Abstract
Several studies have suggested the pivotal roles of eutrophic lakes in carbon (C) cycling at regional and global scales. However, how the co-metabolism effect on lake sediment organic carbon (OC) mineralization changes in response to integrated inputs of labile OC and nutrients is poorly understood. This knowledge gap hinders our ability to predict the carbon sequestration potential in eutrophic lakes. Therefore, a 45-day microcosm experiment was conducted to examine the dominant mechanisms that underpin the co-metabolism response to the inputs of labile C and nutrients in lacustrine sediments. Results indicate that the labile C addition caused a rapid increase in the positive co-metabolism effect during the initial stage of incubation, and the co-metabolism effect was positively correlated with the C input level. The positive co-metabolism effect was consistently higher under high C input, which was 152% higher than that under low C input. The higher β-glucosidase activity after nutrient addition, which, in turn, promoted the OC mineralization in sediments. In addition, different impacts of nutrients on the co-metabolism effect under different C inputs were observed. Compared with the low nutrient treatments, the largest co-metabolism effect under high C with high nutrient treatment was observed by the end of the incubation. In the high C treatment, the intensity of the co-metabolism effect (CE) under high nitrogen treatment was 1.88 times higher than that under low nitrogen condition. However, in the low C treatment, the amount of nitrogen had limited impact on co-metabolism effect. Our study thus proved that the microorganisms obviously regulate sediment OC turnover via stoichiometric flexibility to maintain a balance between resources and microbial requirements, which is meaningful for evaluating the OC budget and lake eutrophication management in lacustrine sediments.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data Availability Statement
The data that support the findings of this study are available from the corresponding author upon reasonable request.
References
Bastida F, Torres I F, Hernández T, Bombach P, Richnow H H, García C. 2013. Can the labile carbon contribute to carbon immobilization in semiarid soils? Priming effects and microbial community dynamics. Soil Biology and Biochemistry, 57: 892–902, https://doi.org/10.1016/j.soilbio.2012.10.037.
Bell C W, Fricks B E, Rocca J D, Steinweg J M, McMahon S K, Wallenstein M D. 2013. High-throughput fluorometric measurement of potential soil extracellular enzyme activities. Journal of Visualized Experiments, (81): e50961, https://doi.org/10.3791/50961.
Bianchi T S, Thornton D C O, Yvon-Lewis S A, King G M, Eglinton T I, Shields M R, Ward N D, Curtis J. 2015. Positive priming of terrestrially derived dissolved organic matter in a freshwater microcosm system. Geophysical Research Letters, 42(13): 5460–5467, https://doi.org/10.1002/2015GL064765.
Bianchi T S. 2011. The role of terrestrially derived organic carbon in the coastal ocean: a changing paradigm and the priming effect. Proceedings of the National Academy of Sciences of the United States of America, 108(49): 19473–19481, https://doi.org/10.1073/pnas.1017982108.
Blagodatskaya E V, Blagodatsky S A, Anderson T H, Kuzyakov Y. 2009. Contrasting effects of glucose, living roots and maize straw on microbial growth kinetics and substrate availability in soil. European Journal of Soil Science, 60(2): 186–197, https://doi.org/10.1111/j.1365-2389.2008.01103.x.
Blagodatskaya E, Kuzyakov Y. 2008. Mechanisms of real and apparent priming effects and their dependence on soil microbial biomass and community structure: critical review. Biology and Fertility of Soils, 45(2): 115–131, https://doi.org/10.1007/s00374-008-0334-y.
Bremer E, Kuikman P. 1994. Microbial utilization of 14C[U] glucose in soil is affected by the amount and timing of glucose additions. Soil Biology and Biochemistry, 26(4): 511–517, https://doi.org/10.1016/0038-0717(94)90184-8.
Chen R R, Senbayram M, Blagodatsky S, Myachina O, Dittert K, Lin X G, Blagodatskaya E, Kuzyakov Y. 2014. Soil C and N availability determine the priming effect: microbial N mining and stoichiometric decomposition theories. Global Change Biology, 20(7): 2356–2367, https://doi.org/10.1111/gcb.12475.
Cole J J, Prairie Y T, Caraco N F, McDowell W H, Tranvik L J, Striegl R G, Duarte C M, Kortelainen P, Downing J A, Middelburg J J, Melack J. 2007. Plumbing the global carbon cycle: integrating inland waters into the terrestrial carbon budget. Ecosystems, 10(1): 172–185, https://doi.org/10.1007/s10021-006-9013-8.
Craine J M, Morrow C, Fierer N. 2007. Microbial nitrogen limitation increases decomposition. Ecology, 88(8): 2105–2113, https://doi.org/10.1890/06-1847.1.
