TRXB土壤学报Acta Pedologica Sinica0564-3929土壤学报编辑部中国南京trxb-60-1-12710.11766/trxb202104010174A研究论文Research Articles石灰性水稻土中硝酸盐依赖型与光合型亚铁氧化过程Nitrate-Dependent and Photosynthetic Fe(II) Oxidation Processes in a Calcareous Paddy Soil陈志怀CHENZhihuai
Iron redox processes under anaerobic conditions are closely correlated to nitrogen cycling in soils. Both nitrate-dependent ferrous oxidation (NDFO) and photosynthetic ferrous oxidation (PFO) are crucial pathways of biological ferrous iron oxidation. However, whether NDFO occurs in calcareous paddy soils and its relation to PFO is still ambiguous.
Method
We collected soil samples from Mengjin County, Henan Province, within the middle and lower reaches of the Yellow River. The soil samples were made into slurries using 10 mmol·L–1\begin{document}$ {\text{NO}}_3^ - $\end{document}/\begin{document}$ {\text{NH}}_4^ + $\end{document} solution or water at the very beginning. Then the slurries were anaerobically incubated under darkness or illuminated. On the 7th day of the incubation, we injected 0.5 mL 70 mmol·L–1\begin{document}$ {\text{NO}}_3^ - $\end{document} or \begin{document}$ {\text{NH}}_4^ + $\end{document} into a part of those slurries made with water to adjust their external \begin{document}$ {\text{NO}}_3^ - $\end{document} or \begin{document}$ {\text{NH}}_4^ + $\end{document} content to 10 mmol L–1. To assess the iron reduction, and ferrous oxidation, Fe(II) in the slurries was measured dynamically using the phenanthroline colorimetric method. To evaluate the nitrogen transformation, \begin{document}$ {\text{NO}}_3^ - $\end{document} and \begin{document}$ {\text{NO}}_2^ - $\end{document} were analyzed dynamically using an ion chromatograph equipped with an electrical conductivity detector, and \begin{document}$ {\text{NH}}_4^ + $\end{document} was measured after the incubation by 1 mol·L–1 KCl extraction-Kjeldahl method. To fractionate the PFO, O2 in the headspaces was determined dynamically using a portable fiber-optic trace oxygen meter.
Result
The results showed that, though no apparent ferrous oxidation was observed, iron reduction rate decreased by 0.28 mg·g–1·d–1 and 0.33 mg·g–1·d–1. Also, the iron reduction rate constant was decreased by 0.15 d–1, and 0.17 d–1 in slurries under darkness with \begin{document}$ {\text{NO}}_3^ - $\end{document} or \begin{document}$ {\text{NH}}_4^ + $\end{document} amended at the very beginning. Ferrous iron was oxidized by 2.21 mg·g–1 and 0.68 mg·g–1 in slurries with \begin{document}$ {\text{NO}}_3^ - $\end{document} or \begin{document}$ {\text{NH}}_4^ + $\end{document} injected on the 7th day of the dark incubation and by 1.99 mg·g–1 in slurries incubated under light. In addition, Fe(II) in the slurries was negatively correlated to O2 in the headspace. Importantly, the reduction of \begin{document}$ {\text{NO}}_3^ - $\end{document}to \begin{document}$ {\text{NH}}_4^ + $\end{document} occurred in the slurries with \begin{document}$ {\text{NO}}_3^ - $\end{document} injected on the 7th day of dark incubation.
Conclusion
Ferrous oxidation caused by NDFO was observed in the calcareous paddy soil amended with 10 mmol·L–1\begin{document}$ {\text{NO}}_3^ - $\end{document} and incubated anaerobically under darkness. However, the oxidation could be inhibited since the ferric iron resulting from NDFO would be reduced rapidly when the \begin{document}$ {\text{NO}}_3^ - $\end{document} becomes depleted. Both NDFO and PFO occurred in the calcareous paddy soil incubated under illumination and the PFO resulted in 1.99 mg·g–1 ferrous iron oxidized. Ferrous oxidation in soils under illumination was increased by 0.57 mg·g–1 when \begin{document}$ {\text{NO}}_3^ - $\end{document} was injected. These results help to further understand the redox processes and the coupled nitrogen transformation in wetland soils.
