Abstract
Aims
Although phosphorus (P) availability and plant cultivation affect diazotrophic populations, studies often consider individual factors rather than their combined effects. Their relative importance to diazotrophs remains poorly understood, especially in acidic soils with P deficiency. It is hypothesized that the influences of P fertilization and plant cultivation on diazotrophic communities differ in acidic soils. The objectives were to investigate these influences and identify the key determining factors.
Methods
Maize was grown in an acidic soil that was supplemented with 0, 20, and 50 mg P kg− 1 for 42 days. Maize biomasses, plant nutrient contents, and soil physicochemical properties were determined. Based on the nifH gene, the abundances and community compositions of diazotrophs in the different plant/soil compartments (bulk soils, rhizosphere soils, and roots) were respectively investigated using quantitative PCR and high-throughput sequencing.
Results
P fertilization significantly improved the diazotrophic abundances in the bulk and rhizosphere soils, but not in the roots. The plant/soil compartments had stronger effects on the abundance and diversity of diazotrophs than did P fertilization. Furthermore, the plant/soil compartments influenced diazotrophic community composition, but P fertilization did not. However, in the same sampling site, P fertilization caused community variations in the bulk and rhizosphere soils, rather than in the roots.
Conclusions
Although P fertilization affected the abundances and compositions of diazotrophic communities in the bulk and rhizosphere soils, the plant/soil compartments resulting from maize cultivation had more noticeable effects than did P fertilization. These findings improved the understanding of biological nitrogen fixation in acidic soils.
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References
Appunu C, Dhar B (2006) Symbiotic effectiveness of acid-tolerant Bradyrhizobium strains with soybean in low pH soil. Afr J Biotechnol 5:842–845
Augusto L, Delerue F, Gallet-Budynek A, Achat DL (2013) Global assessment of limitation to symbiotic nitrogen fixation by phosphorus availability in terrestrial ecosystems using a meta-analysis approach. Global Biogeochem Cy 27:804–815
Barron AR, Wurzburger N, Bellenger JP, Wright SJ, Kraepiel AML, Hedin LO (2009) Molybdenum limitation of asymbiotic nitrogen fixation in tropical forest soils. Nat Geosci 2:42–45
Bashan Y, Holguin G, de-Bashan LE (2004) Azospirillum-plant relationships: physiological, molecular, agricultural, and environmental advances (1997–2003). Can J Microbiol 50:521–577
Batterman SA, Wurzburger N, Hedin LO (2013) Nitrogen and phosphorus interact to control tropical symbiotic N2 fixation: a test in Inga punctata. J Ecol 101:1400–1408
Benner JW, Conroy S, Lunch CK, Toyoda N, Vitousek PM (2007) Phosphorus fertilization increases the abundance and nitrogenase activity of the cyanolichen Pseudocyphellaria crocata in Hawaiian Montane Forests. Biotropica 39:400–405
Bouffaud ML, Renoud S, Moënne-Loccoz Y, Muller D (2016) Is plant evolutionary history impacting recruitment of diazotrophs and nifH expression in the rhizosphere? Sci Rep 6:21690
Bulgarelli D, Rott M, Schlaeppi K, van Themaat EVL, Ahmadinejad N, Assenza F, Rauf P, Huettel B, Reinhardt R, Schmelzer E, Peplies J, Gloeckner FO, Amann R, Eickhorst T, Schulze-Lefert P (2012) Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota. Nature 488:91–95
Chen G, Zhu H, Zhang Y (2003) Soil microbial activities and carbon and nitrogen fixation. Res Microbiol 154:393–398
