Journal of Integrative Agriculture ›› 2024, Vol. 23 ›› Issue (5): 1685-1702.DOI: 10.1016/j.jia.2023.09.002
收稿日期:
2023-06-20
接受日期:
2023-07-28
出版日期:
2024-05-20
发布日期:
2024-04-24
Soybean (Glycine max) rhizosphere organic phosphorus recycling relies on acid phosphatase activity and specific phosphorus-mineralizing-related bacteria in phosphate deficient acidic soils
Qianqian
Chen1*, Qian Zhao1*, Baoxing Xie1*, Xing Lu1,
Qi Guo1, Guoxuan Liu1, Ming Zhou1, Jihui Tian2,
Weiguo Lu3, Kang Chen1, Jiang Tian1#, Cuiyue
Liang1#
1 Root Biology Center, State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, College of Natural Resources and Environment, South China Agricultural University, Guangzhou 510642, China
2 College of Natural Resources and Environment, South China Agricultural University, Guangzhou 510642, China
3 Henan Academy of Crops Molecular Breeding, Henan Academy of Agricultural Sciences, Zhengzhou 450002, China
Received:
2023-06-20
Accepted:
2023-07-28
Online:
2024-05-20
Published:
2024-04-24
About author:
#Correspondence Jiang Tian, Tel: +86-20-85283380, E-mail: jtian@scau.edu.cn; Cuiyue Liang, Mobile: +86-13570467247, E-mail: liangcy@scau.edu.cn
* These authors contributed equally to this study.
Supported by:
摘要:
细菌在调节土壤磷循环过程中发挥着重要的作用。而作物与磷有效性的交互作用对土壤细菌群落的影响,以及细菌群落的重塑对土壤磷循环的反馈作用尚不清楚。本研究选用6份磷效率不同的大豆(Glycine max)基因型为试验材料,进行不同磷肥水平处理的酸性土壤田间试验。测定了非根际土和根际土壤中酸性磷酸酶(Acid phosphatase,AcP)活性和有机磷浓度,并通过微生物高通量测序技术分析土壤16S rRNA和phoC基因细菌群落结构。试验结果表明,低磷肥处理条件下,土壤有机磷浓度与土壤AcP活性以及大豆植株磷含量均呈显著负相关。土壤磷有效性以及大豆根际效应均影响了土壤细菌群落组成。而根际优势物种变形菌门(Proteobacteria)在低磷处理下的相对丰度与土壤有机磷浓度和AcP活性密切相关。土壤phoC基因高通量测序结果显示,大豆根际土壤中贪铜菌属(Cupriavidus)和克雷伯氏菌(Klebsiella)的相对丰度较非根际土高,而黄单胞菌属(Xanthomonas)的相对丰度较低。其中,贪铜菌属(Cupriavidus)为土壤phoC基因优势细菌属,且与土壤有机磷浓度呈显著负相关。以上结果表明,在磷有效性较低的酸性土壤,大豆可能依赖其根系招募的phoC基因细菌(例如,贪铜菌属)所产生的酸性磷酸酶,活化利用土壤有机磷。
. 大豆依赖根际酸性磷酸酶活性及特定磷矿化细菌参与酸性土壤有机磷循环[J]. Journal of Integrative Agriculture, 2024, 23(5): 1685-1702.
Qianqian Chen, Qian Zhao, Baoxing Xie, Xing Lu, Qi Guo, Guoxuan Liu, Ming Zhou, Jihui Tian, Weiguo Lu, Kang Chen, Jiang Tian, Cuiyue Liang.
Soybean (Glycine max) rhizosphere organic phosphorus recycling relies on acid phosphatase activity and specific phosphorus-mineralizing-related bacteria in phosphate deficient acidic soils [J]. Journal of Integrative Agriculture, 2024, 23(5): 1685-1702.
