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Reactive iron, not fungal community, drives organic carbon oxidation potential in floodplain soils

Journal Article · · Soil Biology and Biochemistry
 [1];  [2];  [3];  [4];  [5];  [3]
  1. Stanford Univ., CA (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
  2. Stanford Univ., CA (United States); University of North Carolina, Wilmington, NC (United States)
  3. Stanford Univ., CA (United States)
  4. Univ. of Massachusetts, Amherst, MA (United States); Univ. of Lausanne (UNIL) (Switzerland)
  5. Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); Univ. of California, Berkeley, CA (United States)
Wetlands host ∼20% of terrestrial organic carbon and serve as a major sink for atmospheric carbon. Anoxic soils and sediments accrue soil organic carbon (SOC) partly by hampering the activity of extracellular oxidative enzymes that break down phenolic polymers. Upon aeration, fungal-driven oxidative enzymatic depolymerization and microbial respiration of released monomers ensue. Redox-active metals can simultaneously catalyze abiotic nonspecific oxidation of SOC, notable examples including Mn(III) or Fe(II) through Fenton-like, hydrogen peroxide-catalyzed oxidative radical production. However, the extent of reactive metal contributions to biotic and abiotic SOC degradation is not understood in the context of natural environments with diverse redox chemistry. We tested the relative contributions of fungi, Mn(III) and Fe(II) to phenolic substrate (L-DOPA) oxidation in floodplain soils representing a range of transient redox conditions driven by permanent vs. periodic flooding. Phenol oxidative potential was highest in permanently flooded soils with fewer fungal taxa known for observed (per)oxidase activity and instead correlated with HCl-extractable Fe(II), Fe(total) and Fe(II)/Fe(total), suggesting a specific role of Fe(II). Fe(II) additions enhanced phenol oxidative potential in sterilized and non-sterilized soils in the presence of hydrogen peroxide, indicating abiotic Fe-mediated radical chemistry could significantly enhance wetland SOC oxidative depolymerization throughout redox-active floodplain soils. Fungal community composition did not correlate to phenol oxidative potential overall and only more oxic soils adjacent to the river with diverse fungal communities showed declining oxidative potential after sterilization. Mn(III) addition did not significantly enhance phenol oxidative potential across all soils, although it appeared to drive fungal-mediated oxidative potential in the most aerated floodplain soils. Understanding how metals mediate SOC depolymerization as abiotic oxidants or microbially-harnessed enzyme cofactors and substrates in soils under variable hydrologic controls will improve our ability to represent depolymerization in terrestrial carbon models in wetland and other frequently saturated soils.
Research Organization:
Environmental Molecular Sciences Laboratory (EMSL), Richland, WA (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); USDOE Joint Genome Institute (JGI), Berkeley, CA (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER). Earth & Environmental Systems Science (EESS)
Grant/Contract Number:
AC02-05CH11231; SC0016544
OSTI ID:
2234169
Journal Information:
Soil Biology and Biochemistry, Journal Name: Soil Biology and Biochemistry Vol. 178; ISSN 0038-0717
Publisher:
ElsevierCopyright Statement
Country of Publication:
United States
Language:
English

References (89)

Determination of organic and inorganic carbon, δ 13 C, and nitrogen in soils containing carbonates after acid fumigation with HCl journal February 2010
The Role of One- and Two-Electron Transfer Reactions in Forming Thermodynamically Unstable Intermediates as Barriers in Multi-Electron Redox Reactions journal December 2009
Ferrous Iron Stimulates Phenol Oxidase Activity and Organic Matter Decomposition in Waterlogged Wetlands journal October 2005
Inhibitory effects of drought induced acidification on phenol oxidase activities in Sphagnum-dominated peatland journal May 2013
Development of energetic and enzymatic limitations on microbial carbon cycling in soils journal March 2021
Wetlands, carbon, and climate change journal June 2012
Structure and Action Mechanism of Ligninolytic Enzymes journal June 2008
The oxidation of Fe(II) with H2O2 in seawater journal August 1989
Wood decomposition over a first-order watershed: Mass loss as a function of lignocellulase activity journal August 1992
Resource allocation to extracellular enzyme production: A model for nitrogen and phosphorus control of litter decomposition journal October 1994
