{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,20]],"date-time":"2026-10-20T00:43:02Z","timestamp":1792456982216,"version":"4.5.0"},"reference-count":57,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2023,5,19]],"date-time":"2023-05-19T00:00:00Z","timestamp":1684454400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100007847","name":"Natural Science Foundation of Jilin Province of China","doi-asserted-by":"publisher","award":["20210101100JC"],"award-info":[{"award-number":["20210101100JC"]}],"id":[{"id":"10.13039\/100007847","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Microbiol."],"abstract":"<jats:p>Long-term fertilization can result in the changes in carbon (C) cycle in the maize rhizosphere soil. However, there have been few reports on the impacts of microbial regulatory mechanisms on the C cycle in soil. In the study, we analyzed the response of functional genes that regulate the C fixation, decomposition and methane (CH<jats:sub>4<\/jats:sub>) metabolism in maize rhizosphere soil to different fertilization treatments using metagenomics analysis. As the dominant C fixation pathway in maize rhizosphere soil, the abundance of the functional genes regulating the reductive citrate cycle (rTCA cycle) including <jats:italic>korA, korB,<\/jats:italic> and <jats:italic>IHD1<\/jats:italic> was higher under the chemical nitrogen (N) fertilizer treatments [nitrogen fertilizer (N), compound chemical fertilization (NPK), the combination of compound chemical fertilizer with maize straw (NPKS)] than maize straw return treatments [maize straw return (S), the combination of phosphorus and potassium fertilizer with maize straw (PKS)]. The NPK treatment decreased the abundance of functional genes involved in 3-hydroxypropionate bicycle (3-HP cycle; <jats:italic>porA<\/jats:italic>, <jats:italic>porB<\/jats:italic>, and <jats:italic>porD<\/jats:italic>), which was one of the major C fixation pathways in soil aside from dicarboxylate-hydroxybutyrate (DC\/4-HB cycle) and Calvin cycle. The abundance of functional genes related to C degradation was higher in S, PKS and NPKS treatments than N and NPK treatments, and chemical N fertilizer application had a significant effect on C degradation. The dominant Methanaogenesis pathway in maize rhizosphere soil, used acetate as a substrate, and was significantly promoted under chemical N fertilizer application. The functional genes that were related to CH<jats:sub>4<\/jats:sub> oxidation (i.e., <jats:italic>pmoA<\/jats:italic> and <jats:italic>pmoB<\/jats:italic>) were reduced under N and NPK treatments. Moreover, soil chemical properties had a significant impact on the functional genes related to C fixation and degradation, with SOC (r<jats:sup>2<\/jats:sup> =\u20090.79) and NO<jats:sub>3<\/jats:sub><jats:sup>\u2212<\/jats:sup>-N (r<jats:sup>2<\/jats:sup> =\u20090.63) being the main regulators. These results implied that N fertilization rather than maize straw return had a greater influence on the C cycle in maize rhizosphere soil.<\/jats:p>","DOI":"10.3389\/fmicb.2023.1170214","type":"journal-article","created":{"date-parts":[[2023,5,19]],"date-time":"2023-05-19T05:39:46Z","timestamp":1684474786000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":17,"title":["Metagenomics reveals the effect of long-term fertilization on carbon cycle in the maize rhizosphere"],"prefix":"10.3389","volume":"14","author":[{"given":"Yanan","family":"Li","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chengyu","family":"Wang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hongyan","family":"Chang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yumang","family":"Zhang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shuxia","family":"Liu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Wentian","family":"He","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2023,5,19]]},"reference":[{"key":"ref1","doi-asserted-by":"crossref","first-page":"325","DOI":"10.1007\/978-981-10-6863-8_16","article-title":"Microbial