Abstract
Low nocturnal temperature (LNT) is a primary limitation in the greenhouse cultivation of vegetables during winter and spring, because it limits the availability of soil phosphorus (P), causing P-deficient symptoms. However, how LNT affects the P-cycling-related bacterial community composition and the turnover of soil P fractions is unknown. To address this issue, a 40-day indoor incubation experiment was used to investigate the effects of four nocturnal temperatures (15 °C, 12 °C, 9 °C, and 6 °C) on soil P fractions, alkaline phosphomonoesterase (ALP) activity, and the absolute abundance and composition of phoD- and pqqC-harboring microbial community. The low temperature decreased labile inorganic P (LPi) and increased labile organic P (LPo) and moderately labile Pi and Po (MLPi, MLPo). Low temperature decreased phoD and pqqC gene absolute abundance while increasing pqqC-harboring bacterial richness. The classes Actinobacteria, Alphaproteobacteria, and Betaproteobacteria dominated the phoD- and pqqC-harboring taxa in response to low temperature, despite low temperature, which decreased the absolute abundance of the phoD gene, potentially decreasing NaHCO3-Po and NaOH-Po mineralization. Moreover, low temperature influenced pqqC gene absolute abundance and pqqC-harboring bacterial community composition, likely decreasing NaOH-Pi solubilization. However, the soil LP and MLP fractions were only significantly correlated by pqqC gene absolute abundance and pqqC-harboring community composition.
Similar content being viewed by others
Data availability
The data presented in this study are available on request from the corresponding author.
References
Anzuay MS, Frola O, Angelini JG, Ludueña LM, Ibañez F, Fabra A, Taurian T (2015) Effect of pesticides application on peanut (Arachis hypogaea L.) associated phosphate solubilizing soil bacteria. Appl Soil Ecol 95:31–37. https://doi.org/10.1016/j.apsoil.2015.05.003
Bárcenas-Moreno G, Brandón MG, Rousk J, Bååth E (2009) Adaptation of soil microbial communities to temperature: comparison of fungi and bacteria in a laboratory experiment. Glob Change Biol 15:2950–2957. https://doi.org/10.1111/j.1365-2486.2009.01882.x
Beirinckx S, Viaene T, Haegeman A, Debode J, Amery F, Vandenabeele S, Nelissen H, Inzé D, Tito R, Raes J, de Tender C, Goormachtig S (2020) Tapping into the maize root microbiome to identify bacteria that promote growth under chilling conditions. Microbiome 8:1–13. https://doi.org/10.1186/s40168-020-00833-w
Bi QF, Li KJ, Zheng BX, Liu XP, Li HZ, Jin BJ, Ding K, Yang XR, Lin XY, Zhu YG (2020) Partial replacement of inorganic phosphorus (P) by organic manure reshapes phosphate mobilizing bacterial community and promotes P bioavailability in a paddy soil. Sci Total Environ 703:134977. https://doi.org/10.1016/j.scitotenv.2019.134977
Blagodatskaya E, Kuzyakov Y (2013) Active microorganisms in soil: critical review of estimation criteria and approaches. Soil Biol Biochem 67:192–211. https://doi.org/10.1016/j.soilbio.2013.08.024
Brookes PC, Powlson DS, Jenkinson DS (1982) Measurement of microbial biomass phosphorus in soil. Soil Biol Biochem 14:319–329. https://doi.org/10.1016/0038-0717(82)90001-3
Bünemann EK (2015) Assessment of gross and net mineralization rates of soil organic phosphorus - a review. Soil Biol Biochem 89:82–98. https://doi.org/10.1016/j.soilbio.2015.06.026
Čapek P, Kotas P, Manzoni S, Šantrůčková H (2016) Drivers of phosphorus limitation across soil microbial communities. Funct Ecol 30:1705–1713. https://doi.org/10.1111/1365-2435.12650
