Abstract
Purpose
The iron redox cycle is closely tied to the fate of carbon in terrestrial ecosystems, especially paddy soils. Varies diurnally and seasonally, light—the crucial environmental factor—may be a fundamental factor elucidating temporal and spatial variabilities of carbon-containing gases emission. The role of sunlight in the iron-mediated carbon cycle, however, has not been fully elucidated. We conduct this study to test the role of light in the iron-mediated carbon cycling.
Materials and methods
In this study, we conducted anaerobic incubation experiments of a calcareous paddy soil in serum vials under alternating dark and light conditions. The dynamic evolution of the carbon and iron contents was evaluated by measuring the CO2, CH4, and O2 concentrations in the headspace of the vials, as well as the water-soluble inorganic carbon, microbial biomass carbon, and HCl-extractable ferrous iron contents in soil slurries. We also analyzed the soil microbial community structure by high-throughput 16S rRNA gene sequencing.
Results and discussion
The results highlighted the positive correlation between carbon mineralization and ferric iron reduction under dark conditions. Under light conditions, however, ferrous iron was oxidized by the O2 generated via oxygenic photosynthesis of phototrophic bacteria such as Cyanobacteria, along with a decreased production of CO2, CH4, and water-soluble inorganic carbon. The abundance of Cyanobacteria positively correlated to O2 levels and MBC content significantly. Light-induced periodic variations in the redox conditions facilitated carbon fixation in microbial biomass and up to 31.79 μmol g−1 carbon was sequestrated during 30 days light incubation.
Conclusions
These results indicate that light inhibits the emission of carbon-containing greenhouse gases associated with the iron redox cycle in calcareous paddy soil. Assimilation of inorganic carbon by phototrophs may responsible for the inhibition of carbon mineralization. Our study suggests that procedures allowing more light to reach the soil surface, for instance, reducing the planting density, may mitigate greenhouse gas emissions and promote carbon sequestration in paddy soils.
Similar content being viewed by others
References
Ali MA, Kim PJ, Inubushi K (2015) Mitigating yield-scaled greenhouse gas emissions through combined application of soil amendments: a comparative study between temperate and subtropical rice paddy soils. Sci Total Environ 529:140–148
Azam HM, Finneran KT (2013) Ferric iron amendment increases Fe(III)-reducing microbial diversity and carbon oxidation in on-site wastewater systems. Chemosphere 90(4):1435–1443
Bahia ASRD, Marques J, Panosso AR, Camargo LA, Siqueira DS, Scala NL (2014) Iron oxides as proxies for characterizing anisotropy in soil CO2 emission in sugarcane areas under green harvest. Agr Ecosyst Environ 192:152–162
Birge HE, Conant RT, Follett RF, Haddix ML, Morris SJ, Snapp SS, Wallenstein MD, Paul EA (2015) Soil respiration is not limited by reductions in microbial biomass during long-term soil incubations. Soil Biol Biochem 81:304–310
Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinform 30:2114–2120
Chen G, Liu Y, Yao H, Huang C (2006) A method for measuring microbial biomass C in waterlogged soil: chloroform fumigation extraction—water bath method. Acta Pedol Sinica 43(06):981–988 (In Chinese)
Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinform 27(16):2194–2200
Elghamry W, Elashkar M (1962) Simplified textural classification triangles. Soil Sci Soc Am J 6(26):612–613
Fang K, Qin S, Chen L, Zhang Q, Yang Y (2019) Al/Fe mineral controls on soil organic carbon stock across Tibetan alpine grasslands. J Geophys Res Biogeosci 124(2):247–259