水稻土亚铁氧化光合产氧硝酸盐还原氮素转化Paddy soilFerrous oxidationOxygenic photosynthesisNitrate reductionNitrogen transformation国家自然科学基金项目U1904121国家自然科学基金项目41601309国家自然科学基金项目(U1904121,41601309)资助the National Natural Science Foundation of ChinaU1904121the National Natural Science Foundation of China41601309Supported by the National Natural Science Foundation of China(Nos. U1904121 and 41601309)
Dynamics of 0.5 mol·L–1 HCl extractable Fe(II)in the paddy soil incubated under dark(a. with \begin{document}$ {\text{NO}}_3^ - $\end{document}/\begin{document}$ {\text{NH}}_4^ + $\end{document} added before the incubation, b. with \begin{document}$ {\text{NO}}_3^ - $\end{document}/\begin{document}$ {\text{NH}}_4^ + $\end{document} injected after 7 days' incubation)
–1 NaNO3溶液、培养开始前加入10 mmol·L–1 NH4Cl、7 d后加入10 mmol·L–1 NaNO3和7 d后加入10 mmol·L–1 NH4Cl。下同。]]>
–1 NaNO3 added to the soil before incubation, 10 mmol·L–1 NH4Cl added to the soil before incubation, 10 mmol·L–1 NaNO3 added to soil at 7 d and 10 mmol·L–1 NH4Cl added to soil at 7 d, respectively. The same below.
]]>
Effect of \begin{document}$ {\text{NO}}_3^ - $\end{document}/\begin{document}$ {\text{NH}}_4^ + $\end{document} amendment on key parameters of iron reduction in the paddy soil incubated under dark
处理Treatment
铁还原容量Iron reduction capacity/(mg·g–1)
最大还原速率Max iron reduction rate/(mg·g–1·d–1)
还原速率常数Reduction rate constant/ d–1
决定系数R2
统计学概率P
注:表中数据为平均值±标准差;同列不同字母表示差异达到显著水平(P < 0.05);标记*的处理表示从9 d开始采用logistic方程对Fe(II)含量变化拟合。下同。Note:Mean ± Std;Different letters in the same column mean significant difference at 0.05 level;The treatments of labeled with * respond fitting the changes of Fe(II)with logistic after 9 d. The same below.
Content of 0.5 mol·L–1 HCl extractable Fe(II)in paddy soil under illuminated incubation(a. with \begin{document}$ {\text{NO}}_3^ - $\end{document}/\begin{document}$ {\text{NH}}_4^ + $\end{document} added before the incubation, b. with \begin{document}$ {\text{NO}}_3^ - $\end{document}/\begin{document}$ {\text{NH}}_4^ + $\end{document} injected after 7 days' incubation)
–1 NaNO3溶液、培养开始前加入10 mmol·L–1 NH4Cl、7 d后加入10 mmol·L–1 NaNO3和7 d后加入10 mmol·L–1 NH4Cl。下同。]]>
–1 NaNO3 added to the soil before incubation, 10 mmol·L–1 NH4Cl added to the soil before incubation, 10 mmol·L–1 NaNO3 added to soil at 7 d and 10 mmol·L–1 NH4Cl added to soil at 7 d, respectively. The same below.
]]>
Effect of \begin{document}$ {\text{NO}}_3^ - $\end{document}/\begin{document}$ {\text{NH}}_4^ + $\end{document} amendment on iron redox characteristics in the paddy soil under illumination
Dynamic changes of O2 content in the headspace of paddy soil with \begin{document}$ {\text{NO}}_3^ - $\end{document}/\begin{document}$ {\text{NH}}_4^ + $\end{document} amendment(a. amended before the incubation, b. amended after 7 days' incubation)
ReferencesChenC MHallS JCowardEIron-mediated organic matter decomposition in humid soils can counteract protection2020111225510.1038/s41467-020-16071-5
Chen C M, Hall S J, Coward E, et al. Iron-mediated organic matter decomposition in humid soils can counteract protection[J]. Nature Communications, 2020, 11(1): 2255.
ZhangX FLiuT XLiF BMultiple effects of nitrate amendment on the transport, transformation and bioavailability of antimony in a paddy soil-rice plant system2021100909810.1016/j.jes.2020.07.009
Zhang X F, Liu T X, Li F B, et al. Multiple effects of nitrate amendment on the transport, transformation and bioavailability of antimony in a paddy soil-rice plant system[J]. Journal of Environmental Sciences, 2021, 100: 90-98
YuH YLiF BLiuC SIron redox cycling coupled to transformation and immobilization of heavy metals: implications for paddy rice safety in the red soil of South China2016137279317
Yu H Y, Li F B, Liu C S, et al. Iron redox cycling coupled to transformation and immobilization of heavy metals: implications for paddy rice safety in the red soil of South China[J]. Advances in Agronomy, 2016, 137: 279-317.
