Abstract
Purpose
Alkaline phosphatase (ALP), which was encoded by bacterial phoD genes, hydrolyzes organic phosphorus (P) into dissolved phosphorus in soils and is therefore vital for absorbing phosphorus (P) in vegetation. However, the unreasonable application of chemical fertilizer will inhibit this process of dissolving phosphorus. Until now, although the fact that straw is the optimal C source has been recognized, its impact on phoD-harboring bacteria under decreasing chemical fertilizer is not clear.
Materials and methods
A field experiment was established with chemical fertilizer only (F) and the gradient inorganic fertilizer reduction with straw: inorganic fertilizer with straw (FS), 70% inorganic fertilizer with straw (0.7FS), 60% inorganic fertilizer with straw (0.6FS), and 50% inorganic fertilizer with straw (0.5FS). Mixed treatments received equal amounts of straw. Integrated high-throughput absolute abundance quantification (iHAAQ) was used to investigate the phoD bacterial community structure.
Results and discussion
From the correlation between the plant-total P of three vegetables and microbial variables, only the plant-total P of chili was significantly related to ALP and the abundance of phoD gene. Although the total vegetable yield was significantly increased by the addition of straw, no correlation with ALP and phoD bacterial community was found. In addition, the abundance of the phoD bacterial community and the levels of ALP activity were both higher in a regime featuring 70% inorganic fertilization with straw (0.7FS), but the ability of phoD bacteria ALP release was strongly activated in a regime featuring 50% inorganic fertilization with straw (0.5FS). Distance-based redundancy analysis (db-RDA) indicated that the community of phoD bacteria clustered four groups and suggested that a number of soil factors played key roles in shaping the entire phoD bacterial community, including soil organic carbon, total nitrogen, available phosphorus, Ca2+-Ex, and total potassium. The correlation between the absolute abundance of ALP-regulating bacteria and ALP activity suggests that Amycolatopsis may predominantly account for ALP activity, especially in the 0.5FS regime.
Conclusion
In the reduction of chemical fertilizer, the straw substitution did not reshape the structure of the phoD bacterial community but strongly activated phoD bacteria to release ALP.
Similar content being viewed by others
References
Ahlgren J, Djodjic F, Börjesson G, Mattsson L (2013) Identification and quantification of organic phosphorus forms in soils from fertility experiments. Soil Use Manag 29:24–35. https://doi.org/10.1111/sum.12014
Alniemi TS, Summers ML, Elkins JG, Kahn ML, Mcdermott TR (1997) Regulation of the phosphate stress response in rhizobium meliloti by phoB. Appl Environ Microbiol 63:4978–4589. https://doi.org/10.1089/oli.1.1997.7.585
Bakker MG, Otto-Hanson L, Lange AJ, Bradeen JM, Kinkel LL (2013) Plant monocultures produce more antagonistic soil streptomyces, communities than high-diversity plant communities. Soil Biol Biochem 65:304–312. https://doi.org/10.1016/j.soilbio.2013.06.007
Beyer L, Sieling K, Pingpank K (1999) The impact of a low humus level in arable soils on microbial properties, soil organic matter quality and crop yield. Biol Fertil Soils 28(2):156–161. https://doi.org/10.1007/s003740050478
Chaturvedi S, Upreti DK, Tandon DK, Sharma A, Dixit A (2008) Biowaste from tobacco industry as tailored organic fertilizer for improving yield and nutritional values of tomato crop. J Environ Biol 29:759–763. https://doi.org/10.1093/molbev/msu320
Chen H (2003) Phosphatase activity and p fractions in soils of an 18-year-old Chinese fir (cunninghamia lanceolata) plantation. Forest Ecol Manag 178:301–310. https://doi.org/10.1016/S0378-1127(02)00478-4
Chen XD, Jiang N, Condron LM, Dunfield KE, Chen ZH, Wang JK, Chen LJ (2019a) 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
Chen XD, Jiang N, Condron LM, Dunfield KE, Chen ZH, Wang JK, Chen LJ (2019b) Soil alkaline phosphatase activity and bacterial phoD gene abundance and diversity under long-term nitrogen and manure inputs. Geoderma 349:36–44. https://doi.org/10.1016/j.geoderma.2019.04.039
Duan Y, Xu M, Gao S, Yang X, Huang S, Liu H (2014) Nitrogen use efficiency in a wheat-corn cropping system from 15 years of manure and fertilizer applications. Field Cros Res 157:47–56. https://doi.org/10.1016/j.fcr.2013.12.012
Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics. 26:2460–2461. https://doi.org/10.1093/bioinformatics/btq461
Edgar RC (2013) Uparse: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10:996–998. https://doi.org/10.1038/NMETH.2604
FAO (1988) Soil map of the world, revised legend. World Resources Report
Fraser TD, Lynch DH, Bent E, Entz MH, Dunfield KE (2015a) 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
Fraser TD, Lynch DH, Entz MH, Dunfield KE (2015b) Linking alkaline phosphatase activity with bacterial phoD gene abundance in soil from a long-term management trial. Geoderma. 257–258:115–122. https://doi.org/10.1016/j.geoderma.2014.10.016
Fraser TD, Lynch DH, Gaiero J, Khosla K, Dunfield KE (2017) Quantification of bacterial non-specific acid (phoC) and alkaline (phoD) phosphatase genes in bulk and rhizosphere soil from organically managed soybean fields. Appl Soil Ecol 111:48–56. https://doi.org/10.1016/j.apsoil.2016.11.013
Garg S, Bahl GS (2008) Phosphorus availability to maize as influenced by organic manures and fertilizer P associated phosphatase activity in soils. Bioresour Technol 99:5773–5777. https://doi.org/10.1016/j.biortech.2007.10.063
Goulding K, Jarvis S, Whitmore A (2008) Optimizing nutrient management for farm systems. Philos Trans R Soc Lond 363:667–680. https://doi.org/10.1098/rstb.2007.2177
Hamdali H, Hafidi M, Virolle MJ, Ouhdouch Y (2008) Rock phosphate-solubilizing actinomycetes: screening for plant growth-promoting activities. World J Microbiol Biotechnol 24:2565–2575. https://doi.org/10.1007/s11274-008-9817-0
Herencia JF, Maqueda C (2016) Effects of time and dose of organic fertilizers on soil fertility, nutrient content and yield of vegetables. J Agric Sci 154:1343–1361. https://doi.org/10.1017/s0021859615001136
Hu Y, Xia Y, Sun Q, Liu K, Chen X, Ge T (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
Jiménez DJ, Korenblum E, Elsas JDV (2014) Novel multispecies microbial consortia involved in lignocellulose and 5-hydroxymethylfurfural bioconversion. Appl Microbiol Biotechnol 98:2789–2803. https://doi.org/10.1007/s00253-013-5253-7
Jorquera MA, Martínez OA, Marileo LG, Acuña JJ, Saggar S, Mora ML (2014) Effect of nitrogen and phosphorus fertilization on the composition of rhizobacterial communities of two Chilean andisol pastures. World J Microbiol Biotechnol 30:99–107. https://doi.org/10.1007/s11274-013-1427-9
Kageyama H, Tripathi K, Rai AK, Cha-Um S, Waditee-Sirisattha R, Takabe T (2011) An alkaline phosphatase/phosphodiesterase, phod, induced by salt stress and secreted out of the cells of aphanothece halophytica, a halotolerant cyanobacterium. Appl Environ Microbiol 77:5178–5183. https://doi.org/10.1128/AEM.00667-11
Kathuria S, Martiny AC (2011) Prevalence of a calcium-based alkaline phosphatase associated with the marine cyanobacterium prochlorococcus and other ocean bacteria. Environ Microbiol 13:74–83. https://doi.org/10.1111/j.1462-2920.2010.02310.x
Letunic I, Bork P (2007) Interactive tree of life (itol): an online tool for phylogenetic tree display and annotation. FEBS Lett 23:127–128. https://doi.org/10.1093/bioinformatics/btl529
Li BY, Zhou DM, Cang L, Zhang HL, Fan XH, Qin SW (2007) Soil micronutrient availability to crops as affected by long-term inorganic and organic fertilizer applications. Soil Tillage Res 96:166–173. https://doi.org/10.1016/j.still.2007.05.005
Lin K, Li DC, Zhang GL (2017) Relationships between pH and content of calcium carbonate and equivalents in soil of the Heihe River Valley, Northwest China. Acta Pedol Sin 54:345–353 (in Chinese)
Liu E, Yan C, Mei X, He W, Bing SH, Ding L (2010) Long-term effect of chemical fertilizer, straw, and manure on soil chemical and biological properties in Northwest China. Geoderma 158:0–180. https://doi.org/10.1016/j.geoderma.2010.04.029, 173
Liu X, Li J, Yu L, Pan H, Liu H, Liu Y (2017) Simultaneous measurement of bacterial abundance and composition in response to biochar in soybean field soil using 16S rRNA gene sequencing. Land Degrad Dev 29:2172–2182. https://doi.org/10.1002/ldr.2838
Lou J, Yang L, Wang H, Wu L, Xu J (2018) Assessing soil bacterial community and dynamics by integrated high-throughput absolute abundance quantification. Peer J 6:e4514. https://doi.org/10.7717/peerj.4514
