Abstract
Fertilisers, especially nitrogen (N) and phosphorus (P) supplies, are frequently used in agricultural soil management to attain high crop yields. However, the intensive application of these chemical inputs can decrease the quality of agricultural soils and increase the probability of environmental pollution. In this study, the impact of P fertilisation on the diversity of the soil bacterial community was assessed. For this, a culture-independent approach targeting 16 rRNA and phoD genes was used on DNA extracted from pasture soils subjected to three different P fertilisation regimes for a long-term (42 years). As alkaline phosphomonoesterase (ALP) is necessary for mineralisation of organic P, an inverse relationship between the level of potential ALP activity and soil available P was expected. Indeed, a lower ALP activity was observed in soil subjected to higher chemical P fertiliser input. Analysis of the prevalence of three divergent families of ALP (PhoA, PhoD and PhoX) in metagenomic datasets revealed that PhoD is the most frequent ALP in soil samples and was selected as the most representative ALP possessed by the soil bacterial communities. Diversity of the phoD phosphorus mineraliser group, as well as the total bacterial community, was both increased in response to long-term P fertilisation. Specifically, phosphorus fertilisation decreased the relative abundance of certain taxa, including Acidobacteria and Pseudomonas fluorescens. In conclusion, this study shows that P fertilisation affects the microbial diversity of soil ecosystems, which might potentially modulate the soil biogeochemical cycle.
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References
Anisimova M, Gascuel O (2006) Approximate likelihood-ratio test for branches: a fast, accurate, and powerful alternative. Syst Biol 55:539–552
Barret M, Morrissey JP, O'Gara F (2011) Functional genomics analysis of plant growth-promoting rhizobacterial traits involved in rhizosphere competence. Biol Fertil Soils 47:729–743
Berg G, Smalla K (2009) Plant species and soil type cooperatively shape the structure and function of microbial communities in the rhizosphere. FEMS Microbiol Ecol 68:1–13
Browne P, Rice O, Miller SH, Burke J, Dowling DN, Morrissey JP, O’Gara F (2009) Superior inorganic phosphate solubilization is linked to phylogeny within the Pseudomonas fluorescens complex. Appl Soil Ecol 43:131–138
Carrigg C, Rice O, Kavanagh S, Collins G, O’Flaherty (2007) DNA extraction method affects microbial community profiles from soils and sediment. Appl Microbiol Biotechnol 77:955–964
Chhabra S, Brazil D, Morrissey JP, Burke J, O'Gara F, Dowling D (2012) Fertilization management affects the alkaline phosphatase bacterial community in barley rhizosphere soil. Biol Fertil Soils (in press)
Chu H, Lin X, Fujii T, Morimoto S, Yagi K, Hu J, Zhang J (2007) Soil microbial biomass, dehydrogenase activity, bacterial community structure in response to long-term fertilizer management. Soil Biol Biochem 39:2971–2976
Culleton N, Coulter B, Liebhardt WC (2002) The fate of phosphatic fertiliser applied to grassland. Ir Geogr 35:175–184
Culleton N, Liebhardt W, Murphy W, Cullen J, Cuddihy A (2000) Thirty years of phosphorus fertiliser on Irish pastures: animal–soil–water relationships. Teagasc, Dublin
Drozd M, Gangaiah D, Liu Z, Rajashekara G (2011) Contribution of TAT system translocated PhoX to Campylobacter jejuni phosphate metabolism and resilience to environmental stresses. PLoS One 6:e26336
Eder S, Shi L, Jensen K, Yamane K, Hulett FM (1996) A Bacillus subtilis secreted phosphodiesterase/alkaline phosphatase is the product of a Pho regulon gene, phoD. Microbiology 142:2041–2047
Fierer N, Lauber CL, Ramirez KS, Zaneveld J, Bradford MA, Knight R (2012) Comparative metagenomic, phylogenetic and physiological analyses of soil microbial communities across nitrogen gradients. ISME J 6:1007–1017
Galperin MY, Jedrzejas MJ (2001) Conserved core structure and active site residues in alkaline phosphatase superfamily enzymes. Proteins 45:318–324
Ge Y, Zhang J, Zhang L, Yang M, He J (2008) Long-term fertilization regimes affect bacterial community structure and diversity of an agricultural soil in northern China. J Soils Sed 8:43–50
Goulding K, Jarvis S, Whitmore A (2008) Optimizing nutrient management for farm systems. Philos Trans R Soc Lond B Biol Sci 363:667–680
