{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,3]],"date-time":"2026-08-03T23:03:00Z","timestamp":1785798180616,"version":"3.56.0"},"reference-count":58,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2024,7,10]],"date-time":"2024-07-10T00:00:00Z","timestamp":1720569600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Microbiol."],"abstract":"<jats:p>Soil copper (Cu) pollution is a serious environmental risk in the <jats:italic>Panax notoginseng<\/jats:italic> planting area. However, the effect of Cu on soil microbial metabolism and nutrient cycling in this area remains unknown. Therefore, Biolog ECO-plate and enzyme stoichiometry methods were utilized in this study to investigate the impact of exogenous Cu (control: 0 mg\u00b7kg<jats:sup>\u22121<\/jats:sup>; Cu100: 100 mg\u00b7kg<jats:sup>\u22121<\/jats:sup>; Cu400: 400 mg\u00b7kg<jats:sup>\u22121<\/jats:sup>; and Cu600: 600 mg\u00b7kg<jats:sup>\u22121<\/jats:sup>) on the metabolic function of soil microbial and nutrient limitation in the <jats:italic>P. notoginseng<\/jats:italic> soil. The results indicated that Cu100 significantly increased soil organic carbon (SOC), total phosphorus (TP), soil C:N, microbial biomass carbon (MBC), and microbial biomass nitrogen (MBN) 9.89%, 15.65%, 17.91%, 61.87%, and 90.56% higher than the control, respectively. Moreover, the carbon source utilization ratio of carbohydrates, amino acids, and amphiphilic compounds of Cu100 also increased by 7.16%, 25.47%, and 84.68%, respectively, compared with the control. The activities of \u03b2-1,4-glucosidase, cellobiohyrolase, leucine amino peptidase, \u03b2-1,4-N-acetylglucosaminidase, and phosphatase significantly decreased with increasing Cu concentration. Soil enzyme stoichiometry showed that all treatments were limited by nitrogen (vector angle &amp;lt; 45\u00b0; 19.045\u201322.081). Cu600 led to the lowest carbon limitation (1.798) and highest carbon use efficiency (CUE:0.267). The PLS-SEM model also showed that MBC, MBN, MBP, and microbial diversity positively affected carbon and nitrogen limitation (0.654 and 0.424). Soil carbon, nitrogen, phosphorus, stoichiometric ratio, MBC, MBN, and MBP positively affected CUE (0.527 and 0.589). The microbial diversity index significantly negatively affected CUE (\u22121.490). Multiple linear stepwise regression analyses showed that CUE was mainly influenced by MBC, AP, C:P, and LAP. Thus, <jats:italic>P. notoginseng<\/jats:italic> soil can benefit soil microbial carbon and nitrogen limitations at low Cu concentrations. Clarifying the metabolic activity and nutritional status of microorganisms under Cu stress can provide some theoretical basis for realizing China's comprehensive and effective management and control policies for environmental risks from metals by 2035.<\/jats:p>","DOI":"10.3389\/fmicb.2024.1390921","type":"journal-article","created":{"date-parts":[[2024,7,10]],"date-time":"2024-07-10T05:08:50Z","timestamp":1720588130000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":4,"title":["Effects of exogenous copper on microbial metabolic function and carbon use efficiency of Panax notoginseng planting soil"],"prefix":"10.3389","volume":"15","author":[{"given":"Tong","family":"Wang","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xu","family":"Wang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tarik","family":"Hadibi","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xun","family":"Ma","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Haoyi","family":"Yao","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zhenya","family":"Tang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Fangling","family":"Fan","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yizong","family":"Huang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2024,7,10]]},"reference":[{"key":"B1","doi-asserted-by":"crossref","first-page":"229","DOI":"10.1007\/978-3-642-14225-3_12","article-title":"\u201cEvolutionary-economic principles as regulators of soil enzyme production and ecosystem function,\u201d","volume-title":"Soil Enzymology","author":"Allison","year":"2010"},{"key":"B2","doi-asserted-by":"publisher","first-page":"82","DOI":"10.1016\/j.scitotenv.2013.03.061","article-title":"Soil management of copper mine tailing soils\u2013sludge amendment and tree vegetation could improve biological soil quality","volume":"457","author":"Asensio","year":"2013","journal-title":"Sci. Total Environ."