CO2 fixation bioprocesses and desert as future carbon sink","volume-title":"Optimization and applicability of bioprocesses","author":"Agarwal","year":"2017"},{"key":"ref2","doi-asserted-by":"publisher","first-page":"15025","DOI":"10.1038\/nmicrobiol.2015.25","article-title":"Altered carbon turnover processes and microbiomes in soils under long-term extremely high CO2 exposure","volume":"1","author":"Beulig","year":"2016","journal-title":"Nat. Microbiol."},{"key":"ref3","doi-asserted-by":"publisher","DOI":"10.1016\/j.iswcr.2022.07.004","article-title":"Magnitude, direction, and drivers of rhizosphere effect on soil nitrogen and phosphorus in global agroecosystem","author":"Cai","year":"2022","journal-title":"Int. Soil Water Conserv. Res."},{"key":"ref400","doi-asserted-by":"publisher","first-page":"692","DOI":"10.1038\/nrmicro.2016.130","article-title":"Harnessing the power of microbial autotrophy","volume":"14","author":"Claassens","year":"2016","journal-title":"Nat. Rev. Microbiol."},{"key":"ref4","doi-asserted-by":"publisher","first-page":"100362","DOI":"10.1016\/j.rhisph.2021.100362","article-title":"Changes in the diversity and predicted functional composition of the bulk and rhizosphere soil bacterial microbiomes of tomato and common bean after inorganic N-fertilization","volume":"18","author":"Castellano-Hinojosa","year":"2021","journal-title":"Rhizosphere"},{"key":"ref5","doi-asserted-by":"publisher","first-page":"1546","DOI":"10.1016\/j.jia.2022.12.011","article-title":"Inversion tillage with straw incorporation affects the patterns of soil microbial co-occurrence and multi-nutrient cycling in a Hapli-Udic Cambisol","volume":"22","author":"Chen","year":"2022","journal-title":"J. Integr. Agric."},{"key":"ref6","doi-asserted-by":"publisher","first-page":"110071","DOI":"10.1016\/j.ecolind.2023.110071","article-title":"Bulk soil microbial reservoir or plant recruitment dominates rhizosphere microbial community assembly: evidence from the rare, endangered Lauraceae species Cinmaomum migao","volume":"148","author":"Chen","year":"2023","journal-title":"Ecol. Indic."},{"key":"ref7","doi-asserted-by":"publisher","first-page":"162967","DOI":"10.1016\/j.scitotenv.2023.162967","article-title":"Presence of different microplastics promotes greenhouse gas emissions and alters the microbial community composition of farmland soil","volume":"879","author":"Chen","year":"2023","journal-title":"Sci. Total Environ."},{"key":"ref8","doi-asserted-by":"publisher","first-page":"247","DOI":"10.11766\/trxb201707090275","article-title":"Effects of straw returning and tillage system on crop yield and soil fertility quality in paddy field under double-cropping-rice system","volume":"55","author":"Cheng","year":"2018","journal-title":"Acta Pedol. Sin."},{"key":"ref9","doi-asserted-by":"publisher","first-page":"240","DOI":"10.3390\/f10030240","article-title":"Soil organic carbon chemical functional groups under different revegetation types are coupled with changes in the microbial community composition and the functional genes","volume":"10","author":"Deng","year":"2019","journal-title":"Forests"},{"key":"ref10","doi-asserted-by":"publisher","first-page":"24","DOI":"10.1186\/s13568-021-01182-z","article-title":"Soil fertilization affects the abundance and distribution of carbon and nitrogen cycling genes in the maize rhizosphere","volume":"11","author":"Enebe","year":"2021","journal-title":"AMB Express"},{"key":"ref11","doi-asserted-by":"publisher","first-page":"e01212","DOI":"10.1016\/j.sciaf.2022.e01212","article-title":"Functional diversity of bacterial communities in the rhizosphere of maize grown on a soil under organic and inorganic fertilization","volume":"16","author":"Enebe","year":"2022","journal-title":"Sci. Afr."