Luo G, Ling N, Nannipieri P, Chen H, Raza W, Wang M (2017) Long-term fertilisation regimes affect the composition of the alkaline phosphomonoesterase encoding microbial community of a vertisol and its derivative soil fractions. Biol Fertil Soils 53:375–388. https://doi.org/10.1007/s00374-017-1183-3
Nannipieri P, Giagnoni L, Landi L, Renella G (2011) Role of phosphatase enzymes in soil, phosphorus in action. Springer, Berlin
Neal AAL, Glending BMJ (2019) Calcium exerts a strong influence upon phosphohydrolase gene abundance and phylogenetic diversity in soil. Soil Biol Biochem 139:107613
Nottfige DO, Ojeniyi SO, Asawalam DO (2006) Comparative effect of plant residues and NPK fertilizer on nutrient status and yield of maize (Zea mays L.) in a humid ultisol. Nigerian. J Soil Sci 15
Pathak H, Singh R, Bhatia A, Jain N (2006) Recycling of rice straw to improve wheat yield and soil fertility and reduce atmospheric pollution. Paddy Water Environ 4:111–117. https://doi.org/10.1007/s10333-006-0038-6
Ragot SA, Kertesz MA, Bünemann EK (2015) PhoD alkaline phosphatase gene diversity in soil. Appl Environ Microbiol 81:281–7289. 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 408:1–16. https://doi.org/10.1007/s11104-016-2902-5
Roper MM (1985) Straw decomposition and nitrogenase activity (C2H2, reduction): effects of soil moisture and temperature. Soil Biol Biochem 17:65–71. https://doi.org/10.1016/0038-0717(85)90091-4
Roper MM, Smith NA (1991) Straw decomposition and nitrogenase activity (C2H2 reduction) by free-living microorganisms from soil: effects of pH and clay content. Soil Biol Biochem 23:275–283. https://doi.org/10.1016/0038-0717(91)90064-Q
Rosas SB, Andres JA, Rovera M (2006) Correa NS phosphate-solubilizing pseudomonas putida can influence the rhizobia-legume symbiosis. Soil Biol Biochem 38:3502–3505. https://doi.org/10.1016/j.soilbio.2006.05.008
Saha S, Prakash V, Kundu S, Kumar N, Mina BL (2008) Soil enzymatic activity as affected by long term application of farm yard manure and mineral fertilizer under a rainfed soybean-wheat system in n-w Himalaya. Eur J Soil Biol 44:309–315. https://doi.org/10.1016/j.ejsobi.2008.02.004
Sakurai M, Wasaki J, Tomizawa Y, Shinano T, Osaki M (2008) Analysis of bacterial communities on alkaline phosphatase genes in soil supplied with organic matter. Soil Sci Plant Nutr 54:62–71. https://doi.org/10.1111/j.1747-0765.2007.00210.x
Santos-Beneit F (2015) The Pho regulon: a huge regulatory network in bacteria. Front Microbiol 6:402. https://doi.org/10.3389/fmicb.2015.00402
Schlatter DC, Bakker MG, Bradeen JM, Kinkel LL (2015) Plant community richness and microbial interactions structure bacterial communities in soil. Ecology 96:134–142. https://doi.org/10.1890/13-1648.1
Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB (2009) Introducing Mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541. https://doi.org/10.1128/AEM.01541-09
Singh CP, Amberger A (1991) Solubilization and availability of phosphorus during decomposition of rock phosphate enriched straw and urine. Biol Agric Hortic 7:261–269. https://doi.org/10.1080/01448765.1991.9754553
Smart JB, Dilworth MJ, Robson AD (1984) Effect of phosphorus supply on phosphate uptake and alkaline phosphatase activity in rhizobia. Arch Microbiol 140:281–286. https://doi.org/10.1007/BF00454943
Smets W, Leff JW, Bradford MA, Mcculley RL, Lebeer S, Fierer N (2016) A method for simultaneous measurement of soil bacterial abundances and community composition via 16s rRNA gene sequencing. Soil Biol Biochem 96:145–151. https://doi.org/10.1016/j.soilbio.2016.02.003
Šmilauer P, Lepš J (2014) Multivariate analysis of ecological data using CANOCO 5: introduction and data types. https://doi.org/10.1017/CBO9781139627061.002
Spohn M, Kuzyakov Y (2013) Phosphorus mineralization can be driven by microbial need for carbon. Soil Biol Biochem 61:69–75. https://doi.org/10.1016/j.soilbio.2013.02.013
Spohn M, Treichel NS, Cormann M, Schloter M, Fischer D (2015) Distribution of phosphatase activity and various bacterial phyla in the rhizosphere of Hordeum vulgare, l. depending on P availability. Soil Biol Biochem 89:44–51. https://doi.org/10.1016/j.soilbio.2015.06.018
Stemmer M, von Lützow M, Kandeler E, Pichlmayer F, Gerzabek MH (2010) The effect of maize straw placement on mineralization of c and n in soil particle size. Eur J Soil Sci 50:73–85. https://doi.org/10.1046/j.1365-2389.1999.00204.x