Cleveland CC, Townsend AR, Schimel DS, Fisher H, Howarth RW, Hedin LO, Perakis SS, Latty EF, Von Fischer JC, Elseroad A, Wasson MF (1999) Global patterns of terrestrial biological nitrogen (N2) fixation in natural ecosystems. Global Biogeochem Cy 13:623–645
Coelho MRR, Marriel IE, Jenkins SN, Lanyon CV, Seldin L, O’Donnell AG (2009) Molecular detection and quantification of nifH gene sequences in the rhizosphere of sorghum (Sorghum bicolor) sown with two levels of nitrogen fertilizer. Appl Soil Ecol 42:48–53
Deubel A, Gransee A, Merbach W (2000) Transformation of organic rhizodepositions by rhizosphere bacteria and its influence on the availability of tertiary calcium phosphate. J Plant Nutr Soil Sci 163:387–392
Ferrando L, Scavino AF (2015) Strong shift in the diazotrophic endophytic bacterial community inhabiting rice (Oryza sativa) plants after flooding. FEMS Microbiol Ecol 91:fiv104
Gaby JC, Buckley DH (2014) A comprehensive aligned nifH gene database: a multipurpose tool for studies of nitrogen- fixing bacteria. Database (Oxford) 2014: bau001
Guo JH, Liu XJ, Zhang Y, Shen JL, Han WX, Zhang WF, Christie P, Goulding KWT, Vitousek PM, Zhang FS (2010) Significant acidification in major Chinese croplands. Science 327:1008–1010
Gyaneshwar P, James EK, Reddy PM, Ladha JK (2002) Herbaspirillum colonization increases growth and nitrogen accumulation in aluminium-tolerant rice varieties. New Phytol 154:131–145
Hartley AE, Schlesinger WH (2002) Potential environmental controls on nitrogenase activity in biological crusts of the northern Chihuahuan Desert. J Arid Environ 52:293–304
Huang J, Xu X, Wang M, Nie M, Qiu S, Wang Q, Quan Z, Xiao M, Li B (2016) Responses of soil nitrogen fixation to Spartina alterniflora invasion and nitrogen addition in a Chinese salt marsh. Sci Rep 6:20384
Kochian LV, Hoekenga OA, Piñeros MA (2004) How do crop plants tolerate acid soils? Mechanisms of aluminum tolerance and phosphorous efficiency. Annu Rev Plant Biol 55:459–493
Krause A, Ramakumar A, Bartels D, Battistoni F, Bekel T, Boch J, Bohm M, Friedrich F, Hurek T, Krause L, Linke B, McHardy AC, Sarkar A, Schneiker S, Syed AA, Thauer R, Vorholter FJ, Weidner S, Puhler A, Reinhold-Hurek B, Kaiser O, Goesmann A (2006) Complete genome of the mutualistic, N2-fixing grass endophyte Azoarcus sp. strain BH72. Nat Biotech 24:1385–1391
Kunito T, Isomura I, Sumi H, Park HD, Toda H, Otsuka S, Nagaoka K, Saeki K, Senoo K (2016) Aluminum and acidity suppress microbial activity and biomass in acidic forest soils. Soil Biol Biochem 97:23–30
Lavrent’eva EV, Semenov AM, Zelenev VV, Chzhun Y, Semenova EV, Semenov VM, Namsaraev BB, Van Bruggen AHC (2009) Daily dynamics of cellulase activity in arable soils depending on management practices. Eurasian Soil Sci 42:885–893
Li Y, Yang T, Zhang P, Zou A, Peng X, Wang L, Yang R, Qi J, Yang Y (2012) Differential responses of the diazotrophic community to aluminum-tolerant and aluminum-sensitive soybean genotypes in acidic soil. Eur J Soil Biol 53:76–85
Li D, Voigt TB, Kent AD (2016) Plant and soil effects on bacterial communities associated with Miscanthus × giganteus rhizosphere and rhizomes. GCB Bioenergy 8:183–193
Lindsay EA, Colloff MJ, Gibb NL, Wakelin SA (2010) The abundance of microbial functional genes in grassy woodlands is influenced more by soil nutrient enrichment than by recent weed invasion or livestock exclusion. Appl Environ Microbiol 76:5547–5555
Liu H, Carvalhais LC, Crawford M, Singh E, Dennis PG, Pieterse CMJ, Schenk PM (2017) Inner plant values: diversity, colonization and benefits from endophytic bacteria. Front Microbiol 8:2552
Lu RK (1999) Soil and agricultural chemical analysis methods. Chinese Agriculture and Sciences Press, Beijing