},{"key":"ref12","doi-asserted-by":"publisher","first-page":"1775","DOI":"10.1016\/j.pss.2010.08.014","article-title":"The chemical biology of methanogenesis","volume":"58","author":"Ferry","year":"2010","journal-title":"Planet. Space Sci."},{"key":"ref13","doi-asserted-by":"publisher","DOI":"10.1016\/j.jia.2023.02.037","article-title":"Improvement of soil fertility and rice yield after long-term application of cow manure combined with inorganic fertilizers","author":"Gao","year":"2023","journal-title":"J. Integr. Agric."},{"key":"ref14","doi-asserted-by":"publisher","first-page":"170","DOI":"10.1016\/j.geoderma.2012.05.007","article-title":"The effect of chemical fertilizer application on carbon input and export in soil\u2014a pot experiment with wheat using natural 13C abundance method","author":"Gong","year":"2012","journal-title":"Geoderma"},{"key":"ref15","doi-asserted-by":"publisher","first-page":"115846","DOI":"10.1016\/j.geoderma.2022.115846","article-title":"Metagenomics reveals divergent functional profiles of soil carbon and nitrogen cycling under long-term addition of chemical and organic fertilizers in the black soil region","volume":"418","author":"Hu","year":"2022","journal-title":"Geoderma"},{"key":"ref16","doi-asserted-by":"publisher","first-page":"108764","DOI":"10.1016\/j.soilbio.2022.108764","article-title":"Metabolic pathways of CO2 fixing microorganisms determined C-fixation rates in grassland soils along the precipitation gradient","volume":"172","author":"Huang","year":"2022","journal-title":"Soil Biol. Biochem."},{"key":"ref17","doi-asserted-by":"publisher","first-page":"103926","DOI":"10.1016\/j.apsoil.2021.103926","article-title":"Soil labile organic carbon impacts C:N:P stoichiometry in urban park green spaces depending on vegetation types and time after planting","volume":"163","author":"Huang","year":"2021","journal-title":"Appl. Soil Ecol."},{"key":"ref18","doi-asserted-by":"publisher","first-page":"1617","DOI":"10.3389\/fpls.2017.01617","article-title":"The role of soil microorganisms in plant mineral nutrition-current knowledge and future directions","volume":"8","author":"Jacoby","year":"2017","journal-title":"Front. Plant Sci."},{"key":"ref19","doi-asserted-by":"publisher","first-page":"104250","DOI":"10.1016\/j.apsoil.2021.104250","article-title":"Long-term combined application of chemical fertilizers and organic manure shapes the gut microbial diversity and functional community structures of earthworms","volume":"170","author":"Jin","year":"2022","journal-title":"Appl. Soil Ecol."},{"key":"ref20","doi-asserted-by":"publisher","first-page":"3267","DOI":"10.1016\/j.soilbio.2006.04.006","article-title":"Variable use of plant- and soil-derived carbon by microorganisms in agricultural soils","volume":"38","author":"Kramer","year":"2006","journal-title":"Soil Biol. Biochem."},{"key":"ref21","doi-asserted-by":"publisher","first-page":"126901","DOI":"10.1016\/j.micres.2021.126901","article-title":"Rhizospheric microbiome: bio-based emerging strategies for sustainable agriculture development and future perspectives","volume":"254","author":"Kumawat","year":"2022","journal-title":"Microbiol. Res."},{"key":"ref22","doi-asserted-by":"publisher","first-page":"12","DOI":"10.1111\/j.1574-6941.2011.01192.x","article-title":"Soil characteristics more strongly influence soil bacterial communities than land-use type","volume":"1","author":"Kuramae","year":"2015","journal-title":"FEMS Microbiol. Ecol."},{"key":"ref23","doi-asserted-by":"publisher","first-page":"2407","DOI":"10.1016\/j.soilbio.2008.05.021","article-title":"The influence of soil properties on the structure of bacterial and fungal communities across land-use types","volume":"40","author":"Lauber","year":"2008","journal-title":"Soil Biol. Biochem."