The effects of long term nitrogen deposition on extracellular enzyme activity in an Acer saccharum forest soil journal September 2002
The implications of exoenzyme activity on microbial carbon and nitrogen limitation in soil: a theoretical model journal April 2003
Review: lignin conversion by manganese peroxidase (MnP) journal April 2002
Cell wall alterations in loblolly pine wood decayed by the white-rot fungus, Ceriporiopsis subvermispora journal March 1997
Simulated patterns of litter decay predict patterns of extracellular enzyme activities journal February 2000
Development of a sequential extraction procedure for iron: implications for iron partitioning in continentally derived particulates journal January 2005
FUNGuild: An open annotation tool for parsing fungal community datasets by ecological guild journal April 2016
Soluble Mn(III)–L complexes are abundant in oxygenated waters and stabilized by humic ligands journal February 2017
Influence of iron redox cycling on organo-mineral associations in Arctic tundra soil journal June 2017
The influence of native soil organic matter and minerals on ferrous iron oxidation journal January 2021
Evidence for the presence of strong Mn(III)-binding ligands in the water column of the Chesapeake Bay journal April 2015
Dark production of hydroxyl radicals by aeration of anoxic lake water journal September 2015
A regulatory role for phenol oxidase during decomposition in peatlands journal October 2004
Low levels of nitrogen addition stimulate decomposition by boreal forest fungi journal February 2009
The influence of time, storage temperature, and substrate age on potential soil enzyme activity in acidic forest soils using MUB-linked substrates and l-DOPA journal June 2009
Effects of carbon additions on iron reduction and phosphorus availability in a humid tropical forest soil journal August 2009
Phenol oxidase, peroxidase and organic matter dynamics of soil journal March 2010
Optimization of hydrolytic and oxidative enzyme methods for ecosystem studies journal July 2011
Independent roles of ectomycorrhizal and saprotrophic communities in soil organic matter decomposition journal February 2013
Long-term water regime differentiates changes in decomposition and microbial properties in tropical peat soils exposed to the short-term drought journal May 2013
Measuring phenol oxidase and peroxidase activities with pyrogallol, l-DOPA, and ABTS: Effect of assay conditions and soil type journal December 2013
Functional guild classification predicts the enzymatic role of fungi in litter and soil biogeochemistry journal September 2015
Abiotic and biotic regulation on carbon mineralization and stabilization in paddy soils along iron oxide gradients journal September 2021
Visualizing the transfer of organic matter from decaying plant residues to soil mineral surfaces controlled by microorganisms journal September 2021
Reactive oxygen species and development in microbial eukaryotes journal March 2005
Enzymes, Manganese, or Iron? Drivers of Oxidative Organic Matter Decomposition in Soils journal October 2020
Production of Abundant Hydroxyl Radicals from Oxygenation of Subsurface Sediments journal December 2015
Rapid Iron Reduction Rates Are Stimulated by High-Amplitude Redox Fluctuations in a Tropical Forest Soil journal February 2017
Redox Fluctuations Control the Coupled Cycling of Iron and Carbon in Tropical Forest Soils journal November 2018
Manganese-Driven Carbon Oxidation at Oxic–Anoxic Interfaces journal September 2018
Contaminant Degradation by •OH during Sediment Oxygenation: Dependence on Fe(II) Species journal February 2020
Lignin peroxidase oxidation of manganese(2+) in the presence of veratryl alcohol, malonic or oxalic acid, and oxygen journal November 1990
Superoxide Dismutases and Superoxide Reductases journal January 2014
Rates and Mechanism of Fe(II) Oxidation at Nanomolar Total Iron Concentrations journal March 1995
Reaction kinetics of hydrogen peroxide with copper and iron in seawater journal August 1987
Dark Formation of Hydroxyl Radical in Arctic Soil and Surface Waters journal October 2013
Factors Affecting the Yield of Oxidants from the Reaction of Nanoparticulate Zero-Valent Iron and Oxygen journal February 2008
Reduction of iron (III) and humic substances plays a major role in anaerobic respiration in an Arctic peat soil journal January 2010
Shifts in Precipitation Accumulation Extremes During the Warm Season Over the United States journal August 2018
An enzymic 'latch' on a global carbon store journal January 2001
