Production of reactive oxygen species and its role in mediating the abiotic transformation of organic carbon in sandy soil under vegetation restoration

Carbon Research - Tập 2 - Trang 1-15 - 2023
Fuhao Liu1,2, Kecheng Zhu1,2, Zhiqiang Wang1,2, Jinbo Liu1,2, Zheng Ni1,2, Yuanyuan Ding1,2, Chi Zhang1,2, Hanzhong Jia1,2
1College of Natural Resources and Environment, Northwest A&F University, Yangling, China
2Key Laboratory of Low-Carbon Green Agriculture in Northwestern China, Ministry of Agriculture and Rural Affairs, Yangling, China

Tóm tắt

The significant impact of vegetation restoration on the turnover of organic carbon (OC) is mainly attributed to biological processes. However, the contribution of abiotic processes associated with reactive oxygen species (ROS) during vegetation restoration has remained largely overlooked. Therefore, we systematically explored ROS distribution and production mechanisms in sandy soil and their corresponding effects on OC oxidation through field monitoring and incubation experiments. The cumulative concentrations of hydroxyl radicals (•OH) produced within 24 h varied in different soils undergoing vegetation restoration, ranging from 2.36 to 22.05 μmol kg‒1, which were derived from the Fenton-like reaction of hydrogen peroxide (H2O2) and biotic-induced Fe(II). In addition, during the oxidation of reductive SOC, H2O2 can be formed and react with Fe(II) to generate •OH. Further, •OH significantly induced the abiotic transformation of OC, accounting for 15.93%‒25.80% of carbon dioxide (CO2) efflux. Specifically, 1 mol •OH can induce the production of 0.01–0.02 mol CO2 for particulate organic carbon (POC) and 0.03‒0.23 mol CO2 for mineral-associated organic carbon (MOC), as demonstrated by chemical quenching and sterilisation experiments. This indicated that MOC was more sensitive to •OH attacks. Collectively, our findings provide insights into the accumulation of ROS in sandy soils during vegetation restoration, with •OH playing a key role in SOC oxidation, as well as the patterns of SOC turnover and its response to changes in the soil environment. • Vegetation restoration exerts a regulatory influence on ROS production in sandy soil. • ROS accumulation in tree-covered soil is more than that in shrub-covered soil. • 15.93%‒25.80% of total CO2 efflux in sandy soils is from •OH mediated OC mineralisation. • Mineral-associated OC exhibits a higher susceptibility to •OH attack than particulate OC.

Tài liệu tham khảo

Bao P, Li GX (2017) Sulfur-driven iron reduction coupled to anaerobic ammonium oxidation. Environ Sci Technol 51:6691–6698. https://doi.org/10.1021/acs.est.6b05971 Brookes PC, Kemmitt SJ, Addiscott TM, Bird N (2009) Reply to Kuzyakov et al’.s comments on our paper: ’Kemmitt, S. Lanyon, C. V., Waite, I.S., Wen, Q., O’Donnell, A.G., Brookes, P.C., 2008. Mineralization of native soil organic matter is not regulated by the size, activity or composition of the soil microbil biomass—a new perspective. Soil Biol Biochem 41:440–443. https://doi.org/10.1016/j.soilbio.2008.09.002 Burns JM, Craig PS, Shaw TJ, Ferry JL (2010) Multivariate examination of Fe(II)/Fe(III) cycling and consequent hydroxyl radical generation. Environ Sci Technol 44:7226–7231. https://doi.org/10.1021/es903519m Chao J, Liu YU, He H, Miao HT, Wu GL (2018) Formation of litter crusts and its multifunctional ecological effects in a desert ecosystem. Ecosphere 9:e02196. https://doi.org/10.1002/ecs2.2196 Chen C, Hall SJ, Coward E, Thompson A (2020) Iron-mediated organic matter decomposition in humid soils can counteract protection. Nat Commun 