},{"key":"B3","doi-asserted-by":"publisher","first-page":"e50961","DOI":"10.3791\/50961-v","article-title":"High-throughput fluorometric measurement of potential soil extracellular enzyme activities","volume":"81","author":"Bell","year":"2013","journal-title":"J. Vis. Exp."},{"key":"B4","doi-asserted-by":"publisher","first-page":"115","DOI":"10.1007\/s00374-008-0334-y","article-title":"Mechanisms of real and apparent priming effects and their dependence on soil microbial biomass and community structure: critical review","volume":"45","author":"Blagodatskaya","year":"2008","journal-title":"Biol. Fertil. Soils"},{"key":"B5","doi-asserted-by":"publisher","first-page":"216","DOI":"10.1016\/j.soilbio.2012.11.009","article-title":"Soil enzymes in a changing environment: current knowledge and future directions","volume":"58","author":"Burns","year":"2013","journal-title":"Soil Biol. Biochem."},{"key":"B6","doi-asserted-by":"publisher","first-page":"103033","DOI":"10.1016\/j.earscirev.2019.103033","article-title":"Nitrogen deposition differentially affects soil gross nitrogen transformations in organic and mineral horizons","volume":"201","author":"Cheng","year":"2019","journal-title":"Earth-Sci. Rev."},{"key":"B7","doi-asserted-by":"publisher","first-page":"235","DOI":"10.1007\/s10533-007-9132-0","article-title":"C:N:P stoichiometry in soil: is there a \u201cRedfield ratio\u201d for the microbial biomass?","volume":"85","author":"Cleveland","year":"2007","journal-title":"Biogeochemistry"},{"key":"B8","doi-asserted-by":"publisher","first-page":"273","DOI":"10.1007\/s10705-020-10076-8","article-title":"Microorganisms and nutrient stoichiometry as mediators of soil organic matter dynamics","volume":"117","author":"Coonan","year":"2020","journal-title":"Nutr. Cycling Agroecosyst."},{"key":"B9","doi-asserted-by":"publisher","first-page":"988","DOI":"10.1111\/gcb.12113","article-title":"The microbial efficiency-matrix stabilization (MEMS) framework integrates plant litter decomposition with soil organic matter stabilization: do labile plant inputs form stable soil organic matter?","volume":"19","author":"Cotrufo","year":"2013","journal-title":"Glob. Chang. Biol."},{"key":"B10","doi-asserted-by":"publisher","first-page":"188","DOI":"10.1016\/j.geoderma.2019.06.037","article-title":"Drivers of soil microbial metabolic limitation changes along a vegetation restoration gradient on the Loess Plateau, China","volume":"353","author":"Deng","year":"2019","journal-title":"Geoderma"},{"key":"B11","doi-asserted-by":"publisher","first-page":"3684","DOI":"10.1038\/s41467-020-17502-z","article-title":"Microbial diversity drives carbon use efficiency in a model soil","volume":"11","author":"Domeignoz-Horta","year":"2020","journal-title":"Nat. Commun."},{"key":"B12","doi-asserted-by":"publisher","first-page":"118978","DOI":"10.1016\/j.envpol.2022.118978","article-title":"Microbial metabolic limitation of rhizosphere under heavy metal stress: evidence from soil ecoenzymatic stoichiometry","volume":"300","author":"Duan","year":"2022","journal-title":"Environ. Pollut."},{"key":"B13","doi-asserted-by":"publisher","first-page":"59","DOI":"10.1016\/j.catena.2015.07.006","article-title":"Spatial distribution and environmental factors of catchment-scale soil heavy metal contamination in the dry-hot valley of Upper Red River in southwestern China","volume":"135","author":"Duan","year":"2015","journal-title":"Catena"},{"key":"B14","doi-asserted-by":"publisher","first-page":"213","DOI":"10.1016\/0038-0717(95)00112-3","article-title":"Analytical approaches to the characterization of samples of microbial communities using patterns of potential C source utilization","volume":"28","author":"Garland","year":"1996","journal-title":"Soil Biol. Biochem."},{"key":"B15","volume-title":"Soil Environmental Quality: Risk Control Standard for Soil Contamination of Agricultural Land.","year":"2018"},{"key":"B16","doi-asserted-by":"publisher","first-page":"147","DOI":"10.1016\/S0065-2113(08)60308-9","article-title":"Copper in nutrition","volume":"4","author":"Gilbert","year":"1952","journal-title":"Adv. Agron."