Freeman KR, Pescador MY, Reed SC, Costello EK, Robeson MS, Schmidt SK (2009) Soil CO2 flux and photoautotrophic community composition in highelevation ‘barren’ soil. Environ Microbiol 11(3):674–686
Grahammer K, Jawson MD, Skopp J (1991) Day and night soil respiration from a grassland. Soil Biol Biochem 23(1):77–81
Huang B, Yu K, Gambrell RP (2009) Effects of ferric iron reduction and regeneration on nitrous oxide and methane emissions in a rice soil. Chemosphere 74(4):481–486
Huang G, Li Y, Su YG (2015) Effects of increasing precipitation on soil microbial community composition and soil respiration in a temperate desert Northwestern China. Soil Biol Biochem 83:52–56
Jiang J, Guo S, Zhang Y, Liu Q, Wang R, Wang Z, Li N, Li R (2015) Changes in temperature sensitivity of soil respiration in the phases of a three-year crop rotation system. Soil Tillage Res 150:139–146
Kappler A, Newman DK (2004) Formation of Fe(III)-minerals by Fe(II)-oxidizing photoautotrophic bacteria. Geochim Cosmochim Acta 68(6):1217–1226
Khalil MI, Abdalla M, Lanigan G, Osborne B, Müller C (2016) Evaluation of parametric limitations in simulating greenhouse gas fluxes from Irish arable soils using three process-based models. Agric Sci 07(08):503–520
Kühl M, Lassen C, Jorgensen BB (1994) Light penetration and light intensity in sandy marine sediments measured with irradiance and scalar irradiance fiber-optic microprobes. Mar Ecol Prog Ser 105:139–148
Lalonde K, Mucci A, Ouellet A, Gélinas Y (2012) Preservation of organic matter in sediments promoted by iron. Nature 483(7388):198–200
Li X, Li F, Zhang W, Liu T, Chen L, Chen P (2016) Changes in the composition and diversity of microbial communities during anaerobic nitrate reduction and Fe(II) oxidation at circumneutral pH in paddy soil. Soil Biol Biochem 94:70–79
Liu S, Zhang L, Liu Q, Zhou J (2012) Fe(III) fertilization mitigating net global warming potential and greenhouse gas intensity in paddy rice-wheat rotation systems in China. Environ Pollut 164:73–80
Liu T, Chen D, Li X, Li F (2019) Microbially mediated coupling of nitrate reduction and Fe(II) oxidation under anoxic conditions. FEMS Microb Ecol 95(4):1–12
Lovley DR (1991) Dissimilatory Fe(III) and Mn(IV) reduction. Microbiol Rev 55(2):259–287
Lovley DR, Holmes DE, Nevin KP (2004) Dissimilatory Fe(III) and Mn(IV) reduction. Advances Microb Physiol 49:219–286
Lu R (2000) Analytical method of soil agricultural chemistry (in Chinese). China Agric Sci and Technol Press Beijing
Magoč T, Salzberg SL (2011) FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinform 27(21):2957–2963
Maitte B, Jorand FPA, Grgic D, Abdelmoula M, Carteret C (2015) Remineralization of ferrous carbonate from bioreduction of natural goethite in the Lorraine iron ore (Minette) by Shewanella putrefaciens. Chem Geol 412:48–58
Pham HTL, Nguyen LTT, Duong TA, Bui DTT, Doan QT, Nguyen HTT, Mundt S (2017) Diversity and bioactivities of nostocacean cyanobacteria isolated from paddy soil in Vietnam. Syst Appl Microbiol 40(8):470–481
Qu D, Schnell S (2002) Suppression of methanogenesis by iron oxides in paddy soil (in Chinese). Acta Sci Circumst 22(1):65–69
Qu D, Ratering S, Schnell S (2004) Microbial reduction of weakly crystalline iron (III) oxides and suppression of methanogenesis in paddy soil. Bull Environ Contam Toxicol 72(6):1172–1181
Rey A (2015) Mind the gap: non-biological processes contributing to soil CO2 efflux. Glob Chang Biol 21(5):1752–1761
Roden EE, Mcbeth JM, Marco B, Percak-dennett EM, Fleming EJ, Holyoke RR, Luther GW, Emerson D, Schieber J (2012) The microbial ferrous wheel in a neutral pH groundwater seep. Front Microbiol 3:172
Roslev P, Iversen N, Henriksen K (1997) Oxidation and assimilation of atmospheric methane by soil methane oxidizers. Appl Environ Microbiol 63(3):874–880