},{"key":"ref24","doi-asserted-by":"publisher","first-page":"48","DOI":"10.1186\/s40168-020-00964-0","article-title":"Mechanistic strategies of microbial communities regulating lignocellulose deconstruction in a UK salt marsh","volume":"9","author":"Leadbeater","year":"2021","journal-title":"Microbiome"},{"key":"ref25","doi-asserted-by":"publisher","first-page":"104296","DOI":"10.1016\/j.apsoil.2021.104296","article-title":"Rhizosphere effect alters the soil microbiome composition and C, N transformation in an arid ecosystem","volume":"170","author":"Li","year":"2022","journal-title":"Appl. Soil Ecol."},{"key":"ref26","doi-asserted-by":"publisher","first-page":"329","DOI":"10.3390\/land9090329","article-title":"Effects of different fertilizer treatments on rhizosphere soil microbiome composition and functions","volume":"9","author":"Li","year":"2020","journal-title":"Land"},{"key":"ref27","first-page":"2407","article-title":"Grain yield trends of different food crops under long-term fertilization in China","volume":"42","author":"Li","year":"2009","journal-title":"Sci. Agric. Sin."},{"key":"ref28","doi-asserted-by":"publisher","first-page":"18","DOI":"10.1016\/j.soilbio.2016.10.009","article-title":"Responses of soil microbial functional genes to global changes are indirectly influenced by aboveground plant biomass variation","volume":"104","author":"Li","year":"2017","journal-title":"Soil Biol. Biochem."},{"key":"ref29","doi-asserted-by":"publisher","first-page":"107403","DOI":"10.1016\/j.agee.2021.107403","article-title":"Effect of chemical fertilizer and straw-derived organic amendments on continuous maize yield, soil carbon sequestration and soil quality in a Chinese Mollisol","volume":"314","author":"Liang","year":"2021","journal-title":"Agric. Ecosyst. Environ."},{"key":"ref30","doi-asserted-by":"publisher","first-page":"164","DOI":"10.1016\/j.ibiod.2016.06.019","article-title":"Microbial communities responsible for fixation of CO2 revealed by using mcrA, cbbM, cbbL, fthfs, fefe-hydrogenase genes as molecular biomarkers in petroleum reservoirs of different temperatures","volume":"114","author":"Liu","year":"2016","journal-title":"Int. Biodeterior. Biodegradation"},{"key":"ref31","doi-asserted-by":"publisher","first-page":"156608","DOI":"10.1016\/j.scitotenv.2022.156608","article-title":"14 year applications of chemical fertilizers and crop straw effects on soil labile organic carbon fractions, enzyme activities and microbial community in rice-wheat rotation of middle China","volume":"841","author":"Liu","year":"2022","journal-title":"Sci. Total Environ."},{"key":"ref32","doi-asserted-by":"publisher","first-page":"4327","DOI":"10.13227\/j.hjkx.201711067","article-title":"Soil organic carbon of purple soil as affected by different application of biochar","volume":"39","author":"Luo","year":"2018","journal-title":"Environ. Sci."},{"key":"ref33","doi-asserted-by":"publisher","first-page":"107563","DOI":"10.1016\/j.agwat.2022.107563","article-title":"Physiological response, phytohormone signaling, biomass production and water use efficiency of the CAM plant Ananas comosus under different water and nitrogen regimes","volume":"266","author":"Ma","year":"2022","journal-title":"Agric. Water Manag."},{"key":"ref34","doi-asserted-by":"publisher","first-page":"114151","DOI":"10.1016\/j.jenvman.2021.114151","article-title":"Elucidation of dominant energy metabolic pathways of methane, Sulphur and nitrogen in respect to mangrove-degradation for climate change mitigation","volume":"303","author":"Padhy","year":"2022","journal-title":"J. Environ. Manag."},{"key":"ref35","doi-asserted-by":"publisher","first-page":"108248","DOI":"10.1016\/j.agee.2022.108248","article-title":"Soil organic carbon and nitrogen fractions as affected by straw and nitrogen management on the North China plain","volume":"342","author":"Ren","year":"2023","journal-title":"Agric. Ecosyst. Environ."