Chassé AW, Ohno T (2016) Higher molecular mass organic matter molecules compete with orthophosphate for adsorption to iron (oxy)hydroxide. Environ Sci Technol 50:7461–7469. https://doi.org/10.1021/acs.est.6b01582
Chen X, Jiang N, Chen Z, Tian J, Sun N, Xu M, Chen L (2017) Response of soil phoD phosphatase gene to long-term combined applications of chemical fertilizers and organic materials. Appl Soil Ecol 119:197–204. https://doi.org/10.1016/j.apsoil.2017.06.019
Chen X, Jiang N, Condron LM, Dunfield KE, Chen Z, Wang J, Chen L (2019) Impact of long-term phosphorus fertilizer inputs on bacterial phoD gene community in a maize field, Northeast China. Sci Total Environ 669:1011–1018. https://doi.org/10.1016/j.scitotenv.2019.03.172
Cross AF, Schlesinger WH (1995) A literature review and evaluation of the. Hedley fractionation: applications to the biogeochemical cycle of soil phosphorus in natural ecosystems. Geoderma 64:197–214. https://doi.org/10.1016/0016-7061(94)00023-4
Dalias P, Anderson JM, Bottner P, Coûteaux MM (2001) Long-term effects of temperature on carbon mineralisation processes. Soil Biol Biochem 28:3974–3990. https://doi.org/10.1016/S0038-0717(01)00009-8
Dawson CJ, Hilton J (2011) Fertiliser availability in a resource-limited world: production and recycling of nitrogen and phosphorus. Food Policy 36:S14–S22. https://doi.org/10.1016/j.foodpol.2010.11.012
de Sena A, Madramootoo CA, Whalen JK, von Sperber C (2022) Nucleic acids are a major pool of hydrolyzable organic phosphorus in arable organic soils of Southern Ontario, Canada. Biol Fertil Soils 58:7–16. https://doi.org/10.1007/s00374-021-01603-y
Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10:996–998. https://doi.org/10.1038/nmeth.2604
Feng J, Wang C, Lei J, Yang Y, Yan Q, Zhou X, Tao X, Ning D, Yuan MM, Qin Y, Shi ZJ, Guo X, He Z, van Nostrand JD, Wu L, Bracho-Garillo RG, Penton CR, Cole JR, Konstantinidis KT, Luo Y, Schuur EAG, Tiedje JM, Zhou J (2020) Warming-induced permafrost thaw exacerbates tundra soil carbon decomposition mediated by microbial community. Microbiome 8:3. https://doi.org/10.1186/s40168-019-0778-3
Fraser TD, Lynch DH, Bent E, Entz MH, Dunfield KE (2015) Soil bacterial phoD gene abundance and expression in response to applied phosphorus and long-term management. Soil Biol Biochem 88:137–147. https://doi.org/10.1016/j.soilbio.2015.04.014
Fu Z, Wu F, Song K, Lin Y, Bai Y, Zhu Y, Giesy JP (2013) Competitive interaction between soil-derived humic acid and phosphate on goethite. Appl Geochem 36:125–131. https://doi.org/10.1016/j.apgeochem.2013.05.015
Gao Y, Tariq A, Zeng F, Graciano C, Zhang Z, Sardans J, Peñuelas J (2022) Allocation of foliar-P fractions of Alhagi sparsifolia and its relationship with soil-P fractions and soil properties in a hyperarid desert ecosystem. Geoderma 407:115546. https://doi.org/10.1016/j.geoderma.2021.115546
Hedley MJ, Stewart JWB, Chauhan BS (1982) Changes in inorganic and organic soil phosphorus fractions induced by cultivation practices and by laboratory incubations. Soil Sci Soc Am J 46:970–976. https://doi.org/10.2136/sssaj1982.03615995004600050017x
Helfenstein J, Tamburini F, von Sperber C, Massey MS, Pistocchi C, Chadwick OA, Vitousek PM, Kretzschmar R, Frossard E (2018) Combining spectroscopic and isotopic techniques gives a dynamic view of phosphorus cycling in soil. Nat Commun 9:3226–3234. https://doi.org/10.1038/s41467-018-05731-2
Hu Y, Xia Y, Sun Q, Liu K, Chen X, Ge T, Zhu B, Zhu Z, Zhang Z, Su Y (2018) Effects of long-term fertilization on phoD-harboring bacterial community in Karst soils. Sci Total Environ 628–629:53–63. https://doi.org/10.1016/j.scitotenv.2018.01.314