Dai J H, Sun M Y, Culp R A, Noakes J E. 2009. A laboratory study on biochemical degradation and microbial utilization of organic matter comprising a marine diatom, land grass, and salt marsh plant in estuarine ecosystems. Aquatic Ecology, 43(4): 825–841, https://doi.org/10.1007/s10452-008-9211-x.
De Graaff M A, Classen A T, Castro H F, Schadt C W. 2010. Labile soil carbon inputs mediate the soil microbial community composition and plant residue decomposition rates. New Phytologist, 188(4): 1055–1064, https://doi.org/10.1111/j.1469-8137.2010.03427.x.
Di Lonardo D P, de Boer W, Zweers H, van der Wal A. 2019. Effect of the amount of organic trigger compounds, nitrogen and soil microbial biomass on the magnitude of priming of soil organic matter. PloS One, 14(5): e0216730, https://doi.org/10.1371/journal.pone.0216730.
Fang Y Y, Nazaries L, Singh B K, Singh B P. 2018. Microbial mechanisms of carbon priming effects revealed during the interaction of crop residue and nutrient inputs in contrasting soils. Global Change Biology, 24(7): 2775–2790, https://doi.org/10.1111/gcb.14154.
Fontaine S, Bardoux G, Benest D, Verdier B, Mariotti A, Abbadie L. 2004. Mechanisms of the priming effect in a Savannah soil amended with cellulose. Soil Science Society of America Journal, 68(1): 125–131, https://doi.org/10.2136/sssaj2004.1250.
Grasset C, Mendonça R, Villamor Saucedo G, Bastviken D, Roland F, Sobek S. 2018. Large but variable methane production in anoxic freshwater sediment upon addition of allochthonous and autochthonous organic matter. Limnology and Oceanography, 63(4): 1488–1501, https://doi.org/10.1002/lno.10786.
Gudasz C, Bastviken D, Steger K, Premke K, Sobek S, Tranvik L J. 2010. Temperature-controlled organic carbon mineralization in lake sediments. Nature, 466(7305): 478–481, https://doi.org/10.1038/nature09186.
Guenet B, Danger M, Abbadie L, Lacroix G. 2010a. Priming effect: bridging the gap between terrestrial and aquatic ecology. Ecology, 91(10): 2850–2861, https://doi.org/10.1890/09-1968.1.
Guenet B, Danger M, Harrault L, Allard B, Jauset-Alcala M, Bardoux G, Benest D, Abbadie L, Lacroix G. 2014. Fast mineralization of land-born C in inland waters: first experimental evidences of aquatic priming effect. Hydrobiologia, 721(1): 35–44, https://doi.org/10.1007/s10750-013-1635-1.
Guenet B, Neill C, Bardoux G, Abbadie L. 2010b. Is there a linear relationship between priming effect intensity and the amount of organic matter input? Applied Soil Ecology, 46(3): 436–442, https://doi.org/10.1016/j.apsoil.2010.09.006.
Hanamachi Y, Hama T, Yanai T. 2008. Decomposition process of organic matter derived from freshwater phytoplankton. Limnology, 9(1): 57–69, https://doi.org/10.1007/s10201-007-0232-2.
Heuck C, Weig A, Spohn M. 2018. Corrigendum to Heuck et al. (2015) ‘Soil microbial biomass C:N:P stoichiometry and microbial use of organic phosphorus’, Soil Biology & Biochemistry 85, 119–129. Soil Biology and Biochemistry, 127: 329–330, https://doi.org/10.1016/j.soilbio.2018.09.011.
Horvath R S. 1972. Microbial co-metabolism and the degradation of organic compounds in nature. Bacteriological Reviews, 36(2): 146–155, https://doi.org/10.1128/br.36.2.146-155.1972.
Huang C C, Chen Z L, Gao Y, Luo Y, Huang T, Zhu A X, Yang H, Yang B J. 2019. Enhanced mineralization of sedimentary organic carbon induced by excess carbon from phytoplankton in a eutrophic plateau lake. Journal of Soils and Sediments, 19(5): 2613–2623, https://doi.org/10.1007/s11368-019-02261-2.
Ji Z H, Long Z W, Zhang Y, Wang Y K, Qi X Y, Xia X H, Pei Y S. 2021. Enrichment differences and source apportionment of nutrients, stable isotopes, and trace metal elements in sediments of complex and fragmented wetland systems. Environmental Pollution, 289: 117852, https://doi.org/10.1016/j.envpol.2021.117852.
Kuzyakov Y, Bol R. 2006. Sources and mechanisms of priming effect induced in two grassland soils amended with slurry and sugar. Soil Biology and Biochemistry, 38(4): 747–758, https://doi.org/10.1016/j.soilbio.2005.06.025.
Kuzyakov Y, Friedel J K, Stahr K. 2000. Review of mechanisms and quantification of priming effects. Soil Biology and Biochemistry, 32(11–12): 1485–1498, https://doi.org/10.1016/S0038-0717(00)00084-5.