11:2255. https://doi.org/10.1038/s41467-020-16071-5 Chen N, Fu Q, Wu T, Cui P, Fang G, Liu C, Chen C, Liu G, Wang W, Wang D (2021) Active iron phases regulate the abiotic transformation of organic carbon during redox fluctuation cycles of paddy soil. Environ Sci Technol 55:14281–14293. https://doi.org/10.1021/acs.est.1c04073 Cotrufo MF, Soong JL, Horton AJ, Campbell EE, Haddix ML, Wall DH, Parton AJ (2015) Formation of soil organic matter via biochemical and physical pathways of litter mass loss. Nat Geosci 8:776–779. https://doi.org/10.1038/NGEO2520 Cotrufo MF, Ranalli MG, Haddix ML, Six J, Lugato E (2019) Soil carbon storage informed by particulate and mineral-associated organic matter. Nat Geosci 12:989–994. https://doi.org/10.1038/s41561-019-0484-6 Craig ME, Geyer KM, Beidler KV, Brzostek ER, Frey SD, Stuart Grandy A, Liang C, Phillips RP (2022) Fast-decaying plant litter enhances soil carbon in temperate forests but not through microbial physiological traits. Nat Commun 13:1229. https://doi.org/10.1038/s41467-022-28715-9 Cui YX, Wang X, Zhang XC, Ju WL, Duan CJ, Guo XB, Wang YQ, Fang LC (2020) Soil moisture mediates microbial carbon and phosphorus metabolism during vegetation succession in a semiarid region. Soil Biol Biochem 147:107814. https://doi.org/10.1016/j.soilbio.2020.107814 Dai HY, Wu BB, Chen BL, Ma B, Chu CH (2022) Diel Fluctuation of Extracellular Reactive Oxygen Species Production in the Rhizosphere of Rice. Environ Sci Technol 56:9075–9082. https://doi.org/10.1021/acs.est.2c00005 Diaz JM, Hansel CM, Voelker BM, Mendes CM, Zhang T (2013) Widespread production of extracellular superoxide by heterotrophic bacteria. Science 340:1223–1226. https://doi.org/10.1126/science.1237331 Dong, L., Li, J., Zhang, Y., Liu, Y., Li, A., Shangguan, Z., Deng, L., 2022. Forests have a higher soil C sequestration benefit due to lower C mineralization efficiency: Evidence from the central loess plateau case. Agric., Ecosyst. Environ. 339, 108144. https://doi.org/10.1016/j.agee.2022.108144. Duesterberg CK, Mylon SE, Waite TD (2008) pH effects on iron-catalyzed oxidation using Fenton’s reagent. Environ Sci Technol 42:8522–8527. https://doi.org/10.1021/es801720d Feng X, Fu B, Piao S, Wang S, Ciais P, Zeng Z, Lu Y, Zeng Y, Li Y, Jiang X, Wu B (2016) Revegetation in China’s Loess Plateau is approaching sustainable water resource limits. Nat Clim Change 6:1019–1022. https://doi.org/10.1038/NCLIMATE3092 Garrido-Ramirez EG, Theng B, Mora ML (2010) Clays and oxide minerals as catalysts and nanocatalysts in Fenton-like reactions — A review. Appl Clay Sci 47:182–192. https://doi.org/10.1016/j.clay.2009.11.044 Georgiou CD, Sun HJ, Mckay CP, Grintzalis K, Papapostolou I, Zisimopoulos D, Panagiotidis K, Zhang G, Koutsopoulou E, Christidis GE (2015) Evidence for photochemical production of reactive oxygen species in desert soils. Nat Commun 6:7100. https://doi.org/10.1038/ncomms8100 Gokdere B, Uzer A, Durmazel S, Ercag E, Apak R (2019) Titanium dioxide nanoparticles-based colorimetric sensors for determination of hydrogen peroxide and triacetone triperoxide (TATP). Talanta 202:402–410. https://doi.org/10.1016/j.talanta.2019.04.071 Goldstone JV, Pullin MJ, Bertilsson S, Voelker BM (2002) Reactions of hydroxyl radical with humic substances: Bleaching, mineralization, and production of bioavailable carbon substrates. Environ Sci Technol 36:364–372. https://doi.org/10.1021/es0109646 Hall SJ, Silver WL (2013) Iron oxidation stimulates organic matter decomposition in humid tropical forest soils. Global Change Biol 19:2804–2813. https://doi.org/10.1111/gcb.12229 Han RX, Lv JT, Huang