Itoh S (2002) Application of mechanistic model for phosphorus uptake by barley under low temperature conditions. Soil Sci Plant Nutr 48:441–445. https://doi.org/10.1080/00380768.2002.10409223
IUSS Working Group WRB (2015) World Reference Base for Soil Resources 2014 (Update 2015). International soil classification system for naming soils and creating legends for soil maps. World Soil Resources Reports No. 106, FAO, Rome. https://doi.org/10.1017/S0014479706394902
Jiang N, Wei K, Pu J, Huang W, Bao H, Chen L (2021) A balanced reduction in mineral fertilizers benefits P reserve and inorganic P-solubilizing bacterial communities under residue input. Appl Soil Ecol 159:103833. https://doi.org/10.1016/j.apsoil.2020.103833
Jonasson S, Castro J, Michelsen A (2004) Litter, warming and plants affect respiration and allocation of soil microbial and plant C, N and P in arctic mesocosms. Soil Biol Biochem 36:1129–1139. https://doi.org/10.1016/j.soilbio.2004.02.023
Khan MS, Zaidi A, Ahmad E (2014) Mechanism of phosphate solubilization and physiological functions of phosphate-solubilizing microorganisms. In: Khan MS, Zaidi A, Musarrat J (eds) Phosphate solubilizing microorganisms: principles and application of microphos technology. Springer Cham, Berlin, pp 31–62. https://doi.org/10.1007/978-3-319-08216-5_2
Kong M, Han T, Chen M, Zhao D, Chao J, Zhang Y (2021) High mobilization of phosphorus in black-odor river sediments with the increase of temperature. Sci Total Environ 775:145595. https://doi.org/10.1016/j.scitotenv.2021.145595
Long XE, Yao H, Huang Y, Wei W, Zhu YG (2018) Phosphate levels influence the utilisation of rice rhizodeposition carbon and the phosphate-solubilising microbial community in a paddy soil. Soil Biol Biochem 118:103–114. https://doi.org/10.1016/j.soilbio.2017.12.014
Lu J, Wang Z, Yang X, Wang F, Qi M, Li T, Liu Y (2020) Cyclic electron flow protects photosystem I donor side under low night temperature in tomato. Environ Exp Bot 177:104151. https://doi.org/10.1016/j.envexpbot.2020.104151
Maougal RT, Brauman A, Plassard C, Abadie J, Djekoun A, Drevon JJ (2014) Bacterial capacities to mineralize phytate increase in the rhizosphere of nodulated common bean (Phaseolus vulgaris) under P deficiency. Eur J Soil Biol 62:8–14. https://doi.org/10.1016/j.ejsobi.2014.02.006
Maranguit D, Guillaume T, Kuzyakov Y (2017) Land-use change affects phosphorus fractions in highly weathered tropical soils. CATENA 149:385–393. https://doi.org/10.1016/j.catena.2016.10.010
Menezes-Blackburn D, Paredes C, Zhang H, Giles CD, Darch T, Stutter M, George TS, Shand C, Lumsdon D, Cooper P, Wendler R, Brown L, Blackwell M, Wearing C, Haygarth PM (2016) Organic acids regulation of chemical-microbial phosphorus transformations in soils. Environ Sci Technol 50:11521–11531. https://doi.org/10.1021/acs.est.6b03017
Meyer JB, Frapolli M, Keel C, Maurhofer M (2011) Pyrroloquinoline quinone biosynthesis gene pqqC, a novel molecular marker for studying the phylogeny and diversity of phosphate-solubilizing Pseudomonads. Appl Environ Microbiol 77:7345–7354. https://doi.org/10.1128/AEM.05434-11
Motavalli PP, Miles RJ (2002) Soil phosphorus fractions after 111 years of animal manure and fertilizer applications. Biol Fertil Soils 36:35–42. https://doi.org/10.1007/s00374-002-0500-6
Mou XM, Wu Y, Niu Z, Jia B, Guan ZH, Chen J, Li H, Cui H, Kuzyakov Y, Li XG (2020) Soil phosphorus accumulation changes with decreasing temperature along a 2300 m altitude gradient. Agric Ecosyst Environ 301:107050. https://doi.org/10.1016/j.agee.2020.107050