Luo G, Ling N, Nannipieri P, Chen H, Raza W, Wang M, Guo S, Shen Q (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
Ma JF, Chen ZC, Shen RF (2014) Molecular mechanisms of Al tolerance in gramineous plants. Plant Soil 381:1–12
Magoč T, Salzberg SL (2011) FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27:2957–2963
Mirza BS, Potisap C, Nusslein K, Bohannan BJ, Rodrigues JL (2014) Response of free-living nitrogen-fixing microorganisms to land use change in the Amazon rainforest. Appl Environ Microbiol 80:281–288
Morrissey JP, Walsh UF, O’Donnell A, Moenne-Loccoz Y, O’Gara F (2002) Exploitation of genetically modified inoculants for industrial ecology applications. Antonie Van Leeuwenhoek 81:599–606
Nasto MK, Alvarez-Clare S, Lekberg Y, Sullivan BW, Townsend AR, Cleveland CC (2014) Interactions among nitrogen fixation and soil phosphorus acquisition strategies in lowland tropical rain forests. Ecol Lett 17:1282–1289
Olivares J, Bedmar EJ, Sanjuán J (2013) Biological nitrogen fixation in the context of global change. Mol Plant Microb Interact 26:486–494
Pereira e Silva MC, Schloter-Hai B, Schloter M, van Elsas JD, Salles JF (2013) Temporal dynamics of abundance and composition of nitrogen-fixing communities across agricultural soils. PLoS One 8:e74500
Pérez CA, Carmona MR, Armesto JJ (2010) Non-symbiotic nitrogen fixation during leaf litter decomposition in an old-growth temperate rain forest of Chiloé Island, southern Chile: Effects of single versus mixed species litter. Austral Ecol 35:148–156
Piñeros MA, Shaff JE, Manslank HS, Alves VMC, Kochian LV (2005) Aluminum resistance in maize cannot be solely explained by root organic acid exudation. A comparative physiological study. Plant Physiol 137:231–241
Prakamhang J, Minamisawa K, Teamtaisong K, Boonkerd N, Teaumroong N (2009) The communities of endophytic diazotrophic bacteria in cultivated rice (Oryza sativa L.). Appl Soil Ecol 42:141–149
Primieri S, Costa MD, Stroschein MRD, Stocco P, Santos JCP, Antunes PM (2016) Variability in symbiotic effectiveness of N2 fixing bacteria in Mimosa scabrella. Appl Soil Ecol 102:19–25
Randall K, Brennan F, Clipson N, Creamer R, Griffiths B, Storey S, Doyle E (2019) Soil bacterial community structure and functional responses across a long-term mineral phosphorus (Pi) fertilisation gradient differ in grazed and cut grasslands. Appl Soil Ecol 138:134–143
Reed SC, Seastedt TR, Mann CM, Suding KN, Townsend AR, Cherwin KL (2007) Phosphorus fertilization stimulates nitrogen fixation and increases inorganic nitrogen concentrations in a restored prairie. Appl Soil Ecol 36:238–242
Reed SC, Cleveland CC, Townsend AR (2011) Functional ecology of free-living nitrogen fixation: a contemporary perspective. Annu Rev Ecol Evol Syst 42:489–512
Reed SC, Cleveland CC, Townsend AR (2013) Relationships among phosphorus, molybdenum and free-living nitrogen fixation in tropical rain forests: results from observational and experimental analyses. Biogeochemistry 114:135–147
Rodríguez-Blanco A, Sicardi M, Frioni L (2015) Plant genotype and nitrogen fertilization effects on abundance and diversity of diazotrophic bacteria associated with maize (Zea mays L.). Biol Fertil Soils 51:391–402
Rosenblueth M, Martinez-Romero E (2006) Bacterial endophytes and their interactions with hosts. Mol Plant Microb Interact 19:827–837
Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541
Sims JR, Haby VA (1971) Simplified colorimetric determination of soil organic matter. Soil Sci 112:137–141
Smercina DN, Evans SE, Friesen ML, Tiemann LK (2019) To fix or not to fix: controls on free-living nitrogen fixation in the rhizosphere. Appl Environ Microbiol 85:e02546–e02518