Li X, Cui B S, Yang Q C, Lan Y, Wang T T, Han Z. 2013. Effects of plant species on macrophyte decomposition under three nutrient conditions in a eutrophic shallow lake, North China. Ecological Modelling, 252: 121–128, https://doi.org/10.1016/j.ecolmodel.2012.08.006.
Liu C, Shen Q S, Zhou Q L, Fan C X, Shao S G. 2015. Precontrol of algae-induced black blooms through sediment dredging at appropriate depth in a typical eutrophic shallow lake. Ecological Engineering, 77: 139–145, https://doi.org/10.1016/j.ecoleng.2015.01.030.
Liu X S, Shi C F, Xu X G, Li X J, Xu Y, Huang H Y, Zhao Y P, Zhou Y W, Shen H C, Chen C, Wang G X. 2017. Spatial distributions of β-cyclocitral and β-ionone in the sediment and overlying water of the west shore of Taihu Lake. Science of the Total Environment, 579: 430–438, https://doi.org/10.1016/j.scitotenv.2016.11.079.
Löhnis F. 1926. Effect of growing legumes upon succeeding crops. Soil Science, 22(5): 355–389, https://doi.org/10.1097/00010694-192611000-00002.
Luo Y, Zhu Z K, Liu S L, Peng P Q, Xu J M, Brookes P, Ge T D, Wu J S. 2019. Nitrogen fertilization increases rice rhizodeposition and its stabilization in soil aggregates and the humus fraction. Plant and Soil, 445(1–2): 125–135, https://doi.org/10.1007/s11104-018-3833-0.
Lyu M, Nie Y Y, Giardina C P, Vadeboncoeur M A, Ren Y B, Fu Z Q, Wang M H, Jin C S, Liu X M, Xie J S. 2019. Litter quality and site characteristics interact to affect the response of priming effect to temperature in subtropical forests. Functional Ecology, 33(11): 2226–2238, https://doi.org/10.1111/1365-2435.13428.
Ma J R, Qin B Q, Paerl H W, Brookes J D, Hall N S, Shi K, Zhou Y Q, Guo J S, Li Z, Xu H, Wu T F, Long S X. 2016. The persistence of cyanobacterial (Microcystis spp.) blooms throughout winter in Lake Taihu, China. Limnology and Oceanography, 61(2): 711–722, https://doi.org/10.1002/lno.10246.
Ma J, Xu X G, Yu C C, Liu H C, Wang G X, Li Z C, Xu B, Shi R J. 2020. Molecular biomarkers reveal co-metabolism effect of organic detritus in eutrophic lacustrine sediments. Science of the Total Environment, 698: 134328, https://doi.org/10.1016/j.scitotenv.2019.134328.
Otten T G, Xu H, Qin B, Zhu G, Paerl H W. 2012. Spatiotemporal patterns and ecophysiology of toxigenic Microcystis blooms in Lake Taihu, China: implications for water quality management. Environmental Science & Technology, 46(6): 3480–3488, https://doi.org/10.1021/es2041288.
Phillips R P, Meier I C, Bernhardt E S, Grandy A S, Wickings K, Finzi A C. 2012. Roots and fungi accelerate carbon and nitrogen cycling in forests exposed to elevated CO2. Ecology Letters, 15(9): 1042–1049, https://doi.org/10.1111/j.1461-0248.2012.01827.x.
Qiao N, Schaefer D, Blagodatskaya E, Zou X M, Xu X L, Kuzyakov Y. 2014. Labile carbon retention compensates for CO2 released by priming in forest soils. Global Change Biology, 20(6): 1943–1954, https://doi.org/10.1111/gcb.12458.
Qin B Q, Paerl H W, Brookes J D, Liu J G, Jeppesen E, Zhu G W, Zhang Y L, Xu H, Shi K, Deng J M. 2019. Why Lake Taihu continues to be plagued with cyanobacterial blooms through 10 years (2007–2017) efforts. Science Bulletin, 64(6): 354–356, https://doi.org/10.1016/j.scib.2019.02.008.
Qin B Q, Xu P Z, Wu Q L, Luo L C, Zhang Y L. 2007. Environmental issues of Lake Taihu, China. Hydrobiologia, 581(1): 3–14, https://doi.org/10.1007/s10750-006-0521-5.
Qin B Q, Yang G J, Ma J R, Wu T F, Li W, Liu L Z, Deng J M, Zhou J. 2018. Spatiotemporal changes of cyanobacterial bloom in large shallow eutrophic lake Taihu, China. Frontiers in Microbiology, 9: 451, https://doi.org/10.3389/fmicb.2018.00451.