Nannipieri P, Giagnoni L, Landi L, Renella G (2011) Role of phosphatase enzymes in soil. In: Bünemann EK, Oberson A, Frossard E (eds) Phosphorus in action: biological processes in soil phosphorus cycling. Springer, Berlin, pp 215–243. https://doi.org/10.1007/978-3-642-15271-9_9
Norman JS, King GM, Friesen ML (2017) Rubrobacter spartanus sp. nov., a moderately thermophilic oligotrophic bacterium isolated from volcanic soil. Int J Syst Evol Microbiol 67:3597–3602. https://doi.org/10.1099/ijsem.0.002175
Oteino N, Lally RD, Kiwanuka S, Lloyd A, Ryan D, Germaine KJ, Dowling DN (2015) Plant growth promotion induced by phosphate solubilizing endophytic Pseudomonas isolates. Front Microbiol 6:745. https://doi.org/10.3389/fmicb.2015.00745
Prakash J, Mishra S (2022) Role of beneficial soil microbes in alleviating climatic stresses in plants. In: Kumar A, Singh J, Ferreira LFR (eds) Microbiome under changing climate: implications and solutions. Woodhead Publishing, Sawston, pp 29–68. https://doi.org/10.1016/B978-0-323-90571-8.00002-X
Qin X, Guo S, Zhai L, Pan J, Khoshnevisan B, Wu S, Wang H, Yang B, Ji J, Liu H (2020) How long-term excessive manure application affects soil phosphorous species and risk of phosphorous loss in fluvo-aquic soil. Environ Pollut 266:115304. https://doi.org/10.1016/j.envpol.2020.115304
Ragot SA, Kertesz MA, Bünemann EK (2015) phoD alkaline phosphatase gene diversity in soil. Appl Environ Microbiol 81:7281–7289. https://doi.org/10.1128/AEM.01823-15
Ragot SA, Huguenin-Elie O, Kertesz MA, Frossard E, Bünemann EK (2016) Total and active microbial communities and phoD as affected by phosphate depletion and pH in soil. Plant Soil 408:15–30. https://doi.org/10.1007/s11104-016-2902-5
Ragot SA, Kertesz MA, Mészáros É, Frossard E, Bünemann EK (2017) Soil phoD and phoX alkaline phosphatase gene diversity responds to multiple environmental factors. FEMS Microbiol Ecol 93:212. https://doi.org/10.1093/femsec/fiw212
Richardson AE, Simpson RJ (2011) Soil microorganisms mediating phosphorus availability update on microbial phosphorus. Plant Physiol 156:989–996. https://doi.org/10.1104/pp.111.175448
Richardson AE, Barea JM, McNeill AM, Prigent-Combaret C (2009) Acquisition of phosphorus and nitrogen in the rhizosphere and plant growth promotion by microorganisms. Plant Soil 321:305–339. https://doi.org/10.1007/s11104-009-9895-2
Rodríguez H, Fraga R, Gonzalez T, Bashan Y (2006) Genetics of phosphate solubilization and its potential applications for improving plant growth-promoting bacteria. Plant Soil 287:15–21. https://doi.org/10.1007/s11104-006-9056-9
Saito T, Ishii S, Otsuka S, Nishiyama M, Senoo K (2008) Identification of novel Betaproteobacteria in a succinate-assimilating population in denitrifying rice paddy soil by using stable isotope probing. Microbes Environ 23:192–200. https://doi.org/10.1264/jsme2.23.192
Salazar A, Sulman BN, Dukes JS (2018) Microbial dormancy promotes microbial biomass and respiration across pulses of drying-wetting stress. Soil Biol Biochem 116:237–244. https://doi.org/10.1016/j.soilbio.2017.10.017
Schimel JP, Bilbrough C, Welker JM (2004) Increased snow depth affects microbial activity and nitrogen mineralization in two Arctic tundra communities. Soil Biol Biochem 36:217–227. https://doi.org/10.1016/j.soilbio.2003.09.008
Shaw AN, Cleveland CC (2020) The effects of temperature on soil phosphorus availability and phosphatase enzyme activities: a cross-ecosystem study from the tropics to the Arctic. Biogeochemistry 151:113–125. https://doi.org/10.1007/s10533-020-00710-6
Shi Y, Lalande R, Ziadi N, Sheng M, Hu Z (2012) An assessment of the soil microbial status after 17 years of tillage and mineral P fertilization management. Appl Soil Ecol 62:14–23. https://doi.org/10.1016/j.apsoil.2012.07.004