WangJ BZhuZ KLinSMineralization of goethite-adsorbed and -encapsulated organic carbon and its priming effect in paddy soil202158615301539
Wang J B, Zhu Z K, Lin S, et al. Mineralization of goethite-adsorbed and -encapsulated organic carbon and its priming effect in paddy soil[J]. Acta Pedologica Sinica, 2021, 58(6): 1530-1539.
ShelobolinaEKonishiHXuH FIsolation of phyllosilicate-iron redox cycling microorganisms from an illite-smectite rich hydromorphic soil20123134
Shelobolina E, Konishi H, Xu H F, et al. Isolation of phyllosilicate-iron redox cycling microorganisms from an illite-smectite rich hydromorphic soil[J]. Frontiers in Microbiology, 2012, 3: 134.
MeltonE DSchmidtCKapplerAMicrobial iron(II)oxidation in littoral freshwater lake sediment: the potential for competition between phototrophic vs. nitrate-reducing iron(II)-oxidizers20123197
Melton E D, Schmidt C, Kappler A. Microbial iron(II)oxidation in littoral freshwater lake sediment: the potential for competition between phototrophic vs. nitrate-reducing iron(II)-oxidizers[J]. Frontiers in Microbiology, 2012, 3: 197.
WeberK AAchenbachL ACoatesJ DMicroorganisms pumping iron: Anaerobic microbial iron oxidation and reduction200641075276410.1038/nrmicro1490
Weber K A, Achenbach L A, Coates J D. Microorganisms pumping iron: Anaerobic microbial iron oxidation and reduction[J]. Nature Reviews Microbiology, 2006, 4(10): 752-764.
BryceCBlackwellNSchmidtCMicrobial anaerobic Fe(II)oxidation–Ecology, mechanisms and environmental implications201820103462348310.1111/1462-2920.14328
Bryce C, Blackwell N, Schmidt C, et al. Microbial anaerobic Fe(II)oxidation–Ecology, mechanisms and environmental implications[J]. Environmental Microbiology, 2018, 20(10): 3462-3483.
LauferKNordhoffMRøyHCoexistence of microaerophilic, nitrate-reducing, and phototrophic Fe(II)oxidizers and Fe(III)reducers in coastal marine sediment201582514331447
Laufer K, Nordhoff M, Røy H, et al. Coexistence of microaerophilic, nitrate-reducing, and phototrophic Fe(II)oxidizers and Fe(III)reducers in coastal marine sediment [J]. Applied and Environmental Microbiology, 2015, 82(5): 1433-1447.
LiuT XChenD DLiX MMicrobially mediated coupling of nitrate reduction and Fe(II)oxidation under anoxic conditions2019954fiz030
Liu T X, Chen D D, Li X M, et al. Microbially mediated coupling of nitrate reduction and Fe(II)oxidation under anoxic conditions[J]. FEMS Microbiology Ecology, 2019, 95(4): fiz030.
LiuT XChengKChenD DFormation of Fe(Ⅲ)-minerals by microbially mediated coupling of nitrate reduction and Fe(Ⅱ)oxidation: A review2019283620628
Liu T X, Cheng K, Chen D D, et al. Formation of Fe(Ⅲ)-minerals by microbially mediated coupling of nitrate reduction and Fe(Ⅱ)oxidation: A review [J]. Ecology and Environmental Sciences, 2019, 28(3): 620-628.
LiuT XChenD DLuoX BMicrobially mediated nitrate-reducing Fe(II)oxidation: Quantification of chemodenitrification and biological reactions20192569711510.1016/j.gca.2018.06.040
Liu T X, Chen D D, Luo X B, et al. Microbially mediated nitrate-reducing Fe(II)oxidation: Quantification of chemodenitrification and biological reactions[J]. Geochimica et Cosmochimica Acta, 2019, 256: 97-115.
Benaiges-FernandezROffedduF GMargalef-MartiRGeochemical and isotopic study of abiotic nitrite reduction coupled to biologically produced Fe(II)oxidation in marine environments202026012755410.1016/j.chemosphere.2020.127554
Benaiges-Fernandez R, Offeddu F G, Margalef-Marti R, et al. Geochemical and isotopic study of abiotic nitrite reduction coupled to biologically produced Fe(II)oxidation in marine environments[J]. Chemosphere, 2020, 260: 127554.
ChengB YWangYHuaY MThe performance of nitrate-reducing Fe(II)oxidation processes under variable initial Fe/N ratios: The fate of nitrogen and iron species202015473
Cheng B Y, Wang Y, Hua Y M, et al. The performance of nitrate-reducing Fe(II)oxidation processes under variable initial Fe/N ratios: The fate of nitrogen and iron species[J]. Frontiers of Environmental Science & Engineering, 2020, 15(4): 73.