},{"key":"ref36","doi-asserted-by":"publisher","first-page":"294","DOI":"10.1016\/j.soilbio.2019.05.018","article-title":"Stoichiometric controls of soil carbon and nitrogen cycling after long-term nitrogen and phosphorus addition in a Mesic grassland in South Africa","volume":"135","author":"Schleuss","year":"2019","journal-title":"Soil Biol. Biochem."},{"key":"ref37","doi-asserted-by":"publisher","first-page":"247","DOI":"10.1016\/j.agee.2009.04.021","article-title":"Review of greenhouse gas emissions from crop production systems and fertilizer management effects","volume":"133","author":"Snyder","year":"2009","journal-title":"Agric. Ecosyst. Environ."},{"key":"ref38","doi-asserted-by":"publisher","first-page":"109019","DOI":"10.1016\/j.soilbio.2023.109019","article-title":"Microbial community succession in soil is mainly driven by carbon and nitrogen contents rather than phosphorus and Sulphur contents","volume":"180","author":"Tang","year":"2023","journal-title":"Soil Biol. Biochem."},{"key":"ref39","doi-asserted-by":"publisher","first-page":"87","DOI":"10.1016\/j.soilbio.2018.05.014","article-title":"Nitrogen enrichment shifts functional genes related to nitrogen and carbon acquisition in the fungal community","volume":"123","author":"Treseder","year":"2018","journal-title":"Soil Biol. Biochem."},{"key":"ref40","doi-asserted-by":"publisher","first-page":"1643","DOI":"10.1007\/s10482-016-0764-8","article-title":"Liming in the sugarcane burnt system and the green harvest practice affect soil bacterial community in northeastern so Paulo, Brazil","volume":"109","author":"Val-Moraes","year":"2016","journal-title":"Antonie Van Leeuwenhoek"},{"key":"ref41","doi-asserted-by":"publisher","first-page":"1","DOI":"10.3390\/agriculture11111040","article-title":"Effect of plastic mulching on soil carbon and nitrogen cycling-related bacterial community structure and function in a dryland spring maize field","volume":"11","author":"Wang","year":"2021","journal-title":"Agriculture"},{"key":"ref42","doi-asserted-by":"publisher","first-page":"103992","DOI":"10.1016\/j.apsoil.2021.103992","article-title":"Responses of soil bacterial community and enzyme activity to organic matter components under long-term fertilization on the loess plateau of China","volume":"166","author":"Wang","year":"2021","journal-title":"Appl. Soil Ecol."},{"key":"ref43","doi-asserted-by":"publisher","first-page":"33","DOI":"10.1016\/j.ejsobi.2018.10.002","article-title":"Effects of nitrogen addition on soil organic carbon mineralization after maize stalk addition","volume":"89","author":"Wang","year":"2018","journal-title":"Eur. J. Soil Biol."},{"key":"ref44","first-page":"4004","article-title":"Effect of addition of several types of straws on N2O and CH4 emissions from soil under flooding condition in Hainan Province","volume":"37","author":"Wang Xiaoqi","year":"2017","journal-title":"Acta Sci. Circumst."},{"key":"ref45","doi-asserted-by":"publisher","first-page":"100264","DOI":"10.1016\/j.rhisph.2020.100264","article-title":"Application of bio-organic fertilizer, not biochar, in degraded red soil improves soil nutrients and plant growth","volume":"16","author":"Wu","year":"2020","journal-title":"Rhizosphere"},{"key":"ref46","doi-asserted-by":"publisher","first-page":"108305","DOI":"10.1016\/j.agee.2022.108305","article-title":"Diffusion and transformation of methane within the soil profile and surface uptake in dryland spring maize fields under different fertilizer application depths","volume":"344","author":"Wu","year":"2023","journal-title":"Agric. Ecosyst. Environ."