Increasing of soil iron-bound organic carbon by microorganisms mediated iron/carbon cycle after the mattic layer slipped in alpine meadow

Chenglong Feng , Yuanjia Chen , Yanlin Cao , Deng Ao , Rafiq Anum , Zhaolong Zhu , Baorong Wang , Shaoshan An

Soil Ecology Letters ›› 2025, Vol. 7 ›› Issue (4) : 250342

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Soil Ecology Letters ›› 2025, Vol. 7 ›› Issue (4) : 250342 DOI: 10.1007/s42832-025-0342-y
RESEARCH ARTICLE

Increasing of soil iron-bound organic carbon by microorganisms mediated iron/carbon cycle after the mattic layer slipped in alpine meadow

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Abstract

Iron (Fe) binding was an important mechanism for the stabilisation of organic carbon (C) in soils. Slipping of the mattic layer exposes soils and changes the microbial Fe cycling and iron-bound organic carbon (Fe-OC) distribution. The coupled relationships were investigated among Fe, C, and key Fe redox cycling functional genes in the alpine meadows with and without mattic layer in the Qinghai-Tibet Plateau. Compared with the meadow layer and eluvial horizon, SOC content decreased by 17.7 g kg−1 from 39.7−90.3 g kg−1 after the mattic layer slipped, while the Fe-OC% increased from 2.7% and 5.7% to 12.7%. The proportion of the residual Fe fraction (RES-Fe) increased by 5.2% to 7.9%, and the organic matter-bound Fe fraction (OM-Fe) was decreased by 6%, the shift in Fe fractions caused an increase of Fe-OC%. Furthermore, the total average signal intensity of the genes for Fe cycling and redox was increased. The proportion of RES-Fe increased with CirA, feoB, fhuE and ahpC, fnr, narJ, perR, and soxR. The proportion of RED-Fe decreased with the fhuE and narI genes. In conclusion, the shift in Fe redox genes can be expected to increase the RES-Fe fractions, which promoted the accumulation of Fe-OC after the mattic layer slipped.

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Keywords

iron cycling / Fe-bound organic carbon / alpine meadow / mattic layer slip / Qinghai-Tibet Plateau

Highlight

● Fe-OC content decreased after the mattic layer slipped at the same soil horizon.

● Fe-OC and Fe redox gene diversity increased after the mattic layer slipped.

● The content of Fe-OC was influenced by RES-Fe and RED-Fe.

● RES-Fe and RED-Fe are mainly driven by genes fhuE and narI , respectively.

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Chenglong Feng, Yuanjia Chen, Yanlin Cao, Deng Ao, Rafiq Anum, Zhaolong Zhu, Baorong Wang, Shaoshan An. Increasing of soil iron-bound organic carbon by microorganisms mediated iron/carbon cycle after the mattic layer slipped in alpine meadow. Soil Ecology Letters, 2025, 7(4): 250342 DOI:10.1007/s42832-025-0342-y

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References

[1]

Abbott, B.W., Jones, J.B., Godsey, S.E., Larouche, J.R., Bowden, W.B., 2015. Patterns and persistence of hydrologic carbon and nutrient export from collapsing upland permafrost. Biogeosciences12, 3725–3740.

[2]

Arredondo, M.G., Lawrence, C.R., Schulz, M.S., Tfaily, M.M., Kukkadapu, R., Jones, M.E., Boye, K., Keiluweit, M., 2019. Root-driven weathering impacts on mineral-organic associations in deep soils over pedogenic time scales. Geochimica et Cosmochimica Acta263, 68–84.

[3]

Bao, S.D., 2007. Soil Agricultural Chemistry Analysis. 3rd ed. Beijing: China Agriculture Press20–65.

[4]

Chan, C.S., Emerson, D., Luther III, G.W., 2016. The role of microaerophilic Fe-oxidizing micro-organisms in producing banded iron formations. Geobiology14, 509–528.