HuS WLiuT XLiF BThe Abiotic and biotic transformation processes of soil iron-bearing minerals and its interfacial reaction mechanisms of heavy metals: A review202259112
Hu S W, Liu T X, Li F B, et al. The Abiotic and biotic transformation processes of soil iron-bearing minerals and its interfacial reaction mechanisms of heavy metals: A review[J]. Acta Pedologica Sinica, 2022, 59(1): 12.
SwannerE DWuW FHaoL KPhysiology, Fe(II)oxidation, and Fe mineral formation by a marine planktonic cyanobacterium grown under ferruginous conditions2015360
Swanner E D, Wu W F, Hao L K, et al. Physiology, Fe(II)oxidation, and Fe mineral formation by a marine planktonic cyanobacterium grown under ferruginous conditions[J]. Frontiers in Earth Science, 2015, 3: 60.
PosthN RKonhauserK OKapplerAMicrobiological processes in banded iron formation deposition20136071733175410.1111/sed.12051
Posth N R, Konhauser K O, Kappler A. Microbiological processes in banded iron formation deposition[J]. Sedimentology, 2013, 60(7): 1733-1754.
ThompsonK JKenwardP ABauerK WPhotoferrotrophy, deposition of banded iron formations, and methane production in Archean oceans2019511eaav286910.1126/sciadv.aav2869
Thompson K J, Kenward P A, Bauer K W, et al. Photoferrotrophy, deposition of banded iron formations, and methane production in Archean oceans[J]. Science Advances, 2019, 5(11): eaav2869.
WangX GSunL RChenZ HLight inhibition of carbon mineralization associated with iron redox processes in calcareous paddy soil20202083171318010.1007/s11368-020-02660-w
Wang X G, Sun L R, Chen Z H, et al. Light inhibition of carbon mineralization associated with iron redox processes in calcareous paddy soil[J]. Journal of Soils and Sediments, 2020, 20(8): 3171-3180.
BotheHSchmitzOYatesM GNitrogen fixation and hydrogen metabolism in cyanobacteria201074452955110.1128/MMBR.00033-10
Bothe H, Schmitz O, Yates M G, et al. Nitrogen fixation and hydrogen metabolism in cyanobacteria[J]. Microbiology and Molecular Biology Reviews, 2010, 74(4): 529-551.
ChenP CLiX MLiF BShifts of microbial communities during Fe(II)oxidation coupled to nitrate reduction in paddy soil2017371358366
Chen P C, Li X M, Li F B. Shifts of microbial communities during Fe(II)oxidation coupled to nitrate reduction in paddy soil[J]. China Environmental Science. 2017, 37(1): 358-366.
DengT CQianY FChenX JCiceribacter ferrooxidans sp. nov., a nitrate-reducing Fe(II)-oxidizing bacterium isolated from ferrous ion-rich sediment202058535035610.1007/s12275-020-9471-2
Deng T C, Qian Y F, Chen X J, et al. Ciceribacter ferrooxidans sp. nov., a nitrate-reducing Fe(II)-oxidizing bacterium isolated from ferrous ion-rich sediment[J]. Journal of Microbiology, 2020, 58(5): 350-356.
WangRZhengPZhangMNitrate-dependent anaerobic ferrous/iron oxidation microorganism: Review on its species, distribution and characteristics2015421224482456
Wang R, Zheng P, Zhang M, et al. Nitrate-dependent anaerobic ferrous/iron oxidation microorganism: Review on its species, distribution and characteristics[J]. Microbiology China. 2015, 42(12): 2448-2456.
SunL RWangX GXuX FAnaerobic redox of iron oxides and photosynthetic oxidation of ferrous iron in upland cinnamon soils201552612911300
Sun L R, Wang X G, Xu X F, et al. Anaerobic redox of iron oxides and photosynthetic oxidation of ferrous iron in upland cinnamon soils[J]. Acta Pedologica Sinica, 2015, 52(6): 1291-1300.
WangX GSunL RMaL JTemperature sensitivity of iron redox processes in wetland soil in the Middle and Lower Reaches of the Yellow River2018552380389
Wang X G, Sun L R, Ma L J, et al. Temperature sensitivity of iron redox processes in wetland soil in the Middle and Lower Reaches of the Yellow River[J]. Acta Pedologica Sinica, 2018, 55(2): 380-389.
WangX GGuoD YZhangPEffect of illumination and water condition on iron redox cycle in paddy soil2014514853859
Wang X G, Guo D Y, Zhang P, et al. Effect of illumination and water condition on iron redox cycle in paddy soil[J]. Acta Pedologica Sinica, 2014, 51(4): 853-859.