Griffiths BS, Spilles A, Bonkowski M (2012) C:N:P stoichiometry and nutrient limitation of the soil microbial biomass in a grazed grassland site under experimental P limitation or excess. Ecol Process 1:6
Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704
Hasegawa M, Kishino H, Yano TA (1985) Dating of the human ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol 22:160–174
Hayat R, Ali S, Amara U, Khalid R, Ahmed I (2010) Soil beneficial bacteria and their role in plant growth promotion: a review. Ann Microbiol 60:579–598
İnceoğlu Ö, Al-Soud WA, Salles JF, Semenov AV, Van Elsas JD (2011) Comparative analysis of bacterial communities in a potato field as determined by pyrosequencing. PLoS One 6:e23321
Jones RT, Robeson MS, lauber CL, Hamady M, Knight R, Fierer N (2009) A comprehensive survey of soil acidobacterial diversity using pyrosequencing and clone library analyses. ISME J 3:442–453
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
Kamat SS, Williams HJ, Raushel FM (2011) Intermediates in the transformation of phosphonates to phosphate by bacteria. Nature 480:570–573
Karandashov V, Bucher M (2005) Symbiotic phosphate transport in arbuscular mycorrhizas. Trends Plant Sci 10:22–29
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
Katoh K, Toh H (2008) Recent developments in the MAFFT multiple sequence alignment program. Brief Bioinform 9:286–298
King-Salter GE (2008) Response of arbuscular mycorrhizal fungi to seasonality and long-term phosphorus fertilisation in an Irish grazed grassland. Ph.D. thesis, University College Dublin, Dublin
Kirk GJD (1999) A model of phosphate solubilization by organic anion excretion from plant roots. Eur J Soil Sci 50:369–378
Letunic I, Bork P (2011) Interactive Tree Of Life v2: online annotation and display of phylogenetic trees made easy. Nucleic Acids Res 39:W475–W478
Liu L, Gundersen P, Zhang T, Mo J (2012) Effects of phosphorus addition on soil microbial biomass and community composition in three forest types in tropical China. Soil Biol Biochem 44:31–38
Luo H, Benner R, Long RA, Hu J (2009) Subcellular localization of marine bacterial alkaline phosphatases. Proc Nat Acad Sci USA 106:21219–21223
Mao Y, Yannarell AC, Mackie RI (2011) Changes in N-transforming archaea and bacteria in soil during the establishment of bioenergy crops. PLoS One 6:e24750
Markowitz VM, Ivanova NN, Szeto E, Palaniappan K, Chu K, Dalevi D, Chen IMA, Grechkin Y, Dubchak I, Anderson I, Lykidis A, Mavromatis K, Hugenholtz P, Kyrpides NC (2008) IMG/M: a data management and analysis system for metagenomes. Nucleic Acids Res 36:D534–D538
Miller SH, Browne P, Prigent-Combaret C, Combes-Meynet E, Morrissey JP, O'Gara F (2010) Biochemical and genomic comparison of inorganic phosphate solubilization in Pseudomonas species. Environ Microbiol Rep 2:403–411
Monds RD, Newell PD, Schwartzman JA, O'Toole GA (2006) Conservation of the Pho regulon in Pseudomonas fluorescens Pf0-1. Appl Environ Microbiol 72:1910–1924
Morrissey JP, Dow JM, Mark GL, O'Gara F (2004) Are microbes at the root of a solution to world food production? EMBO Rep 5:922–926
Nacke H, Thuermer A, Wollherr A, Will C, Hodac L, Herold N, Schoening I, Schrumpf M, Daniel R (2011) Pyrosequencing-based assessment of bacterial community structure along different management types in German forest and grassland soils. PLoS One 6:e17000
Nannipieri P, Ascher J, Ceccherini MT, Landi L, Pietramellara G, Renella G (2003) Microbial diversity and soil functions. Eur J Soil Sci 54:655–670
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, vol 100, Soil biology. Springer, Berlin, pp 215–241
Palmer K, Drake HL, Horn MA (2009) Genome-derived criteria for assigning environmental narG and nosZ sequences to operational taxonomic units of nitrate reducers. Appl Environ Microbiol 75:5170–5174
Pennanen T, Perkiömäki J, Kiikkilä O, Vanhala P, Neuvonen S, Fritze H (1998) Prolonged, simulated acid rain and heavy metal deposition: separated and combined effects on forest soil microbial community structure. Microbiol Ecol 27:291–300
Philippot L, Hallin S (2005) Finding the missing link between diversity and activity using denitrifying bacteria as a model functional community. Curr Opin Microbiol 8:234–239