Berendsen R L, Pieterse C M J, Bakker P A H M. 2012. The rhizosphere microbiome and plant health. Trends in Plant Science, 17, 478–486. Bergkemper F, Schöler A, Engel M, Lang F, Krüger J, Schloter M, Schulz S. 2016. Phosphorus depletion in forest soils shapes bacterial communities towards phosphorus recycling systems. Environmental Microbiology, 18, 1988–2000. Bremner J M, Mulvaney C S. 1982. Nitrogen-total. In: Page A L, Miller R H, Keeney D R, eds., Methods of Soil Analysis. ASA-SSSA, Madison. pp. 595–617. Caballero-Mellado J, Onofre-Lemus J, Santos P E D L, Martinez-Aguilar L. 2007. The tomato rhizosphere, an environment rich in nitrogen-fixing Burkholderia species with capabilities of interest for agriculture and bioremediation. Applied Microbiology and Biotechnology, 73, 5308–5319. Cao N, Zhi M L, Zhao W Q, Pang J Y, Hu W, Zhou Z G, Meng Y L. 2022. Straw retention combined with phosphorus fertilizer promotes soil phosphorus availability by enhancing soil P-related enzymes and the abundance of phoC and phoD genes. Soil and Tillage Research, 220, 105390. Chen C R, Condron L M, Davis M R, Sherlock R R. 2002. Phosphorus dynamics in the rhizosphere of perennial ryegrass (Lolium perenne L.) and radiata pine (Pinus radiate D. Don.). Soil Biology and Biochemistry, 34, 487–499. Chen H J. 2003. Phosphatase activity and P fractions in soils of an 18-year-old Chinese fir (Cunninghamia lanceolata) plantation. Forest Ecology and Management, 178, 301–310. Chen Q Q, Wu W W, Zhao T, Tan W Q, Tian J, Liang C Y. 2019. Complex gene regulation underlying mineral nutrient homeostasis in soybean root response to acidity stress. Genes, 10, 402. Chen X D, Jiang N, Condron L M, Dunfield K E, Chen Z H, Wang J K, Chen L J. 2019. Impact of long-term phosphorus fertilizer inputs on bacterial phoD gene community in a maize field, Northeast China. Science of the Total Environment, 669, 1011–1018. Deng Q X, Zhang T, Xie D T, Yang Y H. 2021. Rhizosphere microbial communities are significantly affected by optimized phosphorus management in a slope farming system. Frontiers in Microbiology, 12, 739844. Dick W A, Cheng L, Wang P. 2000. Soil acid and alkaline phosphatase activity as pH adjustment indicators. Soil Biology and Biochemistry, 32, 1915–1919. Edgar R C. 2013. UPARSE: Highly accurate OTU sequences from microbial amplicon reads. Nature Methods, 10, 996–998. Edgar R C, Haas B J, Clemente J C, Quince C, Knight R. 2011. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics, 27, 2194–2200. Fierer N, Bradford M A, Jackson R B. 2007. Toward an ecological classification of soil bacteria. Ecology, 88, 1354–1364. Fraser T, Lynch D H, Entz M H, Dunfield K E. 2015. Linking alkaline phosphatase activity with bacterial phoD gene abundance in soil from a long-term management trial. Geoderma, 257–258, 115–122. Fraser T D, Lynch D H, Gaiero J, Khosla K, Dunfield K E. 2017. Quantification of bacterial non-specific acid (phoC) and alkaline (phoD) phosphatase genes in bulk and rhizosphere soil from organically managed soybean fields. Applied Soil Ecology, 111, 48–56. Gao W H, Gao K, Guo Z H, Liu Y, Jiang L, Liu C, Liu X Y, Wang G L. 2021. Different responses of soil bacterial and fungal communities to 3 years of biochar amendment in an alkaline soybean soil. Frontiers in Microbiology, 12, 630418. George T S, Turner B L, Gregory P J, Cade-Menun B J, Richardson A E. 2006. Depletion of organic phosphorus from Oxisols in relation to phosphatase activities in the rhizosphere. European Journal of Soil Science, 57, 47–57. Guo L, Wang C, Shen R F. 2022. Stronger effects of maize rhizosphere than phosphorus fertilization