},{"key":"ref47","doi-asserted-by":"publisher","first-page":"116393","DOI":"10.1016\/j.geoderma.2023.116393","article-title":"New insights into carbon mineralization in tropical paddy soil under land use conversion: coupled roles of soil microbial community, metabolism, and dissolved organic matter chemodiversity","volume":"432","author":"Wu","year":"2023","journal-title":"Geoderma"},{"key":"ref48","doi-asserted-by":"publisher","first-page":"759","DOI":"10.1016\/j.jbiosc.2012.01.007","article-title":"Effect of carbon source and COD\/NO3\u2212\u2013N ratio on anaerobic simultaneous denitrification and methanogenesis for high-strength wastewater treatment","volume":"113","author":"Xie","year":"2012","journal-title":"J. Biosci. Bioeng."},{"key":"ref49","doi-asserted-by":"publisher","first-page":"102009","DOI":"10.1016\/j.bcab.2021.102009","article-title":"Biodiversity, and biotechnological contribution of beneficial soil microbiomes for nutrient cycling, plant growth improvement and nutrient uptake","volume":"33","author":"Yadav","year":"2021","journal-title":"Biocatal. Agric. Biotechnol."},{"key":"ref50","doi-asserted-by":"publisher","first-page":"499","DOI":"10.1038\/s41559-017-0463-5","article-title":"Community proteogenomics reveals the systemic impact of phosphorus availability on microbial functions in tropical soil","volume":"2","author":"Yao","year":"2018","journal-title":"Nat. Eco. Evol."},{"key":"ref51","doi-asserted-by":"publisher","first-page":"109790","DOI":"10.1016\/j.ecolind.2022.109790","article-title":"Effects of decadal nitrogen and phosphorus fertilization on microbial taxonomic and functional attributes associated with soil organic carbon decomposition and concentration in an alpine meadow","volume":"146","author":"Ye","year":"2023","journal-title":"Ecol. Indic."},{"key":"ref52","doi-asserted-by":"publisher","first-page":"770","DOI":"10.1016\/j.scitotenv.2018.01.233","article-title":"Effects of different fertilizers on methane emissions and methanogenic community structures in paddy rhizosphere soil","volume":"627","author":"Yuan","year":"2018","journal-title":"Sci. Total Environ."},{"key":"ref53","doi-asserted-by":"publisher","DOI":"10.1016\/j.jia.2022.09.025","article-title":"The effects of co-utilizing green manure and rice straw on soil aggregates and soil carbon stability in a paddy soil in South China","author":"Zhang","year":"2022","journal-title":"J. Integr. Agric."},{"key":"ref54","doi-asserted-by":"publisher","first-page":"105342","DOI":"10.1016\/j.catena.2021.105342","article-title":"Long-term manure application enhances the stability of aggregates and aggregate-associated carbon by regulating soil physicochemical characteristics","volume":"203","author":"Zhang","year":"2021","journal-title":"Catena"},{"key":"ref55","first-page":"317","article-title":"Research progress of SOC function and transformation mechanisms","volume":"53","author":"Zhang","year":"2020","journal-title":"Sci. Agric. Sin."},{"key":"ref56","doi-asserted-by":"publisher","first-page":"103116","DOI":"10.1016\/j.ejsobi.2019.103116","article-title":"Effects of reduced inorganic fertilization and rice straw recovery on soil enzyme activities and bacterial community in double-rice paddy soils","volume":"94","author":"Zhu","year":"2019","journal-title":"Eur. J. Soil Biol."}],"container-title":["Frontiers in Microbiology"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fmicb.2023.1170214\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,5,19]],"date-time":"2023-05-19T05:39:56Z","timestamp":1684474796000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fmicb.2023.1170214\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,5,19]]},"references-count":57,"alternative-id":["10.3389\/fmicb.2023.1170214"],"URL":"https:\/\/doi.org\/10.3389\/fmicb.2023.1170214","relation":{},"ISSN":["1664-302X"],"issn-type":[{"value":"1664-302X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,5,19]]},"article-number":"1170214"}}