Stanton DE, Batterman SA, Von Fischer JC, Hedin LO (2019) Rapid nitrogen fixation by canopy microbiome in tropical forest determined by both phosphorus and molybdenum. Ecology 100:e02795
Steenhoudt O, Vanderleyden J (2000) Azospirillum, a free-living nitrogen-fixing bacterium closely associated with grasses: genetic, biochemical and ecological aspects. FEMS Microbiol Rev 24:487–506
Tang Y, Zhang X, Li D, Wang H, Chen F, Fu X, Fang X, Sun X, Yu G (2016) Impacts of nitrogen and phosphorus additions on the abundance and community structure of ammonia oxidizers and denitrifying bacteria in Chinese fir plantations. Soil Biol Biochem 103:284–293
Tang Y, Yu G, Zhang X, Wang Q, Tian J, Niu S, Tian D, Ge J (2019) Different strategies for regulating free-living N2 fixation in nutrient-amended subtropical and temperate forest soils. Appl Soil Ecol 136:21–29
Villadas PJ, Fernandez-Lopez M, Ramirez-Saad H, Toro N (2007) Rhizosphere-bacterial community in Eperua falcata (Caesalpiniaceae) a putative nitrogen-fixing tree from French Guiana rainforest. Microb Ecol 53:317–327
Wang C, Zheng M, Song W, Wen S, Wang B, Zhu C, Shen R (2017) Impact of 25 years of inorganic fertilization on diazotrophic abundance and community structure in an acidic soil in southern China. Soil Biol Biochem 113:240–249
Wang C, Zheng MM, Hu AY, Zhu CQ, Shen RF (2018a) Diazotroph abundance and community composition in an acidic soil in response to aluminum-tolerant and aluminum-sensitive maize (Zea mays L.) cultivars under two nitrogen fertilizer forms. Plant Soil 424:463–478
Wang Q, Wang J, Li Y, Chen D, Ao J, Zhou W, Shen D, Li Q, Huang Z, Jiang Y (2018b) Influence of nitrogen and phosphorus additions on N2-fixation activity, abundance, and composition of diazotrophic communities in a Chinese fir plantation. Sci Total Environ 619–620:1530–1537
Wang C, Wu B, Jiang K, Wei M, Wang S (2019) Effects of different concentrations and types of Cu and Pb on soil N-fixing bacterial communities in the wheat rhizosphere. Appl Soil Ecol 144:51–59
Wei X, Hu Y, Razavi BS, Zhou J, Shen J, Nannipieri P, Wu J, Ge T (2019) Rare taxa of alkaline phosphomonoesterase-harboring microorganisms mediate soil phosphorus mineralization. Soil Biol Biochem 131:62–70
Wurzburger N, Bellenger JP, Kraepiel AML, Hedin LO (2012) Molybdenum and phosphorus interact to constrain asymbiotic nitrogen fixation in tropical forests. PLoS One 7:e33710
Yang L, Bai J, Zeng N, Zhou X, Liao Y, Lu Y, Rees RM, Nie J, Cao W (2019) Diazotroph abundance and community structure are reshaped by straw return and mineral fertilizer in rice-rice-green manure rotation. Appl Soil Ecol 136:11–20
Yu P, Wang C, Baldauf JA, Tai H, Gutjahr C, Hochholdinger F, Li C (2018) Root type and soil phosphate determine the taxonomic landscape of colonizing fungi and the transcriptome of field-grown maize roots. New Phytol 217:1240–1253
Zheng M, Li D, Lu X, Zhu X, Zhang W, Huang J, Fu S, Lu X, Mo J (2016) Effects of phosphorus addition with and without nitrogen addition on biological nitrogen fixation in tropical legume and non-legume tree plantations. Biogeochemistry 131:65–76
Acknowledgements
This work was financially supported by the National Key Research and Development Program of China (2018YFC1803100, 2016YFD0200302), and the Natural Science Foundation of China (41501328).
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Wang, C., Zheng, M.M. & Shen, R.F. Diazotrophic communities are more responsive to maize cultivation than phosphorus fertilization in an acidic soil. Plant Soil 452, 499–512 (2020). https://doi.org/10.1007/s11104-020-04596-z
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DOI: https://doi.org/10.1007/s11104-020-04596-z