on phosphatase activity and phosphorus-mineralizing-related bacteria in acidic soils. Rhizosphere, 23, 100555. Harrison A F. 1987. Soil Organic Phosphorus: A Review of World Literature. Commonwealth Agricultural Bureaux International, Wallingford. Hedin L O, Vitousek P M, Matson P A. 2003. Nutrient losses over four million years of tropical forest development. Ecology, 84, 2231–2255. Hinsinger P. 2001. Bioavailability of soil inorganic P in the rhizosphere as affected by root-induced chemical changes: A review. Plant and Soil, 237, 173–195. Hu M J, Peñuelas J, Sardans J, Tong C, Chang C T, Cao W Z. 2020. Dynamics of phosphorus speciation and the phoD phosphatase gene community in the rhizosphere and bulk soil along an estuarine freshwater-oligohaline gradient. Geoderma, 365, 114236. Huang J S, Hu B, Qi K B, Chen W J, Pang X Y, Bao W K, Tian G L. 2016. Effects of phosphorus addition on soil microbial biomass and community composition in a subalpine spruce plantation. European Journal of Soil Science, 72, 35–41. Huang Y L, Dai Z M, Lin J H, Ye H C, Dahlgrene R A, Xu J M. 2021. Labile carbon facilitated phosphorus solubilization as regulated by bacterial and fungal communities in Zea mays. Soil Biology and Biochemistry, 163, 108465. Jaccard P. 1908. Nouvelles recherches sur la distribution florale. Bulletin de la Société Vaudoise des Sciences Naturelles, 44, 223–270. (in French) Janssen P J, Van Houdt R, Moors H, Monsieurs P, Morin N, Michaux A, Benotmane M A, Leys N, Vallaeys T, Lapidus A, Monchy S, Médigue C, Taghavi S, McCorkle S, Dunn J, van der Lelie D, Mergeay M. 2010. The complete genome sequence of Cupriavidus metallidurans strain CH34, a master survivalist in harsh and anthropogenic environments. PLoS ONE, 5, e10433. Jorquera M, Martínez O, Maruyama F, Marschner P, de la Luz Mora M. 2008. Current and future biotechnological applications of bacterial phytases and phytase-producing bacteria. Microbes and Environments, 23, 182–191. Kamat S S, Williams H J, Raushel F M. 2011. Intermediates in the transformation of phosphonates to phosphate by bacteria. Nature, 480, 570–573. Kochian L V. 2012. Plant nutrition: Rooting for more phosphorus. Nature, 488, 466–467. Kundu B S, Nehra K, Yadav R, Tomar M. 2009. Biodiversity of phosphate solubilizing bacteria in rhizosphere of chickpea, mustard and wheat grown in different regions of Haryana. Indian Journal of Microbiology, 49, 120–127. Kuo S. 1996. Phosphorus. In: Sparks D L, Page A L, Helmke P A, Loeppert R H, eds., Methods of Soil Analysis Part 3. Chemical Methods. Soil Science Society of America, American Society of Agronomy, Madison. pp. 869–919. Kuppusamy S, Thavamani P, Megharaj M, Lee Y B, Naidu R. 2016. Polyaromatic hydrocarbon (PAH) degradation potential of a new acid tolerant, diazotrophic P-solubilizing and heavy metal resistant bacterium Cupriavidus sp. MTS-7 isolated from long-term mixed contaminated soil. Chemosphere, 162, 31–39. Lambers H. 2022. Phosphorus acquisition and utilization in plants. Annual Review of Plant Biology, 73, 17–42. Lang M, Christie P, Zhang J L, Li X L. 2018. Long-term phosphorus application to a maize monoculture influences the soil microbial community and its feedback effects on maize seedling biomass. Applied Soil Ecology, 128, 12–22. Lareen A, Burton F, Schäfer P. 2016. Plant root-microbe communication in shaping root microbiomes. Plant Molecular Biology, 90, 575–587. Li H Z, Bi Q F, Yang K, Zheng B X, Pu Q, Cui L. 2019. D2O-isotopelabeling approach to probing phosphate-solubilizing bacteria in complex soil communities by single-cell Raman spectroscopy. Analytical Chemistry, 91, 2239–2246. Liang