Drought-induced carbon loss in peatlands journal November 2011
Thermodynamically controlled preservation of organic carbon in floodplains journal May 2017
Anaerobic microsites have an unaccounted role in soil carbon stabilization journal November 2017
Millennial scale persistence of organic carbon bound to iron in Arctic marine sediments journal January 2021
Production of hydrogen peroxide in an intra-meander hyporheic zone at East River, Colorado journal January 2022
Dramatic declines in snowpack in the western US journal March 2018
Pathways for degradation of lignin in bacteria and fungi journal January 2011
Oxidation of hydroquinones by the versatile ligninolytic peroxidase from Pleurotus eryngii journal September 2001
Long-term litter decomposition controlled by manganese redox cycling journal September 2015
Easily decomposable organic matter in paddy soil journal June 1984
Advanced Oxidation Processes for Organic Contaminant Destruction Based on the Fenton Reaction and Related Chemistry journal January 2006
The UNITE database for molecular identification of fungi: handling dark taxa and parallel taxonomic classifications journal October 2018
Presence of the distinct systems responsible for superoxide anion and hydrogen peroxide generation in red tide phytoplankton Chattonella marina and Chattonella ovata journal January 2007
Carbon sequestration journal August 2007
Iron oxidation stimulates organic matter decomposition in humid tropical forest soils journal July 2013
Pathways of mineral‐associated soil organic matter formation: Integrating the role of plant carbon source, chemistry, and point of entry journal November 2018
Global and regional importance of the tropical peatland carbon pool: TROPICAL PEATLAND CARBON POOL journal January 2011
ITS primers with enhanced specificity for basidiomycetes - application to the identification of mycorrhizae and rusts journal April 1993
Size and functional diversity of microbe populations control plant persistence and long-term soil carbon accumulation: Modelling long-term SOM dynamics journal August 2005
New primers to amplify the fungal ITS2 region - evaluation by 454-sequencing of artificial and natural communities journal July 2012
The Plant Cell Wall-Decomposing Machinery Underlies the Functional Diversity of Forest Fungi journal July 2011
Widespread Production of Extracellular Superoxide by Heterotrophic Bacteria journal May 2013
Introducing mothur: Open-Source, Platform-Independent, Community-Supported Software for Describing and Comparing Microbial Communities journal October 2009
Involutin Is an Fe 3+ Reductant Secreted by the Ectomycorrhizal Fungus Paxillus involutus during Fenton-Based Decomposition of Organic Matter journal October 2015
Anthropogenic N Deposition Alters the Composition of Expressed Class II Fungal Peroxidases journal February 2018
Reverse Transcription-PCR Analysis of the Regulation of the Manganese Peroxidase Gene Family journal February 1998
Penetrability of White Rot-Degraded Pine Wood by the Lignin Peroxidase of Phanerochaete chrysosporium journal November 1988
Mn(II) Regulation of Lignin Peroxidases and Manganese-Dependent Peroxidases from Lignin-Degrading White Rot Fungi journal January 1990
Roles of manganese and organic acid chelators in regulating lignin degradation and biosynthesis of peroxidases by Phanerochaete chrysosporium. journal January 1992
Laccase isoenzymes of Pleurotus eryngii: characterization, catalytic properties, and participation in activation of molecular oxygen and Mn2+ oxidation. journal January 1997
Predicting long-term patterns of mass loss, nitrogen dynamics, and soil organic matter formation from initial fine litter chemistry in temperate forest ecosystems journal October 1990
The Ecology of Soil Carbon: Pools, Vulnerabilities, and Biotic and Abiotic Controls journal November 2017
phyloseq: An R Package for Reproducible Interactive Analysis and Graphics of Microbiome Census Data journal April 2013
Wood Decay by Brown-Rot Fungi: Changes in Pore Structure and Cell Wall Volume journal January 1991
The carbon balance of North American wetlands journal December 2006
Tropical forest soil microbial communities couple iron and carbon biogeochemistry journal September 2010
Oxygen Effects on Carbon, Polyphenols, and Nitrogen Mineralization Potential in Soil journal January 2007
The Controls of Iron and Oxygen on Hydroxyl Radical (•OH) Production in Soils journal December 2018
Enzymatic Degradation of Lignin in Soil: A Review journal July 2017

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