ZQ, Zhang SH, Zhang SZ (2020) Pathway for the production of hydroxyl radicals during the microbially mediated redox transformation of iron (oxyhydr) oxides. Environ Sci Technol 54:902–910. https://doi.org/10.1021/acs.est.9b06220 Han RX, Wang Z, Lv J, Zhu Z, Yu GH, Li G, Zhu YG (2022) Multiple Effects of Humic Components on Microbially Mediated Iron Redox Processes and Production of Hydroxyl Radicals. Environ Sci Technol 56:16419–16427. https://doi.org/10.1021/acs.est.2c03799 Heckman K, Pries CEH, Lawrence CR, Rasmussen C, Crow SE, Hoyt AM, von Fromm SF, Shi Z, Stoner S, McGrath C, Beem-Miller J, Berhe AA, Blankinship JC, Keiluweit M, Marin-Spiotta E, Monroe JG, Plante AF, Schimel J, Sierra CA, Thompson A, Wagai R (2022) Beyond bulk: Density fractions explain heterogeneity in global soil carbon abundance and persistence. Global Change Biol 28:1178–1196. https://doi.org/10.1111/gcb.16023 Heimann M, Reichstein M (2008) Terrestrial ecosystem carbon dynamics and climate feedbacks. Nature 451:289–292. https://doi.org/10.1038/nature06591 Huang Y, Xin Z, Ran L, Qin Y, Cai M (2022) Topsoil carbon sequestration of vegetation restoration on the Loess Plateau. Ecol Eng 177:106570. https://doi.org/10.1016/j.ecoleng.2022.106570 Jansson JK, Hofmockel KS (2020) Soil microbiomes and climate change. Nat Rev Microbiol 18:35–46. https://doi.org/10.1038/s41579-019-0265-7 Jilling A, Keiluweit M, Gutknecht JLM, Grandy AS (2021) Priming mechanisms providing plants and microbes access to mineral-associated organic matter. Soil Biol Biochem 158:108256. https://doi.org/10.1016/j.soilbio.2021.108265 Kleber M, Bourg IC, Coward EK, Hansel CM, Myneni SCB, Nunan N (2021) Dynamic interactions at the mineral-organic matter interface. Nat Rev Earth Environ 2:402–421. https://doi.org/10.1038/s43017-021-00162-y Kuzyakov Y, Blagodatskaya E, Blagodatsky, S.,Comments on the paper by Kemmitt, et al (2009) (2008) ’Mineralization of native soil organic matter is not regulated by the size, activity or composition of the soil microbial biomass - a new perspective. Soil Biol Biochem 41:435–439. https://doi.org/10.1016/j.soilbio.2008.07.023 Lavallee, J.M., Soong, J.L., Cotrufo, M.F., 2020. Conceptualizing soil organic matter into particulate and mineral-associated forms to address global change in the 21st century. 26, 261–273. https://doi.org/10.1111/gcb.14859. Lehmann J, Hansel CM, Kaiser C, Kleber M, Maher K, Manzoni S, Nunan N, Reichstein M, Schimel JP, Torn MS, Wieder WR, Koegel-Knabner I (2020) Persistence of soil organic carbon caused by functional complexity. Nat Geosci 13:529–534. https://doi.org/10.1038/s41561-020-0612-3 Li G, Kim S, Han SH, Chang H, Du D, Son Y (2018) Precipitation affects soil microbial and extracellular enzymatic responses to warming. Soil Biol Biochem 120:212–221. https://doi.org/10.1016/j.soilbio.2018.02.014 Liang C, Schimel JP, Jastrow JD (2017) The importance of anabolism in microbial control over soil carbon storage. Nat Microbiol 2:17105–17110. https://doi.org/10.1038/nmicrobiol.2017.105 Liu XZ, Liu Y, Zhang L, Yin R, Wu GL (2021) Bacterial contributions of bio-crusts and litter crusts to nutrient cycling in the Mu Us Sandy Land. CATENA 199:105090. https://doi.org/10.1016/j.catena.2020.105090 Liu JB, Zhu KC, Zhang C, Zhang XC, Chen N, Jia HZ (2022) Microscale spatiotemporal variation and generation mechanisms of reactive oxygen species in the rhizosphere of ryegrass: Coupled biotic-abiotic processes. Environ Sci Technol 56:16483–16493. https://doi.org/10.1021/acs.est.2c06167 Lovley DR, Holmes DE, Nevin KP (2004) Dissimilatory Fe(III) and Mn(IV) reduction. Adv