C Y, Tian J, Lam H M, Lim B L, Yan X L, Liao H. 2010. Biochemical and molecular characterization of PvPAP3, a novel purple acid phosphatase isolated from common bean enhancing extracellular ATP utilization. Plant Physiology, 152, 854–865. Lidbury I D E A, Borsetto C, Murphy A R J, Bottrill A, Jones A M E, Bending G D, Hammond J P, Chen Y, Wellington E M H, Scanlan D J. 2021. Niche-adaptation in plant-associated Bacteroidetes favours specialisation in organic phosphorus mineralisation. The ISME Journal, 15, 1040–1055. Long X E, Yao H Y, Huang Y, Wei W X, Zhu Y G. 2018. Phosphate levels influence the utilization of rice rhizodeposition carbon and the phosphate-solubilising microbial community in a paddy soil. Soil Biology and Biochemistry, 118, 103–114. Luo G W, Sun B, Li L, Li M H, Liu M Q, Zhu Y Y, Guo S W, Ling N, Shen Q R. 2019. Understanding how long-term organic amendments increase soil phosphatase activities: Insight into phoD- and phoC-harboring functional microbial populations. Soil Biology and Biochemistry, 139, 107632. Mander C, Wakelin S, Young S, Condron L, O’Callaghan M. 2012. Incidence and diversity of phosphate-solubilising bacteria are linked to phosphorus status in grassland soils. Soil Biology and Biochemistry, 44, 93–101. Marschner P, Crowley D, Yang C H. 2004. Development of specific rhizosphere bacterial communities in relation to plant species, nutrition and soil type. Plant and Soil, 261, 199–208. Martinez-Aguilar L, Diaz R, Pena-Cabriales J J, Santos P E D L, Dunn M F, Caballero-Mellado J. 2008. Multichromosomal genome structure and confirmation of diazotrophy in novel plant-associated Burkholderia species. Applied Microbiology and Biotechnology, 74, 4574–4579. Mora M D L L, Demanet R, Acuña J J, Viscardi S, Jorquera M, Rengel Z, Duran P. 2017. Aluminum-tolerant bacteria improve the plant growth and phosphorus content in ryegrass grown in a volcanic soil amended with cattle dung manure. Applied Soil Ecology, 115, 19–26. Murphy J, Riley J P. 1962. A modified single solution method for the determination of phosphate in natural waters. Analytica Chimica Acta, 27, 31–36. Nannipieri P, Giagnoni L, Landi L, Renella G. 2011. Role of phosphatase enzymes in soil. In: Bünemann E, Oberson A, Frossard E, eds., Phosphorus in Action. Springer, Heidelberg. pp. 215–243. Neal A L, Blackwell M, Akkari E, Guyomar C, Clark I, Hirsch P R. 2018. Phylogenetic distribution, biogeography and the effects of land management upon bacterial non-specific acid phosphatase gene diversity and abundance. Plant and Soil, 427, 175–189. Neumann G. 2006. Quantitative determination of acid phosphatase activity in the rhizosphere and on the root surface. In: Luster J, Finlay R, eds., Handbook of Methods Used in Rhizosphere Research. Swiss Federal Research Institute WSL, Birmensdorf. pp. 426–427. Neumann G, Martinoia E. 2002. Cluster roots - an underground adaptation for survival in extreme environments. Trends in Plant Science, 7, 162–167. Nilsson R H, Ryberg M, Kristiansson E, Abarenkov K, Larsson K H, Kõljalg U. 2006. Taxonomic reliability of DNA sequences in public sequence databases: A fungal perspective. PLoS ONE, 1, e59. Peix A, Mateos P F, Rodriguez-Barrueco C, Martinez-Molina E, Velazquez E. 2001. Growth promotion of common bean (Phaseolus vulgaris L.) by a strain of Burkholderia cepacian under growth chamber conditions. Soil Biology and Biochemistry, 33, 1927–1935. Plaxton W C, Lambers H. 2015. Phosphorus: Back to the roots. In: Plaxton W C, Lambers H, eds., Annual Plant Reviews, Phosphorus Metabolism in Plants. John Wiley & Sons, Hoboken, NJ. pp. 3–15. Qian Y C, Shi J Y, Chen Y X, Lou L P, Cui X Y, Li P F, Tang J. 2010. Characterization of phosphate solubilizing bacteria in sediments from a shallow Eutrophic lake and a wetland: isolation, molecular identification and phosphorus release ability determination. Molecules, 15, 8518–8533. Qin L, Jiang H, Tian J, Zhao J, Liao H. 2011. Rhizobia enhance acquisition of phosphorus from different sources by soybean plants. Plant and Soil, 349, 25–36. Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner F O. 2013. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Research, 41, D590-D596. Ragot S A, Kertesz M A, Bünemann E K. 2015. PhoD alkaline phosphatase gene diversity in soil. Applied and Environmental Microbiology, 81, 7281–7289. Richardson A E, Barea J M, McNeill A M, Prigent-Combaret C. 2009. Acquisition of phosphorus and nitrogen in the rhizosphere and plant growth promotion by microorganisms. Plant and Soil, 321, 305–339. Santos P E D L, Bustillos-Cristales R, Caballero-Mellado J. 2001. Burkholderia, a genus rich in plant-associated nitrogen fixers with wide environmental and geographic distribution. Applied Microbiology and Biotechnology, 67, 2790–2798. Sattari S Z, Bouwman A F, Giller K E, van Ittersum M K. 2012. Residual soil phosphorus as the missing piece in the global phosphorus crisis puzzle. Proceedings of the National Academy of Sciences of the United States of America, 109, 6348–6353. Sawyer A, Staley C, Lamb J, Sheaffer C, Kaiser T, Gutknecht J, Sadowsky M J, Rosen C. 2019. Cultivar and phosphorus effects on switchgrass yield and rhizosphere microbial diversity. Applied Microbiology and Biotechnology, 103, 1973–1987. Sharma S B, Sayyed R Z, Trivedi M H, Gobi T A. 2013. Phosphate solubilizing microbes: sustainable approach for managing phosphorus deficiency in agricultural soils. Springerplus, 2, 587. Sims J T. 2000. Soil test phosphorus: Bray and Kurtz P-1. In: Pierzynski G M, ed., Methods of Phosphorus Analysis for Soils, Sediments, Residuals, and Waters. North Carolina State University, Raleigh. pp. 13–14. Spohn M, Ermak A, Kuzyakov Y. 2013. Microbial gross organic phosphorus mineralization can be stimulated by root exudates - A 33P isotopic dilution study. Soil Biology and Biochemistry, 65, 254–263. Sugiyama A, Ueda Y, Zushi T, Takase H, Yazaki K. 2014. Changes in the bacterial community of soybean rhizospheres during growth in the field. PLoS ONE, 9, e100709. Tan H, Barret M, Mooij M J, Rice O, Morrissey J P, Dobson A, Griffiths B, O’Gara F. 2013. Long-term phosphorus fertilisation increased the diversity of the total bacterial community and the phoD phosphorus mineraliser group in pasture soils. Biology and Fertility of Soils, 49, 661–672. Tian J H, Kuang X Z, Tang M T, Chen X D, Huang F, Cai Y X, Cai K Z. 2021. Biochar application under low phosphorus input promotes soil organic phosphorus mineralization by shifting bacterial phoD gene community composition. Science of the Total Environment, 779, 146556. Tian J H, Lu X, Chen Q Q, Kuang X Z, Liang C Y, Deng L S, Lin D J, Cai K Z, Tian J. 2020. Phosphorus fertilization affects soybean rhizosphere phosphorus dynamics and the bacterial community in karst soils. Plant and Soil, 475, 137–152. Uroz S, Calvaruso C, Turpault M P, Frey-Klett P. 2009. Mineral weathering by bacteria: Ecology, actors and mechanisms. Trends in Microbiology, 17, 378–387. USEPA. 