},{"key":"B17","doi-asserted-by":"publisher","first-page":"771","DOI":"10.1016\/j.ecoenv.2019.01.016","article-title":"Effects of copper on the growth, antioxidant enzymes and photosynthesis of spinach seedlings","volume":"171","author":"Gong","year":"2019","journal-title":"Ecotoxicol. Environ. Saf."},{"key":"B18","doi-asserted-by":"publisher","first-page":"249","DOI":"10.1007\/s00374-005-0830-2","article-title":"Organic matter accumulation and fertilizer-induced acidification interact to affect soil microbial and enzyme activity on a long-term sugarcane management experiment","volume":"41","author":"Graham","year":"2005","journal-title":"Biol. Fertil. Soils"},{"key":"B19","doi-asserted-by":"publisher","first-page":"977","DOI":"10.1038\/s41564-018-0201-z","article-title":"Understanding how microbiomes influence the systems they inhabit","volume":"3","author":"Hall","year":"2018","journal-title":"Nat. Microbiol."},{"key":"B20","doi-asserted-by":"publisher","first-page":"304","DOI":"10.1016\/S1360-1385(00)01656-3","article-title":"Are microorganisms more effective than plants at competing for nitrogen?","volume":"5","author":"Hodge","year":"2000","journal-title":"Trends Plant Sci."},{"key":"B21","doi-asserted-by":"publisher","first-page":"9029","DOI":"10.1007\/s10653-022-01392-9","article-title":"Characteristics of heavy metal accumulation and risk assessment in understory Panax notoginseng planting system","volume":"45","author":"Huang","year":"2023","journal-title":"Environ. Geochem. Health"},{"key":"B22","doi-asserted-by":"publisher","first-page":"2013","DOI":"10.1007\/s10311-020-01155-x","article-title":"Ecotoxicity of copper input and accumulation for soil biodiversity in vineyards","volume":"19","author":"Karimi","year":"2021","journal-title":"Environ. Chem. Lett."},{"key":"B23","doi-asserted-by":"publisher","first-page":"118978","DOI":"10.2136\/sssaj2001.1751","article-title":"A simple soil test for detecting sites that are nonresponsive to nitrogen fertilization","volume":"65","author":"Khan","year":"2001","journal-title":"Soil Sci. Soc. Am. J."},{"key":"B24","doi-asserted-by":"publisher","first-page":"33","DOI":"10.1007\/s10533-013-9892-7","article-title":"Nitrogen, organic carbon and sulphur cycling in terrestrial ecosystems: linking nitrogen saturation to carbon limitation of soil microbial processes","volume":"115","author":"Kop\u00e1\u010dek","year":"2013","journal-title":"Biogeochemistry"},{"key":"B25","doi-asserted-by":"publisher","first-page":"974","DOI":"10.1016\/S1002-0160(17)60404-1","article-title":"Impact of land-use change on soil microbial community composition and organic carbon content in the dry tropics of India","volume":"27","author":"Kumar","year":"2017","journal-title":"Pedosphere"},{"key":"B26","doi-asserted-by":"publisher","first-page":"371","DOI":"10.1890\/06-2057.1","article-title":"Nitrogen limitation of net primary productivity in terrestrial ecosystems is globally distributed","volume":"89","author":"Lebauer","year":"2008","journal-title":"Ecology"},{"key":"B27","doi-asserted-by":"publisher","first-page":"843","DOI":"10.1016\/j.scitotenv.2013.08.090","article-title":"A review of soil heavy metal pollution from mines in China: pollution and health risk assessment","volume":"469","author":"Li","year":"2014","journal-title":"Sci. Total Environ."},{"key":"B28","doi-asserted-by":"publisher","first-page":"3591","DOI":"10.1038\/s41467-018-05980-1","article-title":"Land use driven change in soil pH affects microbial carbon cycling processes","volume":"9","author":"Malik","year":"2018","journal-title":"Nat. Commun."},{"key":"B29","doi-asserted-by":"publisher","first-page":"79","DOI":"10.1111\/j.1469-8137.2012.04225.x","article-title":"Environmental and stoichiometric controls on microbial carbon-use efficiency in soils","volume":"196","author":"Manzoni","year":"2012","journal-title":"New Phytol."},{"key":"B30","doi-asserted-by":"publisher","first-page":"148","DOI":"10.1007\/s00248-018-1206-0","article-title":"Determinants of soil bacterial and fungal community composition toward carbon-use efficiency across primary and secondary forests in a Costa Rican conservation area","volume":"77","author":"McGee","year":"2019","journal-title":"Microb. Ecol."