Rutledge S, Campbell DI, Baldocchi D, Schipper LA (2010) Photodegradation leads to increased carbon dioxide losses from terrestrial organic matter. Glob Chang Biol 16(11):3065–3074
Soo RM, Hemp J, Parks DH, Fischer WW, Hugenholtz P (2017) On the origins of oxygenic photosynthesis and aerobic respiration in Cyanobacteria. Science 355(6332):1436
Stal LJ, Moezelaar R (1997) Fermentation in cyanobacteria. FEMS Microbiol Rev 21:179–211
Steffen W, Rochstrom J, Richardson K, Lenton T, Folke C, Liverman D, Summerhayes C, Barnosky A, Cornell S, Crucifix M, Donges J, Fetzer I, Lade S, Scheffer M, Winkelmann R, Schellnhuber H (2018) Trajectories of the Earth System in the Anthropocene. PNAS 115(33):8252–8259
Sun L, Qu D, Wei Y (2008) Effect of illumination on iron oxide reduction in anaerobic paddy soils (in Chinese). Acta Pedol Sinica 45(4):628–634
Vermeire M, Bonneville S, Stenuit B, Delvaux B, Cornélis J (2019) Is microbial reduction of Fe (III) in podzolic soils influencing C release? Geoderma 340:1–10
Wang Y, Yang H, Ye C, Chen X, Xie B, Huang C, Zhang J, Xu M (2013) Effects of plant species on soil microbial processes and CH4 emission from constructed wetlands. Environ Pollut 174:273–278
Wang Y, Wang H, He J, Feng X (2017) Iron-mediated soil carbon response to water-table decline in an alpine wetland. Nat Commun 8:15972–15981
Weber KA, Achenbach LA, Coates JD (2006a) Microorganisms pumping iron: anaerobic microbial iron oxidation and reduction. Nat Rev Microbiol 4(10):752–764
Weber KA, Pollock J, Cole KA, O’Connor SM, Achenbach LA, Coates JD (2006b) Anaerobic nitrate-dependent iron(II) bio-oxidation by a novel lithoautotrophic betaproteobacterium strain 2002. Appl Environ Microbiol 72(1):686–694
Wei S, Zhang X, McLaughlin NB, Yang X, Liang A, Jia S, Chen X (2016) Effect of breakdown and dispersion of soil aggregates by erosion on soil CO2 emission. Geoderma 264:238–243
Yang R, Chen B, Liu H, Liu Z, Yan H (2015) Carbon sequestration and decreased CO2 emission caused by terrestrial aquatic photosynthesis: insights from diel hydrochemical variations in an epikarst spring and two spring-fed ponds in different seasons. Appl Geochem 63:248–260
Yin X, Wu W, Maeke M, Richter-Heitmannn T, Kulkarni AC, Oni OE, Wendt J, Elvert M, Friedrich M (2019) CO2 conversion to methane and biomass in obligate methylotrophic methanogens in marine sediments. ISME J. https://doi.org/10.1038/s41396-019-0425-9
Zhang W, Yu Y, Huang Y, Li T, Wang P (2011) Modeling methane emissions from irrigated rice cultivation in China from 1960 to 2050. Glob Chang Biol 17(12):3511–3523
Zhao Q, Adhikari D, Huang R, Patel A, Wang X, Tang Y, Obrist D, Roden EE, Yang Y (2017) Coupled dynamics of iron and iron-bound organic carbon in forest soils during anaerobic reduction. Chem Geol 464:118–126
Acknowledgments
We sincerely appreciate the anonymous reviewers for their constructive comments and helpful suggestions.
Funding
This study was funded by the National Natural Science Foundation of China (U1904121, U1504402, and 41601369) and the China Scholarship Council (201908410062).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Patients’ rights and animal protection statements
This article does not contain any studies with human participants or animals performed by any of the authors.
Additional information
Responsible editor: Yan He
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Wang, X., Sun, L., Chen, Z. et al. Light inhibition of carbon mineralization associated with iron redox processes in calcareous paddy soil. J Soils Sediments 20, 3171–3180 (2020). https://doi.org/10.1007/s11368-020-02660-w
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11368-020-02660-w