SunL RWangX GGuoD YDynamics of anaerobic reduction of iron oxides in upland cinnamon soils2013501106112
Sun L R, Wang X G, Guo D Y, et al. Dynamics of anaerobic reduction of iron oxides in upland cinnamon soils[J]. Acta Pedologica Sinica, 2013, 50(1): 106-112.
LuR KBeijingChina Agricultural Science and Technology Press2000
Lu R K. Analytical method for soil and agricultural chemistry[M]. Beijing: China Agricultural Science and Technology Press, 2000.
鲁如坤北京中国农业科学技术出版社2000
鲁如坤. 土壤农业化学分析方法[M]. 北京: 中国农业科学技术出版社, 2000]
WangX GSunL RZhangY LCharacterization of reduction of iron oxide and oxidation of ferrous iron in upland cinnamon soil profiles in west Henan, China201855511991211
Wang X G, Sun L R, Zhang Y L, et al. Characterization of reduction of iron oxide and oxidation of ferrous iron in upland cinnamon soil profiles in west Henan, China[J]. Acta Pedologica Sinica, 2018, 55(5): 1199-1211.
LiX MZhangWLiuT XChanges in the composition and diversity of microbial communities during anaerobic nitrate reduction and Fe(II)oxidation at circumneutral pH in paddy soil2016947079
Li X M, Zhang W, Liu T X, et al. Changes in the composition and diversity of microbial communities during anaerobic nitrate reduction and Fe(II)oxidation at circumneutral pH in paddy soil[J]. Soil Biology and Biochemistry, 2016, 94: 70-79.
KapplerABryceCMansorMAn evolving view on biogeochemical cycling of iron2021196360374
Kappler A, Bryce C, Mansor M, et al. An evolving view on biogeochemical cycling of iron[J]. Nature Reviews Microbiology, 2021, 19(6): 360-374.
ClémentJShresthaJEhrenfeldJ GAmmonium oxidation coupled to dissimilatory reduction of iron under anaerobic conditions in wetland soils2005371223232328
Clément J, Shrestha J, Ehrenfeld J G, et al. Ammonium oxidation coupled to dissimilatory reduction of iron under anaerobic conditions in wetland soils[J]. Soil Biology and Biochemistry, 2005, 37(12): 2323-2328.
ShuaiWJafféP RAnaerobic ammonium oxidation coupled to iron reduction in constructed wetland mesocosms2019648984992
Shuai W, Jaffé P R. Anaerobic ammonium oxidation coupled to iron reduction in constructed wetland mesocosms[J]. Science of the Total Environment, 2019, 648: 984-992.
KuypersM M MMarchantH KKartalBThe microbial nitrogen-cycling network2018165263276
Kuypers M M M, Marchant H K, Kartal B. The microbial nitrogen-cycling network[J]. Nature Reviews Microbiology, 2018, 16(5): 263-276.
KraftBStrousMTegetmeyerH EMicrobial nitrate respiration–Genes, enzymes and environmental distribution20111551104117
Kraft B, Strous M, Tegetmeyer H E. Microbial nitrate respiration–Genes, enzymes and environmental distribution[J]. Journal of Biotechnology, 2011, 155(1): 104-117.
DangY ALiS QWangG DThe different characteristics of soil fixed ammonium from south to north on the Loess Plateau2007135831837
Dang Y A, Li S Q, Wang G D, et al. The different characteristics of soil fixed ammonium from south to north on the Loess Plateau[J]. Journal of Plant Nutrition and Fertilizers, 2007, 13(5): 831-837.
JamiesonJPrommerHKaksonenA HIdentifying and quantifying the intermediate processes during nitrate-dependent iron(II)oxidation2018521057715781
Jamieson J, Prommer H, Kaksonen A H, et al. Identifying and quantifying the intermediate processes during nitrate-dependent iron(II)oxidation[J]. Environmental Science & Technology, 2018, 52(10): 5771-5781.
KluegleinNKapplerAAbiotic oxidation of Fe(II)by reactive nitrogen species in cultures of the nitrate- reducing Fe(II)oxidizer Acidovorax sp. BoFeN1– questioning the existence of enzymatic Fe(II)oxidation2013112180190
Klueglein N, Kappler A. Abiotic oxidation of Fe(II)by reactive nitrogen species in cultures of the nitrate- reducing Fe(II)oxidizer Acidovorax sp. BoFeN1– questioning the existence of enzymatic Fe(II)oxidation[J]. Geobiology, 2013, 11(2): 180-190.