},{"key":"B31","doi-asserted-by":"publisher","first-page":"737","DOI":"10.1007\/s10534-021-00306-z","article-title":"Copper: uptake, toxicity and tolerance in plants and management of Cu-contaminated soil","volume":"34","author":"Mir","year":"2021","journal-title":"Biometals"},{"key":"B32","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/j.soilbio.2015.10.019","article-title":"Vector analysis of ecoenzyme activities reveal constraints on coupled C, N and P dynamics","volume":"93","author":"Moorhead","year":"2015","journal-title":"Soil Biol. Biochem."},{"key":"B33","doi-asserted-by":"publisher","first-page":"e1602781","DOI":"10.1126\/sciadv.1602781","article-title":"Decoupling of microbial carbon, nitrogen, and phosphorus cycling in response to extreme temperature events","volume":"3","author":"Mooshammer","year":"2017","journal-title":"Sci. Adv."},{"key":"B34","volume-title":"Estimation of Available Phosphorus in Soils by Extraction with Sodium Bicarbonate.","author":"Olsen","year":"1954"},{"key":"B35","doi-asserted-by":"publisher","first-page":"1089","DOI":"10.3390\/ijerph13111089","article-title":"Soil-plant metal relations in Panax notoginseng: an ecosystem health risk assessment","volume":"13","author":"Ou","year":"2016","journal-title":"Int. J. Environ. Res. Public Health"},{"key":"B36","doi-asserted-by":"publisher","first-page":"151632","DOI":"10.1016\/j.scitotenv.2021.151632","article-title":"Soil heavy metal pollution of industrial legacies in China and health risk assessment","volume":"816","author":"Peng","year":"2022","journal-title":"Sci. Total Environ."},{"key":"B37","doi-asserted-by":"publisher","first-page":"226","DOI":"10.1038\/s41579-023-00980-5","article-title":"The interplay between microbial communities and soil properties","volume":"22","author":"Philippot","year":"2023","journal-title":"Nat. Rev. Microbiol."},{"key":"B38","doi-asserted-by":"publisher","first-page":"119406","DOI":"10.1016\/j.envpol.2022.119406","article-title":"Contamination with multiple heavy metals decreases microbial diversity and favors generalists as the keystones in microbial occurrence networks","volume":"306","author":"Qi","year":"2022","journal-title":"Environ. Pollut."},{"key":"B39","doi-asserted-by":"publisher","first-page":"36","DOI":"10.1016\/j.apsoil.2016.02.004","article-title":"Temperature effects on soil organic carbon, soil labile organic carbon fractions, and soil enzyme activities under long-term fertilization regimes","volume":"102","author":"Qi","year":"2016","journal-title":"Appl. Soil Ecol."},{"key":"B40","doi-asserted-by":"publisher","first-page":"121","DOI":"10.1038\/s43705-023-00331-8","article-title":"Exploring the competitive dynamic enzyme allocation scheme through enzyme cost minimization","volume":"3","author":"Qi","year":"2023","journal-title":"ISME Commun."},{"key":"B41","unstructured":"RaymentG. E.\n            HigginsonF. R.\n          Australian Laboratory Handbook of Soil and waTer Chemical Methods.1992"},{"key":"B42","doi-asserted-by":"publisher","first-page":"172","DOI":"10.1890\/15-2110.1","article-title":"Stoichiometry of microbial carbon use efficiency in soils","volume":"86","author":"Sinsabaugh","year":"2016","journal-title":"Ecol. Monogr."},{"key":"B43","doi-asserted-by":"publisher","first-page":"795","DOI":"10.1038\/nature08632","article-title":"Ecoenzymatic stoichiometry of microbial organic nutrient acquisition in soil and sediment","volume":"462","author":"Sinsabaugh","year":"2009","journal-title":"Nature"},{"key":"B44","doi-asserted-by":"publisher","first-page":"930","DOI":"10.1111\/ele.12113","article-title":"Carbon use efficiency of microbial communities: stoichiometry, methodology and modelling","volume":"16","author":"Sinsabaugh","year":"2013","journal-title":"Ecol. Lett."},{"key":"B45","doi-asserted-by":"publisher","first-page":"195","DOI":"10.1016\/j.soilbio.2019.01.010","article-title":"Microbial growth and carbon use efficiency in soil: links to fungal-bacterial dominance, SOC-quality and stoichiometry","volume":"131","author":"Soares","year":"2019","journal-title":"Soil Biol. Biochem."