Rice O, Miller S, Morrissey J, O’Gara F (2012) Exploitation of glucose catabolic gene fusions to investigate in situ expression during Pseudomonas–plant interactions. Biol Fertil Soils 48:235–238
Richardson AE, Barea J-M, 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
Richardson AE, Simpson RJ (2011) Soil microorganisms mediating phosphorus availability. Plant Physiol 156:989–996
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
Roesch LF, Fulthorpe RR, Riva A, Casella G, Hadwin AKM, Kent AD, Daroub SH, Camargo FAO, Farmerie WG, Triplett EW (2007) Pyrosequencing enumerates and contrasts soil microbial diversity. ISME J 1:283–290
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
Schloss PD, Handelsman J (2006) Toward a census of bacteria in soil. PLoS Comput Biol 2:e92
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
Sebastian M, Ammerman JW (2011) Role of the phosphatase PhoX in the phosphorus metabolism of the marine bacterium Ruegeria pomeroyi DSS-3. Environ Microbiol Rep 3:535–542
Smalla K, Wieland G, Buchner A, Zock A, Parzy J, Kaiser S, Roskot N, Heuer H, Berg G (2001) Bulk and rhizosphere soil bacterial communities studied by denaturing gradient gel electrophoresis: plant-dependent enrichment and seasonal shifts revealed. Appl Environ Microbiol 67:4742–4751
Tabatabai MA, Bremner JM (1969) Use of p-nitrophenyl phosphate for assay of soil phosphatase activity. Soil Biol Biochem 1:301–307
Tilman D, Cassman KG, Matson PA, Naylor R, Polasky S (2002) Agricultural sustainability and intensive production practices. Nature 418:671–677
Uroz S, Buée M, Murat C, Frey-Klett P, Martin F (2010) Pyrosequencing reveals a contrasted bacterial diversity between oak rhizosphere and surrounding soil. Environ Microbiol Rep 2:281–288
Uroz S, Calvaruso C, Turpault M-P, Frey-Klett P (2009) Mineral weathering by bacteria: ecology, actors and mechanisms. Trends Microbiol 17:378–387
Van Aarle IM, Plassard C (2010) Spatial distribution of phosphatase activity associated with ectomycorrhizal plants is related to soil type. Soil Biol Biochem 42:324–330
Whelan S, Goldman N (2001) A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. Mol Biol Evol 18:691–699
Wu JR, Shien JH, Shieh HK, Hu CC, Gong SR, Chen LY, Chang PC (2007) Cloning of the gene and characterization of the enzymatic properties of the monomeric alkaline phosphatase (PhoX) from Pasteurella multocida strain X-73. FEMS Microbiol Lett 267:113–120
Yamane K, Maruo B (1978) Purification and characterization of extracellular soluble and membrane-bound insoluble alkaline phosphatases possessing phosphodiesterase activities in Bacillus subtilis. J Bacteriol 134:100–107
Yao MZ, Zhang YH, Lu WL, Hu MQ, Wang W, Liang AH (2012) Phytases: crystal structures, protein engineering and potential biotechnological applications. J Appl Microbiol 112:1–14
Zaheer R, Morton R, Proudfoot M, Yakunin A, Finan TM (2009) Genetic and biochemical properties of an alkaline phosphatase PhoX family protein found in many bacteria. Environ Microbiol 11:1572–1587
Zhong WH, Cai ZC (2007) Long-term effects of inorganic fertilizers on microbial biomass and community functional diversity in a paddy soil derived from quaternary red clay. Appl Soil Ecol 36:84–91
Acknowledgments
This research was supported in part by grants awarded by the Science Foundation of Ireland (04/BR/B0597, 07/IN.1/B948, 07/SK/B1236b, 08/RFP/GEN1319, 08/RFP/GEN1295, SFI09/RFP/BMT 2350); the Department of Agriculture, Fisheries and Food (DAF RSF 06-321, DAF RSF 06-377, FIRM 08/RDC/629); the Environmental Protection Agency (EPA 2006-PhD-S-21, EPA 2008-PhD-S-2), the Irish Research Council for Science, Engineering and Technology (IRC EMBARK PD/2011/2414), the European Commission (FP6#036314, MTKD-CT2006-042062, TRAMWAYS, MicroB3-287589-OCEAN2012, MACUMBA-CP-TP 311975; PharmaSea-CP-TP 312184, EU 256596); and the Marine Institute (Beaufort award - C&CRA 2007/082) and the HRB (RP/2006/271, RP/2007/290, HRA/2009/146). The authors would like to acknowledge the Boole Centre for Research in Informatics at University College Cork for providing access to computational facilities.
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Tan, H., Barret, M., Mooij, M.J. et al. 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 (2013). https://doi.org/10.1007/s00374-012-0755-5
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DOI: https://doi.org/10.1007/s00374-012-0755-5