[5]

Che, R.X., Wang, Y.F., Li, K.X., Xu, Z.H., Hu, J.M., Wang, F., Rui, Y.C., Li, L.F., Pang, Z., Cui, X.Y., 2019. Degraded patch formation significantly changed microbial community composition in alpine meadow soils. Soil and Tillage Research195, 104426.

[6]

Chen, C.M., Dynes, J.J., Wang, J., Sparks, D.L., 2014. Properties of Fe-organic matter associations via coprecipitation versus adsorption. Environmental Science & Technology48, 13751–13759.

[7]

Chen, H., Ju, P.J., Zhu, Q.A. Xu, X.L., Wu, N., Gao, Y.H., Feng, X.J., Tian, J.Q., Niu, S.L., Zhang, Y.J., Peng, C.H., Wang, Y.F., 2022. Carbon and nitrogen cycling on the Qinghai–Tibetan Plateau. Nature Reviews Earth & Environment3, 701–716.

[8]

Cutting, R.S., Coker, V.S., Fellowes, J.W., Lloyd, J.R., Vaughan, D.J., 2009. Mineralogical and morphological constraints on the reduction of Fe (III) minerals by Geobacter sulfurreducens. Geochimica et Cosmochimica Acta73, 4004–4022.

[9]

Dong, S.K., Shang, Z.H., Gao, J.X., Boone, R., 2022. Enhancing the ecological services of the Qinghai-Tibetan Plateau’s grasslands through sustainable restoration and management in era of global change. Agriculture, Ecosystems & Environment326, 107756.

[10]

Doran, G., Eberbach, P., Helliwell, S., 2006. The impact of rice plant roots on the reducing conditions in flooded rice soils. Chemosphere63, 1892–1902.

[11]

Duan, C.W., Li, X.L., Li, C.Y., Yang, P.N., Shi, Y., Chai, Y., Xu, W.Y., 2022. Analysis on the soil physical, chemical, and microbial community properties of different alpine meadow patches in the Source Zone of the Yellow River, West China. Ecological Indicators144, 109531.

[12]

Edwards, K.J., Rogers, D.R., Wirsen, C.O., McCollom, T.M., 2003. Isolation and characterization of novel psychrophilic, neutrophilic, Fe-oxidizing, chemolithoautotrophic α- and γ-Proteobacteria from the deep sea. Applied and Environmental Microbiology69, 2906–2913.

[13]

Eusterhues, K., Rumpel, C., Kögel-Knabner, I., 2005. Stabilization of soil organic matter isolated via oxidative degradation. Organic Geochemistry36, 1567–1575.

[14]

Hedrich, S., Schlömann, M., Johnson, D.B. 2011. The iron-oxidizing proteobacteria. Microbiology157, 1551–1564.

[15]

Huang, K., Zhang, Y.J., Zhu, J.T., Liu, Y.J., Zu, J.X., Zhang, J., 2016. The influences of climate change and human activities on vegetation dynamics in the Qinghai-Tibet Plateau. Remote Sensing8, 876.

[16]

Huang, R., Dong, M.L., Mao, P., Zhuang, P., Paz-Ferreiro, J., Li, Y.X., Li, Y.W., Hu, X.Y., Netherway, P., Li, Z.A., 2020. Evaluation of phytoremediation potential of five Cd (hyper)accumulators in two Cd contaminated soils. Science of the Total Environment721, 137581.

[17]

Jensen, A.E., Lohse, K.A., Crosby, B.T., Mora, C.I., 2014. Variations in soil carbon dioxide efflux across a thaw slump chronosequence in northwestern Alaska. Environmental Research Letters9, 025001.

[18]

Jiao, Y.Q., Kappler, A., Croal, L.R., Newman, D.K., 2005. Isolation and characterization of a genetically tractable photoautotrophic Fe(II)-oxidizing bacterium, Rhodopseudomonas palustris strain TIE-1. Applied and Environmental Microbiology71, 4487–4496.