Tan H, Barret M, Mooij MJ, Olivia R (2013) Long-term phosphorus fertilisation increased the diversity of the total bacterial community and the phoD phosphorus mineraliser group in pasture soils. Biol Fertil Soils 49:661–672. https://doi.org/10.1007/s00374-012-0755-5
Tang HM, Xiao XP, Li C, Cheng KK, Wang K (2018) Effects of different long-term fertilization managements on nutrition accumulation and translocation of rice plant in double cropping paddy field. Ecol Environ Sci 27:469–477. https://doi.org/10.16258/j.cnki.1674-5906.2018.03.010
Tilman D, Cassman KG, Matson PA, Naylor R, Polasky S (2002) Agricultural sustainability and intensive production practices. Nature 418:671–677. https://doi.org/10.1038/nature01014
Vershinina O, Znamenskaya L (2002) The Pho regulons of bacteria. Microbiology 71:497–511. https://doi.org/10.1023/A:1020547616096
Waldrip HM, He Z, Erich MS (2011) Effects of poultry manure amendment on phosphorus uptake by ryegrass, soil phosphorus fractions and phosphatase activity. Biol Fertil Soils 47:407–418. https://doi.org/10.1007/s00374-011-0546-4
Wang Y, Tang J, Zhang H, Schroder JL, He Y (2014) Phosphorus availability and sorption as affected by long-term fertilization. Agron J 106:1583–1592. https://doi.org/10.2134/agronj14.0059
Warncke D, Brown JR (1998) Potassium and other basic cations. In: Brown JR (ed) Recommended chemical soil test procedures for the north central region, vol 221. Missouri Agricultural Experiment Station, Columbia, pp 31–33
Welsh C, Tenuta M, Flaten DN, Thiessenmartens JR, Entz MH (2009) High yielding organic crop management decreases plant-available but not recalcitrant soil phosphorus. Agron J 101:1027–1035. https://doi.org/10.2134/agronj2009.0043
Wink J (2004) Amycolatopsis decaplanina sp. nov. a novel member of the genus with unusual morphology. Int J Syst Evol Microbiol 54:235–239. https://doi.org/10.1099/ijs.0.02586-0
Withers PJA, Haygarth PM (2010) Agriculture, phosphorus and eutrophication: a European perspective. Soil Use Manag 23:1–4. https://doi.org/10.1111/j.1475-2743.2007.00116.x
Xiao Y, Tang J, Wang MK (2016) Physicochemical properties of three typical purple soils with different parent materials and land uses in Sichuan basin, China. Nat Resour Eng 1:59–68. https://doi.org/10.1080/23802693.2016.1258854
Yang JH, Wang CL, Dai HL (2008) Agricultural soil analysis and environmental monitoring. China Land Press, Beijing (in Chinese)
Yang L, Lou J, Wang H, Wu L, Xu J (2018) Use of an improved high-throughput absolute abundance quantification method to characterize soil bacterial community and dynamics. Sci Total Environ 633:360–371. https://doi.org/10.1016/j.scitotenv.2018.03.201
Zhang FS, Chen XP, Duan BW (2009) Guide to fertilization of major crops in China. China Agricultural University Press, Beijing (in Chinese)
Zhang G, Chen Z, Zhang A, Chen L, Wu Z, Ma X (2014a) Phosphorus composition and phosphatase activities in soils affected by long-term application of pig manure and inorganic fertilizers. Commun Soil Sci Plan 45:1866–1876. https://doi.org/10.1080/00103624.2014.909831
Zhang J, Kobert K, Flouri T, Stamatakis A (2014b) A pear: a fast and accurate illumina paired-end read merger. Bioinformatics. 30:614–620. https://doi.org/10.1093/bioinformatics/btt593
Zimmerman A, Martiny AC, Allison SD (2013) Microdiversity of extracellular enzyme genes among sequenced prokaryotic genomes. Isme J 7:1187–1199. https://doi.org/10.1038/ismej.2012.176
Funding
This study was financially supported by the National Key Research and Development Plan of China (Grant No. 2017YFD0800101).
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare that they have no competing interests.
Ethical approval
This research does not involve human participants and/or animals.
Additional information
Responsible editor: Yuan Ge
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
ESM 1
(DOCX 191 kb)
Rights and permissions
About this article
Cite this article
Wang, Y., Huang, R., Xu, G. et al. Soil alkaline phosphatase activity and bacterial phoD gene abundance and diversity under regimes of inorganic fertilizer reduction with straw. J Soils Sediments 21, 388–402 (2021). https://doi.org/10.1007/s11368-020-02748-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11368-020-02748-3