1971. Phosphorus, All Forms (Colorimetric, Ascorbic Acid, Single Reagent). U.S. Environmental Protection Agency, Office of Water, Washington, D. C. Walkley A, Black I A. 1934. An examination of the Degtjareff method for determining soil organic matter and a proposed modification of the chromic acid titration method. Soil Science, 37, 29–38. Wang C Q, Xue L, Jiao R Z. 2022. Stoichiometric imbalances and the dynamics of phosphatase activity and the abundance of phoC and phoD genes with the development of Cunninghamia lanceolata (Lamb.) hook plantations. Applied Soil Ecology, 173, 104373. Wang Q, Wang C, Yu W W, Turak A, Chen D W, Huang Y, Ao J H, Jiang Y, Huang Z R. 2018. Effects of nitrogen and phosphorus inputs on soil bacterial abundance, diversity, and community composition in Chinese fir plantations. Frontiers in Microbiology, 9, 1543. Wang Y, Zhao X, Guo Z Y, Jia Z J, Wang S Q, Ding K. 2018. Response of soil microbes to a reduction in phosphorus fertilizer in rice–wheat rotation paddy soils with varying soil P levels. Soil and Tillage Research, 181, 127–135. Warton D I, Wright S T, Wang Y. 2012. Distance-based multivariate analyses confound location and dispersion effects. Methods in Ecology and Evolution, 3, 89–101. Weisskopf L, Heller S, Eberl L. 2011. Burkholderia species are major inhabitants of white lupin cluster roots. Applied and Environmental Microbiology, 77, 7715–7720. Xiao X, Chen W M, Zong L, Yang J, Jiao S, Lin Y B, Wang E T, Wei G H. 2017. Two cultivated legume plants reveal the enrichment process of the microbiome in the rhizocompartments. Molecular Ecology, 26, 1641–1651. Yamazaki S, Mardani-Korrani H, Kaida R, Ochiai K, Kobayashi M, Nagano A J, Fujii Y, Sugiyama A, Aoki Y. 2021. Field multi-omics analysis reveals a close association between bacterial communities and mineral properties in the soybean rhizosphere. Scientific Reports, 11, 8878. Yang W N, Yu L, Luo D H, Xiong Z Y, Wang Y Y, Xu M, Wang Z F, Gao M. 2022. Effect of combined application of biochar with chemical fertilizer and organic fertilizer on soil phosphatase activity and microbial community. Environmental Science, 43, 540–549. (in Chinese) Yu X, Liu X, Zhu T H, Liu G H, Mao C. 2011. Isolation and characterization of phosphate-solubilizing bacteria from walnut and their effect on growth and phosphorus mobilization. Biology and Fertility of Soils, 47, 437–446. Zhang S, Zhou J, Wang G H, Wang X R, Liao H. 2015. The role of mycorrhizal symbiosis in aluminum and phosphorus interactions in relation to aluminum tolerance in soybean. Applied Microbiology and Biotechnology, 99, 10225–10235. Zhao J, Fu J B, Liao H, He Y, Nian H, Hu Y M, Qiu L J, Dong Y S, Yan X L. 2004. Characterization of root architecture in an applied core collection for phosphorus efficiency of soybean germplasm. Chinese Science Bulletin, 49, 1611–1620. Zheng M M, Wang C, Li W X, Guo L, Cai Z J, Wang B R, Chen J, Shen R F. 2021. Changes of acid and alkaline phosphatase activities in long-term chemical fertilization are driven by the similar soil properties and associated microbial community composition in acidic soil. European Journal of Soil Biology, 104, 103312. Zheng M M, Wang C, Li W X, Song W F, Shen R F. 2019. Soil nutrients drive function and composition of phoC-harboring bacterial community in acidic soils of southern China. Frontiers in Microbiology, 10, 2654. Zhu S N, Chen M H, Liang C Y, Xue Y B, Lin S L, Tian J. 2020. Characterization of purple acid phosphatase family and functional analysis of GmPAP7a/7b involved in extracellular ATP utilization in soybean. Frontiers in Plant Science, 11, 661. Zhuang L B, Li Y, Wang Z S, Yu Y, Zhang N, Yang C, Zeng Q C, Wang Q. 2020. Synthetic community with six Pseudomonas strains screened from garlic rhizosphere microbiome promotes plant growth. Microbial Biotechnology, 14, 488–502.
|
No related articles found! |
阅读次数 | ||||||
全文 |
|
|||||
摘要 |
|
|||||