Shi Q, Pang J, Yong JWH, Bai C, Pereira CG, Song Q, Wu D, Dong Q, Cheng X, Wang F, Zheng J, Liu Y, Lambers H (2020) Phosphorus-fertilisation has differential effects on leaf growth and photosynthetic capacity of Arachis hypogaea L. Plant Soil 447:99–116. https://doi.org/10.1007/s11104-019-04041-w
Song Q, Liu Y, Pang J, Yong JWH, Chen Y, Bai C, Gille C, Shi Q, Wu D, Han X, Li T, Siddique KHM, Lambers H (2020) Supplementary calcium restores peanut (Arachis hypogaea) growth and photosynthetic capacity under low nocturnal temperature. Front Plant Sci 10:1637–1651. https://doi.org/10.3389/fpls.2019.01637
Stackebrandt E, Goebel BM (1994) Taxonomic note: a place for DNA-DNA reassociation and 16S rRNA sequence analysis in the present species definition in bacteriology. Int J Syst Bacteriol 44:846–849. https://doi.org/10.1099/00207713-44-4-846
Stockfisch N, Joergensen RG, Wolters V, Klein T, Eberhardt U (1995) Examination of microbial biomass in beech forest moder profiles. Biol Fertil Soils 19:209–214. https://doi.org/10.1007/BF00336161
Sun Q, Guo S, Wang R, Song J (2021) Responses of bacterial communities and their carbon dynamics to subsoil exposure on the Loess Plateau. Sci Total Environ 756:144146. https://doi.org/10.1016/j.scitotenv.2020.144146
Sun H, Wu Y, Zhou J, Yu D, Chen Y (2022) Microorganisms drive stabilization and accumulation of organic phosphorus: an incubation experiment. Soil Biol Biochem 172:108750. https://doi.org/10.1016/j.soilbio.2022.108750
Tabatabai M (1994) Soil enzymes. In: Weaver RW, Angle JS, Bottomly PS (eds) Methods of soil analyses, Part 2, Microbiological and biochemical properties. Soil Science Society of America, Madison, pp 775–833
Tiessen H, Moir JO (1993) Characterization of available P by sequential fractionation. In: Carter MR (ed) Soil sampling and methods of analysis. Canadian Society of Soil Science. Lewis Publishers, Boca Raton, pp 75–86
Turner BL, Haygarth PM (2001) Biogeochemistry-phosphorus solubilization in rewetted soils. Nature 411:258–258. https://doi.org/10.1038/35077146
Vincent AG, Sundqvist MK, Wardle DA, Giesler R (2014) Bioavailable soil phosphorus decreases with increasing elevation in a subarctic tundra landscape. PLoS One 9:e92942. https://doi.org/10.1371/journal.pone.0092942
Wan W, Liu S, Li X, Xing Y, Chen W, Huang Q (2021) Dispersal limitation driving phoD-harboring bacterial community assembly: a potential indicator for ecosystem multifunctionality in long-term fertilized soils. Sci Total Environ 754:141960. https://doi.org/10.1016/j.scitotenv.2020.141960
Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naïve Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267. https://doi.org/10.1128/AEM.00062-07
Warren CR (2020) Soil microbial populations substitute phospholipids with betaine lipids in response to low P availability. Soil Biol Biochem 140:107655. https://doi.org/10.1016/j.soilbio.2019.107655
Wei Y, Zhao Y, Shi M, Cao Z, Lu Q, Yang T, Fan Y, Wei Z (2018) Effect of organic acids production and bacterial community on the possible mechanism of phosphorus solubilization during composting with enriched phosphate-solubilizing bacteria inoculation. Bioresour Technol 247:190–199. https://doi.org/10.1016/j.biortech.2017.09.092
Wu D, Liu Y, Pang J, Yong JWH, Chen Y, Bai C, Han X, Liu X, Sun Z, Zhang S, Sheng J, Li T, Siddique KHM, Lambers H (2020) Exogenous calcium alleviates nocturnal chilling-induced feedback inhibition of photosynthesis by improving sink demand in peanut (Arachis hypogaea). Front Plant Sci 11:e607029. https://doi.org/10.3389/fpls.2020.607029