},{"key":"B46","doi-asserted-by":"publisher","first-page":"319","DOI":"10.18311\/jmmf\/2017\/27012","article-title":"Heavy metals pollution in iron tailing soil and its effects on microbial communities metabolism and enzyme activities","volume":"65","author":"Song","year":"2017","journal-title":"J. Mines Metals Fuels"},{"key":"B47","doi-asserted-by":"publisher","first-page":"130666","DOI":"10.1016\/j.jhazmat.2022.130666","article-title":"Metagenomic study of carbon metabolism in black soil microbial communities under lead-lanthanum stress","volume":"446","author":"Tao","year":"2022","journal-title":"J. Hazard. Mater."},{"key":"B48","doi-asserted-by":"publisher","first-page":"363","DOI":"10.1016\/S1002-0160(08)60026-0","article-title":"Tolerance of grasses to heavy metals and microbial functional diversity in soils contaminated with copper mine tailings1","volume":"18","author":"Teng","year":"2008","journal-title":"Pedosphere"},{"key":"B49","doi-asserted-by":"publisher","first-page":"703","DOI":"10.1016\/0038-0717(87)90052-6","article-title":"An extraction method for measuring soil microbial biomass c","volume":"19","author":"Vance","year":"1987","journal-title":"Soil Biol. Biochem."},{"key":"B50","doi-asserted-by":"publisher","first-page":"109058","DOI":"10.1016\/j.soilbio.2023.109058","article-title":"Heavy metal contamination collapses trophic interactions in the soil microbial food web via bottom-up regulation","volume":"184","author":"Wang","year":"2023","journal-title":"Soil Biol. Biochem."},{"key":"B51","doi-asserted-by":"publisher","first-page":"101","DOI":"10.1007\/s10533-013-9849-x","article-title":"Ecoenzymatic stoichiometry of microbial nutrient acquisition in tropical soils","volume":"117","author":"Waring","year":"2014","journal-title":"Biogeochemistry"},{"key":"B52","doi-asserted-by":"publisher","first-page":"219","DOI":"10.1016\/j.eehl.2022.10.004","article-title":"Heavy metals in agricultural soil in China: a systematic review and meta-analysis","volume":"1","author":"Wen","year":"2022","journal-title":"Eco Environ. Health"},{"key":"B53","doi-asserted-by":"publisher","first-page":"106261","DOI":"10.1016\/j.resconrec.2022.106261","article-title":"Review of soil heavy metal pollution in China: spatial distribution, primary sources, and remediation alternatives","volume":"181","author":"Wu","year":"2022","journal-title":"Resour. Conserv. Recycl."},{"key":"B54","doi-asserted-by":"publisher","first-page":"230","DOI":"10.1007\/s42832-021-0094-2","article-title":"Heavy metal pollution increases soil microbial carbon limitation: evidence from ecological enzyme stoichiometry","volume":"3","author":"Xu","year":"2021","journal-title":"Soil Ecol. Lett."},{"key":"B55","first-page":"317","article-title":"The Cu, Pb, Cd, and Zn Content and pollution evaluation of Panax notoginseng cultivated soil in Wenshan","volume":"31","author":"Zeng","year":"2009","journal-title":"Chin. Tradit. Patent Med."},{"key":"B56","doi-asserted-by":"publisher","first-page":"13205","DOI":"10.1038\/s41598-019-49625-9","article-title":"Impact of continuous Panax notoginseng plantation on soil microbial and biochemical properties","volume":"9","author":"Zhang","year":"2019","journal-title":"Sci. Rep."},{"key":"B57","doi-asserted-by":"publisher","first-page":"513","DOI":"10.1007\/s12665-023-11204-7","article-title":"Risk assessment of soil heavy metals in mining activity areas: a case study in Eastern Shandong Province, China","volume":"82","author":"Zhao","year":"2023","journal-title":"Environ. Earth Sci."},{"key":"B58","doi-asserted-by":"publisher","first-page":"317","DOI":"10.11934\/j.issn.1673-4831.2017.04.004","article-title":"Distribution of Pb, Cd, Cu and Zn in plant of Panax notoginseng and soil in Wenshan prefecture, a Panax notoginseng-growing region","volume":"33","author":"Zu","year":"2017","journal-title":"J. Ecol. Rural Environ."}],"container-title":["Frontiers in Microbiology"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fmicb.2024.1390921\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,7,10]],"date-time":"2024-07-10T05:08:58Z","timestamp":1720588138000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fmicb.2024.1390921\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,7,10]]},"references-count":58,"alternative-id":["10.3389\/fmicb.2024.1390921"],"URL":"https:\/\/doi.org\/10.3389\/fmicb.2024.1390921","relation":{},"ISSN":["1664-302X"],"issn-type":[{"value":"1664-302X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,7,10]]},"article-number":"1390921"}}