[19]

Kato, S., Ohkuma, M., 2021. A single bacterium capable of oxidation and reduction of iron at circumneutral pH. Microbiology Spectrum9, e0016121.

[20]

Kramer, M.G., Chadwick, O.A., 2018. Climate-driven thresholds in reactive mineral retention of soil carbon at the global scale. Nature Climate Change8, 1104–1108.

[21]

Lalonde, K., Mucci, A., Ouellet, A., Gélinas, Y., 2012. Preservation of organic matter in sediments promoted by iron. Nature483, 198–200.

[22]

Lehmann, J., Bossio, D.A., Kögel-Knabner, I., Rillig, M.C., 2020. The concept and future prospects of soil health. Nature Reviews Earth & Environment1, 544–553.

[23]

Li, Y., Dong, S.K., Liu, S.L., Su, X.K., Wang, X.X., Zhang, Y., Zhao, Z.Z., Gao, X.X., Li, S., Tang, L., 2019. Relationships between plant diversity and biomass production of alpine grasslands are dependent on the spatial scale and the dimension of biodiversity. Ecological Engineering127, 375–382.

[24]

Liu, Y.B., Wang, Y.S., Wang, Z.R., Gao, T.P., 2022. Characteristics of iron cycle and its driving mechanism during the development of biological soil crusts associated with desert revegetation. Soil Biology and Biochemistry164, 108487.

[25]

Liu, Y.B., Zhao, L.N., Wang, Z.R., Liu, L.C., Zhang, P., Sun, J.Y., Wang, B.Y., Song, G., Li, X.R., 2018. Changes in functional gene structure and metabolic potential of the microbial community in biological soil crusts along a revegetation chronosequence in the Tengger Desert. Soil Biology and Biochemistry126, 40–48.

[26]

Mcbeth, J.M., Little, B.J., Ray, R.I., Farrar, K.M., Emerson, D., 2011. Neutrophilic iron-oxidizing "Zetaproteobacteria" and mild steel corrosion in nearshore marine environments. Applied and Environmental Microbiology77, 1405–1412.

[27]

Melton, E.D., Swanner, E.D., Behrens, S., Schmidt, C., Kappler, A., 2014. The interplay of microbially mediated and abiotic reactions in the biogeochemical Fe cycle. Nature Reviews Microbiology12, 797–808.

[28]

Mikutta, R., Lorenz, D., Guggenberger, G., Haumaier, L., Freund, A., 2014. Properties and reactivity of Fe-organic matter associations formed by coprecipitation versus adsorption: clues from arsenate batch adsorption. Geochimica et Cosmochimica Acta144, 258–276.

[29]

Mu, C.C., Abbott, B.W., Zhao, Q., Su, H., Wang, S.F., Wu, Q.B., Zhang, T.J., Wu, X.D., 2017. Permafrost collapse shifts alpine tundra to a carbon source but reduces N2O and CH4 release on the northern Qinghai-Tibetan Plateau. Geophysical Research Letters44, 8945–8952.

[30]

Mu, C.C., Zhang, F., Mu, M., Chen, X., Li, Z.L., Zhang, T.J., 2020. Organic carbon stabilized by iron during slump deformation on the Qinghai-Tibetan Plateau. Catena187, 104282.

[31]

Mu, C.C., Zhang, T.J., Zhao, Q., Guo, H., Zhong, W., Su, H., Wu, Q.B., 2016. Soil organic carbon stabilization by iron in permafrost regions of the Qinghai-Tibet Plateau. Geophysical Research Letters43, 10286–10294.

[32]

Niu, W., Zhang, Y.P., Liu, J.Q., Wen, T., Miao, T., Basit, A., Jiang, W., 2020. OxyR controls magnetosome formation by regulating magnetosome island (MAI) genes, iron metabolism, and redox state. Free Radical Biology and Medicine161, 272–282.