Wu L, Zhang Y, Guo X, Ning D, Zhou X, Feng J, Yuan MM, Liu S, Guo J, Gao Z, Ma J, Kuang J, Jian S, Han S, Yang Z, Ouyang Y, Fu Y, Xiao N, Liu X, Wu L, Zhou A, Yang Y, Tiedje JM, Zhou J (2022) Reduction of microbial diversity in grassland soil is driven by long-term climate warming. Nat Microbiol 7:1054–1062. https://doi.org/10.1038/s41564-022-01147-3
Xu G, Sun JN, Xu RF, Lv YC, Shao HB, Yan K, Zhang LH, Blackwell MSA (2011) Effects of air-drying and freezing on phosphorus fractions in soils with different organic matter contents. Plant, Soil Environ 57:228–234. https://doi.org/10.17221/428/2010-pse
Yan L, Sunoj VSJ, Short AW, Lambers H, Elsheery NI, Kajita T, Wee AKS, Cao KF (2021) Correlations between allocation to foliar phosphorus fractions and maintenance of photosynthetic integrity in six mangrove populations as affected by chilling. New Phytol 232:2267–2282. https://doi.org/10.1111/nph.17770
Zederer DP, Talkner U, Spohn M, Joergensen RG (2017) Microbial biomass phosphorus and C/N/P stoichiometry in forest floor and A horizons as affected by tree species. Soil Biol Biochem 111:166–175. https://doi.org/10.1016/j.soilbio.2017.04.009
Zhang H, Shi L, Fu S (2020) Effects of nitrogen deposition and increased precipitation on soil phosphorus dynamics in a temperate forest. Geoderma 380:114650. https://doi.org/10.1016/j.geoderma.2020.114650
Zheng BX, Hao XL, Ding K, Zhou GW, Chen QL, Zhang JB, Zhu YG (2017) Long-term nitrogen fertilization decreased the abundance of inorganic phosphate solubilizing bacteria in an alkaline soil. Sci Rep 7:42284–42293. https://doi.org/10.1038/srep42284
Zheng BX, Zhang DP, Wang Y, Hao XL, Wadaan MAM, Hozzein WN, Peñuelas J, Zhu YG, Yang XR (2019) Responses to soil pH gradients of inorganic phosphate solubilizing bacteria community. Sci Rep 9:25. https://doi.org/10.1038/s41598-018-37003-w
Zhou J, Li XL, Peng F, Li C, Lai C, You Q, Xue X, Wu Y, Sun H, Chen Y, Zhong H, Lambers H (2021) Mobilization of soil phosphate after 8 years of warming is linked to plant phosphorus-acquisition strategies in an alpine meadow on the Qinghai-Tibetan Plateau. Glob Change Biol 27:6578–6591. https://doi.org/10.1111/gcb.15914
Zuccarini P, Asensio D, Ogaya R, Sardans J, Peñuelas J (2020) Effects of seasonal and decadal warming on soil enzymatic activity in a P-deficient Mediterranean shrubland. Glob Change Biol 26:3698–3714. https://doi.org/10.1111/gcb.15077
Funding
This study was financially supported by the National Key R&D Program of China (2022YFD1602110-3), the Project of Education Department of Liaoning Province (LXZX202204), the China Agriculture Research System (CARS-23-B02), Shenyang Science and Technology Project (22317207), and the Project of Education Department of Liaoning Province (LJKMZ20221023).
Author information
Authors and Affiliations
Contributions
Shi Q, Fu H, Sun Z, Liu Y, and Li T conceived the ideas. Shi Q and Li X collected the data, and Shi Q, Song Q, Wang S, and Shan X analyzed the data. All authors have participated in the preparation of this manuscript and have approved the final version.
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare no competing interests.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Hongdan Fu and Tianlai Li contributed equally to this work.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Shi, Q., Song, Q., Shan, X. et al. Microorganisms regulate soil phosphorus fractions in response to low nocturnal temperature by altering the abundance and composition of the pqqC gene rather than that of the phoD gene. Biol Fertil Soils 59, 973–987 (2023). https://doi.org/10.1007/s00374-023-01766-w
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00374-023-01766-w