Razanamalala K, Fanomezana R A, Razafimbelo T, Chevallier T, Trap J, Blanchart E, Bernard L. 2018. The priming effect generated by stoichiometric decomposition and nutrient mining in cultivated tropical soils: actors and drivers. Applied Soil Ecology, 126: 21–33, https://doi.org/10.1016/j.apsoil.2018.02.008.
Scheffer M, Carpenter S, Foley J A, Folke C, Walker B. 2001. Catastrophic shifts in ecosystems. Nature, 413(6856): 591–596, https://doi.org/10.1038/35098000.
Scheffer M, Hosper S H, Meijer M L, Moss B, Jeppesen E. 1993. Alternative equilibria in shallow lakes. Trends in Ecology & Evolution, 8(8): 275–279, https://doi.org/10.1016/0169-5347(93)90254-M.
Shi K, Zhang Y L, Xu H, Zhu G W, Qin B Q, Huang C C, Liu X H, Zhou Y Q, Lv H. 2015. Long-term satellite observations of microcystin concentrations in Lake Taihu during cyanobacterial bloom periods. Environmental Science & Technology, 49(11): 6448–6456, https://doi.org/10.1021/es505901a.
Sobek S, Durisch-Kaiser E, Zurbrügg R, Wongfun N, Wessels M, Pasche N, Wehrli B. 2009. Organic carbon burial efficiency in lake sediments controlled by oxygen exposure time and sediment source. Limnology and Oceanography, 54(6): 2243–2254, https://doi.org/10.4319/lo.2009.54.6.2243.
Van Nugteren P, Moodley L, Brummer G J, Heip C H R, Herman P M J, Middelburg J J. 2009. Seafloor ecosystem functioning: the importance of organic matter priming. Marine Biology, 156(11): 2277–2287, https://doi.org/10.1007/s00227-009-1255-5.
Wakeham S G, Canuel E A. 2006. Degradation and preservation of organic matter in marine sediments. In: Volkman J K ed. Marine Organic Matter: Biomarkers, Isotopes and DNA. Springer, Berlin Heidelberg. p.295–321, https://doi.org/10.1007/698_2_009.
Wang D D, Zhu Z K, Shahbaz M, Chen L, Liu S L, Inubushi K, Wu J S, Ge T D. 2019. Split N and P addition decreases straw mineralization and the priming effect of a paddy soil: a 100-day incubation experiment. Biology and Fertility of Soils, 55(7): 701–712, https://doi.org/10.1007/s00374-019-01383-6.
Wang H, Boutton T W, Xu W H, Hu G Q, Jiang P, Bai E. 2015. Quality of fresh organic matter affects priming of soil organic matter and substrate utilization patterns of microbes. Scientific Reports, 5(1): 10102, https://doi.org/10.1038/srep10102.
Xu X G, Li W, Fujibayashi M, Nomura M, Nishimura O, Li X N. 2015. Predominance of terrestrial organic matter in sediments from a cyanobacteria-blooming hypereutrophic lake. Ecological Indicators, 50: 35–43, https://doi.org/10.1016/j.ecolind.2014.10.020.
Yan X C, Xu X G, Wang M Y, Wang G X, Wu S J, Li Z C, Sun H, Shi A, Yang Y H. 2017. Climate warming and cyanobacteria blooms: looks at their relationships from a new perspective. Water Research, 125: 449–457, https://doi.org/10.1016/j.watres.2017.09.008.
Zhao Y P, Zhang Z Q, Wang G X, Li X J, Ma J, Chen S, Deng H, Annalisa O H. 2019. High sulfide production induced by algae decomposition and its potential stimulation to phosphorus mobility in sediment. Science of the Total Environment, 650: 163–172, https://doi.org/10.1016/j.scitotenv.2018.09.010.
Zhu Z K, Ge T D, Luo Y, Liu S L, Xu X L, Tong C L, Shibistova O, Guggenberger G, Wu J S. 2018. Microbial stoichiometric flexibility regulates rice straw mineralization and its priming effect in paddy soil. Soil Biology and Biochemistry, 121: 67–76, https://doi.org/10.1016/j.soilbio.2018.03.003.
Author information
Authors and Affiliations
Corresponding author
Additional information
Supported by the National Natural Science Foundation of China (No. 42077294), the Special basic research service for the Central Level Public Welfare Research Institute (No. GYZX210517), the Major Science and Technology Program for Water Pollution Control and Treatment (Nos. 2017ZX07203-003, 2017ZX07301006), and the Excellent Young Talents Fund Program of Higher Education Institutions of Anhui Province (No. gxyqZD2020047)
Rights and permissions
About this article
Cite this article
Ma, J., He, F., Yan, X. et al. Stoichiometric flexibility regulates the co-metabolism effect during organic carbon mineralization in eutrophic lacustrine sediments. J. Ocean. Limnol. 40, 1974–1984 (2022). https://doi.org/10.1007/s00343-021-1261-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00343-021-1261-0