Microb Physiol 49:219–286. https://doi.org/10.1016/S0065-2911(04)49005-5 Melton ED, Swanner ED, Behrens S, Schmidt C, Kappler A (2014) The interplay of microbially mediated and abiotic reactions in the biogeochemical Fe cycle. Nat Rev Microbiol 12:797–808. https://doi.org/10.1038/nrmicro3347 Michlits H, Lier B, Pfanzagl V, Djinovic-Carugo K, Furtmuller PG, Oostenbrink C, Obinger C, Hofbauer S (2020) Actinobacterial Coproheme Decarboxylases Use Histidine as a Distal Base to Promote Compound I Formation. ACS Catal 10:5405–5418. https://doi.org/10.1021/acscatal.0c00411 Mopper K, Zhou X (1990) Hydroxyl radical photoproduction in the sea and its potential impact on marine processes. Science 250:661–664. https://doi.org/10.1126/science.250.4981.661 Murphy SA, Meng S, Solomon BM, Dias D, Shaw TJ, Ferry JL (2016) Hydrous ferric oxides in sediment catalyze formation of reactive oxygen species during sulfide oxidation. Front Mar Sci 3:1–12. https://doi.org/10.3389/fmars.2016.00227 Page SE, Sander M, Arnold WA, McNeill K (2012) Hydroxyl radical formation upon oxidation of reduced humic acids by oxygen in the dark. Environ Sci Technol 46:1590–1597. https://doi.org/10.1021/es203836f Page SE, Kling GW, Sander M, Harrold KH, Logan JR, McNeill K, Cory RM (2013) Dark formation of hydroxyl radical in arctic soil and surface waters. Environ Sci Technol 47:12860–12867. https://doi.org/10.1021/es4033265 Petigara BR, Blough NV, Mignerey AC (2002) Mechanisms of hydrogen peroxide decomposition in soils. Environ Sci Technol 36:639–645. https://doi.org/10.1021/es001726y Qiu HS, Ge TD, Liu JY, Chen XB, Hu YJ, Wu JS, Su YR, Kuzyakov Y (2018) Effects of biotic and abiotic factors on soil organic matter mineralization: Experiments and structural modeling analysis. Eur J Soil Biol 84:27–34. https://doi.org/10.1016/j.ejsobi.2017.12.003 Redanz S, Cheng XQ, Giacaman RA, Pfeifer CS, Merritt J, Kreth J (2018) Live and let die: Hydrogen peroxide production by the commensal flora and its role in maintaining a symbiotic microbiome. Mol Oral Microbiol 33:337–352. https://doi.org/10.1111/omi.12231 Rodrigues C, Borges R, Lima VN, Madeira LM (2018) p-Nitrophenol degradation by Fenton’s oxidation in a bubble column reactor. J Environ Manage 206:774–785. https://doi.org/10.1016/j.jenvman.2017.11.032 Schmidt MWI, Torn MS, Abiven S, Dittmar T, Guggenberger G, Janssens IA, Kleber M, Kogel-Knabner I, Lehmann J, Manning DAC, Nannipieri P, Rasse DP, Weiner S, Trumbore SE (2011) Persistence of soil organic matter as an ecosystem property. Nature 478:49–56. https://doi.org/10.1038/nature10386 Singh M, Sarkar B, Biswas B, Bolan NS, Churchman GJ (2017) Relationship between soil clay mineralogy and carbon protection capacity as influenced by temperature and moisture. Soil Biol Biochem 109:95–106. https://doi.org/10.1016/j.soilbio.2017.02.003 Tong M, Yuan SH, Ma SC, Jin MG, Liu D, Cheng D, Liu XX, Gan YQ, Wang YX (2016) Production of abundant hydroxyl radicals from oxygenation of subsurface sediments. Environ Sci Technol 50:214–221. https://doi.org/10.1021/acs.est.5b04323 Trusiak A, Treibergs LA, Kling GW, Cory RM (2018) The role of iron and reactive oxygen species in the production of CO2 in arctic soil waters. Geochim Cosmochim Acta 224:80–95. https://doi.org/10.1016/j.gca.2017.12.022 Vaughan PP, Blough NV (1998) Photochemical formation of hydroxyl radical by constituents of natural waters. Environ Sci Technol 32:2947–2953. https://doi.org/10.1021/es9710417 Waggoner DC, Chen HM, Willoughby AS, Hatcher PG (2015) Formation of black carbon-like and alicyclic aliphatic compounds by hydroxyl radical initiated