[33]

Pan, W.N., Kan, J.J., Inamdar, S., Chen, C.M., Sparks, D., 2016. Dissimilatory microbial iron reduction release DOC (dissolved organic carbon) from carbon-ferrihydrite association. Soil Biology and Biochemistry103, 232–240.

[34]

Paula, F.S., Rodrigues, J.L.M., Zhou, J.Z., Wu, L.Y., Mueller, R.C., Mirza, B.S., Bohannan, B.J.M., Nüsslein, K., Deng, Y., Tiedje, J.M., Pellizari, V.H., 2014. Land use change alters functional gene diversity, composition and abundance in Amazon forest soil microbial communities. Molecular Ecology23, 2988–2999.

[35]

Pizano, C., Barón, A.F., Schuur, E.A.G., Crummer, K.G., Mack, M.C., 2014. Effects of thermo-erosional disturbance on surface soil carbon and nitrogen dynamics in upland arctic tundra. Environmental Research Letters9, 075006.

[36]

Qu, J.P., Liu, M., Yang, M., Zhang, Z.B., Zhang, Y.M., 2015. Effects of fertility control in plateau pikas (Ochotona curzoniae) on diversity of native birds on Tibetan Plateau. Acta Theriologica Sinica35, 164–169.

[37]

Riedel, T., Zak, D., Biester, H., Dittmar, T., 2013. Iron traps terrestrially derived dissolved organic matter at redox interfaces. Proceedings of the National Academy of Sciences of the United States of America110, 10101–10105.

[38]

Singh, M., Sarkar, B., Sarkar, S., Churchman, J., Bolan, N., Mandal, S., Menon, M., Purakayastha, T.J., Beerling, D.J., 2018. Stabilization of soil organic carbon as influenced by clay mineralogy. Advances in Agronomy148, 33–84.

[39]

Sobolev, D., Roden, E.E., 2001. Suboxic deposition of ferric iron by bacteria in opposing gradients of Fe(II) and oxygen at circumneutral pH. Applied and Environmental Microbiology67, 1328–1334.

[40]

Song, Z.H., Li, X.L., Li, J.X., Kazhao, C. R., Ma, G.L, 2020. Effects of plateau pika (Ochotona curzoniae) trails on enlargement and connection of degraded patches in alpine meadow. Chinese Journal of Ecology39, 3276–3284.

[41]

Sun, X.J., Zhang, Q.G., Li, M.Y., Wang, J., Lu, Z.J., Guo, J.M., Kang, S.C., Shi, J.B., 2023. Insight into the relationships between total suspended particles and mercury in meltwater in a typical glacierized basin in the inland Tibetan Plateau. Journal of Hazardous Materials452, 131250.

[42]

Wagai, R., Mayer, L.M., 2007. Sorptive stabilization of organic matter in soils by hydrous iron oxides. Geochimica et Cosmochimica Acta71, 25–35.

[43]

Wang, G.X., Mao, T.X., Chang, J., Du, J.Z., 2014. Impacts of surface soil organic content on the soil thermal dynamics of alpine meadows in permafrost regions: data from field observations. Geoderma232–234, 414–425.

[44]

Wang, K.L., Ma, X., Li, D.B., Qi, Y.L., Hua, Z.S., Tian, T., Liu, D.F., Min, D., Li, W.W., Huang, G.X., Yu, H.Q. 2024. Single phototrophic bacterium-mediated iron cycling in aquatic environments. Research7, 0528.

[45]

Wang, Y.C., Lu, G.X., Yu, H., Du, X.F., He, Q., Yao, S.T., Zhao, L.R., Huang, C.X., Wen, X.C., Deng, Y., 2021. Meadow degradation increases spatial turnover rates of the fungal community through both niche selection and dispersal limitation. Science of the Total Environment798, 149362.

