Enzymes Adsorbed to Soil Minerals Olagoke, Folasade K.; Kaiser, Klaus; Mikutta, Robert Microorganisms, Vol. 8, Issue 11 https://doi.org/10.3390/microorganisms8111796	journal	November 2020
Variation in the Molecular Structure and Radiocarbon Abundance of Mineral-Associated Organic Matter across a Lithosequence of Forest Soils Heckman, Katherine; Throckmorton, Heather; Horwath, William Soil Systems, Vol. 2, Issue 2 https://doi.org/10.3390/soilsystems2020036	journal	June 2018
The MPLEx Protocol for Multi-omic Analyses of Soil Samples Nicora, Carrie D.; Burnum-Johnson, Kristin E.; Nakayasu, Ernesto S. Journal of Visualized Experiments, Issue 135 https://doi.org/10.3791/57343	journal	January 2018
Extracellular polymeric substances, a key element in understanding biofilm phenotype Di Martino, Patrick AIMS Microbiology, Vol. 4, Issue 2 https://doi.org/10.3934/microbiol.2018.2.274	journal	January 2018
Turnover of microbial groups and cell components in soil: ¹³C analysis of cellular biomarkers Gunina, Anna; Dippold, Michaela; Glaser, Bruno Biogeosciences, Vol. 14, Issue 2 https://doi.org/10.5194/bg-14-271-2017	journal	January 2017
Iron and aluminum association with microbially processed organic matter via meso-density aggregate formation across soils: organo-metallic glue hypothesis Wagai, Rota; Kajiura, Masako; Asano, Maki SOIL, Vol. 6, Issue 2 https://doi.org/10.5194/soil-6-597-2020	journal	January 2020
Variation of soil microbial carbon use efficiency (CUE) and its Influence mechanism in the context of global environmental change: a review Adingo, Samuel; Yu, Jie-Ru; Xuelu, Liu PeerJ, Vol. 9 https://doi.org/10.7717/peerj.12131	journal	October 2021

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54 ENVIRONMENTAL SCIENCES
lipid
metabolite
mineral-associated soil carbon
necromass
protein
soil

Biomolecular budget of persistent, microbial-derived soil organic carbon: The importance of underexplored pools

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