degradation of lignin. Org Geochem 82:69–76. https://doi.org/10.1016/j.orggeochem.2015.02.007 Wang HH, Yue C, Mao QQ, Zhao J, Ciais P, Li W, Yu Q, Mu XM (2020) Vegetation and species impacts on soil organic carbon sequestration following ecological restoration over the Loess Plateau. China Geoderma 371:114389. https://doi.org/10.1016/j.geoderma.2020.114389 Witzgall K, Vidal A, Schubert DI, Hoschen C, Schweizer SA, Buegger F, Pouteau V, Chenu C, Mueller CW (2021) Particulate organic matter as a functional soil component for persistent soil organic carbon. Nat Commun 12:4115. https://doi.org/10.1038/s41467-021-24192-8 Yu GH, Kuzyakov Y (2021) Fenton chemistry and reactive oxygen species in soil: Abiotic mechanisms of biotic processes, controls and consequences for carbon and nutrient cycling. Earth-Sci Rev 214:103525. https://doi.org/10.1016/j.earscirev.2021.103525 Yu CL, Zhang YT, Lu YX, Qian A, Zhang P, Cui YP, Yuan SH (2021) Mechanistic insight into humic acid-enhanced hydroxyl radical production from Fe(II)-bearing clay mineral oxygenation. Environ Sci Technol 55:13366–13375. https://doi.org/10.1021/acs.est.1c02461 Yu WJ, Huang WJ, Weintraub-Leff SR, Hall SJ (2022) Where and why do particulate organic matter (POM) and mineral-associated organic matter (MAOM) differ among diverse soils? Soil Biol Biochem 172:108756. https://doi.org/10.1016/j.soilbio.2022.108756 Zeng DH, Hu YL, Chang SX, Fan ZP (2009) Land cover change effects on soil chemical and biological properties after planting Mongolian pine (Pinus sylvestris var. mongolica) in sandy lands in Keerqin, northeastern China. Plant Soil 317:121–133. https://doi.org/10.1007/s11104-008-9793-z Zhang T, Hansel CM, Voelker BM, Lamborg CH (2016) Extensive dark biological production of reactive oxygen species in brackish and freshwater ponds. Environ Sci Technol 50:2983–2993. https://doi.org/10.1021/acs.est.5b03906 Zhang W, Qiao W, Gao D, Dai Y, Deng J, Yang G, Han X, Ren G (2017) Relationship between soil nutrient properties and biological activities along a restoration chronosequence of Pinus tabulaeformis plantation forests in the Ziwuling Mountains, China. CATENA 161:85–95. https://doi.org/10.1016/j.catena.2017.10.021 Zhang BG, Li YN, Fei YM, Cheng YT (2021a) Novel Pathway for Vanadium(V) Bio-Detoxification by Gram-Positive Lactococcus raffinolactis. Environ Sci Technol 55:2121–2131. https://doi.org/10.1021/acs.est.0c07442 Zhang S, Lv J, Han R, Wang Z, Christie P, Zhang S (2021b) Sustained production of superoxide radicals by manganese oxides under ambient dark conditions. Water Res 196:117034. https://doi.org/10.1016/j.watres.2021.117034 Zhang Y, Zhang N, Qian A, Yu C, Zhang P, Yuan S (2022) Effect of C/Fe molar ratio on H2O2 and •OH production during oxygenation of Fe(II)-humic acid coexisting systems. Environ Sci Technol 56:13408–13418. https://doi.org/10.1021/acs.est.2c01312 Zhao YP, Xiang W, Huang CL, Liu Y, Tan Y (2021) Production of hydroxyl radicals following water-level drawdown in peatlands: A new induction mechanism for enhancing laccase activity in carbon cycling. Soil Biol Biochem 156:108241. https://doi.org/10.1016/j.soilbio.2021.108241 Zhao G, Wu B, Zheng X, Chen B, Kappler A, Chu C (2022) Tide-triggered production of reactive oxygen species in coastal soils. Environ Sci Technol 56:11888–11896. https://doi.org/10.1021/acs.est.2c03142 Zhu BZ, Zhao HT, Kalyanaraman B, Frei B (2002) Metal-independent production of hydroxyl radicals by halogenated quinones and hydrogen peroxide: An ESR spin trapping study. Free Radical Biol Med 32:465–473. https://doi.org/10.1016/S0891-5849(01)00824-3