[46]

Weber, K.A., Achenbach, L.A., Coates, J.D., 2006. Microorganisms pumping iron: anaerobic microbial iron oxidation and reduction. Nature Reviews Microbiology4, 752–764.

[47]

Weiss, J.V., Emerson, D., Backer, S.M., Megonigal, J.P., 2003. Enumeration of Fe(II)-oxidizing and Fe(III)-reducing bacteria in the root zone of wetland plants: implications for a rhizosphere iron cycle. Biogeochemistry64, 77–96.

[48]

Wiesmeier, M., Urbanski, L., Hobley, E., Lang, B., von Lützow, M., Marin-Spiotta, E., van Wesemael, B., Rabot, E., Ließ, M., Garcia-Franco, N., Wollschläger, U., Vogel, H.J., Kögel -Knabner, I., 2019. Soil organic carbon storage as a key function of soils - A review of drivers and indicators at various scales. Geoderma333, 149–162.

[49]

Yu, G.H., Xiao, J., Hu, S.J., Polizzotto, M.L., Zhao, F.J., McGrath, S.P., Li, H., Ran,W., Shen, Q.R., 2017. Mineral availability as a key regulator of soil carbon storage. Environmental Science & Technology51, 4960–4969.

[50]

Yu, J.L., Wan, L.F., Liu, G.H., Ma, K.M., Cheng, H., Shen, Y., Liu, Y.Q., Su, X.K., 2022. A meta-analysis on degraded alpine grassland mediated by climate factors: enlightenment for ecological restoration. Frontiers in Plant Science12, 821954.

[51]

Yue, H.W., Wang, M.M., Wang, S.P., Gilbert, J.A., Sun, X., Wu, L.W., Lin, Q.Y., Hu, Y.G., Li, X.Z., He, Z.L., Zhou, J.Z., Yang, Y.F., 2015. The microbe-mediated mechanisms affecting topsoil carbon stock in Tibetan grasslands. The ISME Journal9, 2012–2020.

[52]

Zhang, G.F., Nan, Z.T., Wu, X.B., Ji, H.L., Zhao, S.P., 2019. The role of winter warming in permafrost change over the Qinghai-Tibet Plateau. Geophysical Research Letters46, 11261–11269.

[53]

Zhang, G.L., Yang, F., Long, H., 2023. Save the life-sustaining mattic layer on the Qinghai-Tibetan Plateau. The Innovation4, 100418.

[54]

Zhang, Y., Dong, S.K., Gao, Q.Z., Liu, S.L., Zhou, H.K., Ganjurjav, H., Wang, X.X., 2016. Climate change and human activities altered the diversity and composition of soil microbial community in alpine grasslands of the Qinghai-Tibetan Plateau. Science of the Total Environment562, 353–363.

[55]

Zhao, Q., Dunham-Cheatham, S., Adhikari, D., Chen, C.M., Patel, A, Poulson, S.R., Obrist, D., Verburg, P.S.J., Wang, X.L., Roden, E.R., Thompson, A., Yang, Y., 2020. Oxidation of soil organic carbon during an anoxic-oxic transition. Geoderma377, 114584.

[56]

Zhou, J., Bruns, M.A., Tiedje, J.M., 1996. DNA recovery from soils of diverse composition. Applied and Environmental Microbiology62, 316–322.

[57]

Zhou, J.Z., Xue, K., Xie, J.P., Deng, Y., Wu, L.Y., Cheng, X.L., Fei, S.F., Deng, S.P., He, Z.L., Van Nostrand, J.D., Luo, Y.Q., 2012. Microbial mediation of carbon-cycle feedbacks to climate warming. Nature Climate Change2, 106–110.

[58]

Zou, Y.C., Lu, X.G., Jiang, M., 2009. Dynamics of dissolved iron under pedohydrological regime caused by pulsed rainfall events in wetland soils. Geoderma150, 46–53.

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