Abstract
Abundant phosphorus (P) has been applied to paddy fields in the red soil region of subtropical China. Microbial communities play important roles in soil nutrient cycling; however, the effects of P surplus on soil microbial diversity and community composition are still unclear. Soils collected from paddy fields in subtropical China was incubated and subjected to four P treatments: 33 kg ha−1 (CK), 66 kg ha−1 (P1), 132 kg ha−1 (P2), and 264 kg ha−1 (P3). Changes in bacterial and fungal diversity and community composition were evaluated by high-throughput sequencing. The different P rates had no significant effect on bacterial diversity, whereas fungal richness and diversity indexes declined significantly by increasing P rates. Principle coordinate analysis (PCoA) also indicated a shift in fungal community composition when P rates were higher than 132 kg ha−1. Available P (AP) was the dominant factor affecting fungal community composition as evaluated by canonical correspondence analysis (CCA). Multivariate regression trees (MRT) revealed that the key threshold of 53.6 mg kg−1 of AP divided treatments into two distinct groups. Linear discriminant analysis effect size (LEfSe) showed that abundances of Pseudogymnoascus and Geomyces increased, but those of Penicillium and an unknown genus of Trichocomaceae decreased when AP was ≥ 53.6 mg kg−1.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Arenza BE, Helda BW, Jurgensa JA, Farrellb RL, Blanchette RA (2006) Fungal diversity in soils and historic wood from the Ross Sea Region of Antarctica. Soil Biol Biochem 38(10):3057–3064. https://doi.org/10.1016/j.soilbio.2006.01.016
Beauregard MS, Atul-Nayyar CH, St-Arnaud M (2010) Long-term phosphorus fertilization impacts soil fungal and bacterial diversity but not AM fungal community in alfalfa. Microb Ecol 59(2):379–389. https://doi.org/10.1007/s00248-009-9583-z
Bouwman AF, Beusen AHW, Billen G (2009) Human alteration of the global nitrogen and phosphorus soil balances for the period 1970–2050. Global Biogeochem Cy 23:GB0A04
Bouwman L, Goldewijk KK, Hoek KWVD, Beusen AHW, Vuuren DPV, Willems J, Rufino MC, Stehfest E (2013) Exploring global changes in nitrogen and phosphorus cycles in agriculture induced by livestock production over the 1900–2050 period. P Natl Acad Sci USA 110(52):20882–20887. https://doi.org/10.1073/pnas.1012878108
Brookes PC, Powlsen DS, Jenkinson DS (1982) Measurement of microbial biomass phosphorus in soil. Soil Biol Biochem 14(4):319–329. https://doi.org/10.1016/0038-0717(82)90001-3
Brussaard L, Ruiter PC, Brown GG (2007) Soil biodiversity for agricultural sustainability. Agric Ecosyst Environ 121(3):233–244. https://doi.org/10.1016/j.agee.2006.12.013
Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Tanya Y, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7(5):335–336. https://doi.org/10.1038/nmeth.f.303
Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Lozupone CA, Turnbaugh PJ, Fierer N, Knight R (2011) Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. P Natl Acad Sci USA 108(Supplement_1):4516–4522. https://doi.org/10.1073/pnas.1000080107
Ceulemans T, Stevens CJ, Duchateau L, Jacquemyn H, Gowing DJG, Merckx R, Wallace H, Rooijen NV, Goethem T, Bobbink R, Dorland E, Gaudnik C, Alard D, Corcket E, Muller S, Dise NB, Dupre C, Diekmann M, Honnay O (2014) Soil phosphorus constrains biodiversity across European grasslands. Glob Chang Biol 20(12):3814–3822. https://doi.org/10.1111/gcb.12650
Chen C, Zhang JN, Lu M, Qin C, Chen YH, Yang L, Huang QW, Wang JC, Shen ZG, Shen QR (2016) Microbial communities of an arable soil treated for 8 years with organic and inorganic fertilizers. Biol Fert Soils 52(4):455–467. https://doi.org/10.1007/s00374-016-1089-5
Chhabra S, Brazil D, Morrissey J, Burke J, O’Gara F, Dowling DN (2013) Fertilization management affects the alkaline phosphatase bacterial community in barley rhizosphere soil. Biol Fert Soils 49(1):31–39. https://doi.org/10.1007/s00374-012-0693-2
Cleveland C, Townsend AR, Taylor P, Alvarez-Clare S, Bustamante MMC, Chuyong G, Dobrowski SZ, Grierson P, Harms KE, Houlton BZ, Marklein A, Parton W, Porder S, Reed SC, Sierra CA, Silver WL, Tanner EV, Wieder WR (2011) Relationships among net primary productivity, nutrients and climate in tropical rain forest: a pan-tropical analysis. Ecol Lett 14(9):939–947. https://doi.org/10.1111/j.1461-0248.2011.01658.x
Crowther TW, Boddy L, Jones TH (2011) Outcomes of fungal interactions are determined by soil invertebrate grazers. Ecol Lett 14(11):1134–1142. https://doi.org/10.1111/j.1461-0248.2011.01682.x
Daynes CM, Mcgee PA, Midgley DJ (2008) Utilisation of plant cell-wall polysaccharides and organic phosphorus substrates by isolates of Aspergillus and Penicillium isolated from soil. Fungal Ecol 1(2-3):94–98. https://doi.org/10.1016/j.funeco.2008.09.001
De’Ath G (2002) Multivariate regression trees: a new technique for modeling species-environment relationships. Ecology 83:1105–1117
Docampo R, Ulrich P, Moreno SNJ (2010) Evolution of acidocalcisomes and their role in polyphosphate storage and osmoregulation in eukaryotic microbes. Philos T R Soc B 365(1541):775–784. https://doi.org/10.1098/rstb.2009.0179
Ezawa T, Cavagnaro TR, Smith SE, Smith FA, Ohtomo R (2003) Rapid accumulation of polyphosphate in extraradical hyphae of an arbuscular mycorrhizal fungus as revealed by histochemistry and a polyphosphate kinase/luciferase system. New Phytol 161:387–392
Ezawa T, Smith SE, Smith FA (2002) P metabolism and transport in AM fungi. Plant Soil 244(1/2):221–230. https://doi.org/10.1023/A:1020258325010
Gómez-Muñoz B, Pittroff SM, Ad N, Jensen LS, Nicolaisen MH, Magid J (2017) Penicillium bilaii effects on maize growth and P uptake from soil and localized sewage sludge in a rhizobox experiment. Biol Fert Soils 53(1):23–35. https://doi.org/10.1007/s00374-016-1149-x
Hammel K (1997) Fungal degradation of lignin. In: Cadisch G (ed) Driven by nature: plant litter quality and decomposition. CAB International, Wallingford, pp 33–45
Hamel C, Hanson K, Selles F, Cruz AF, Lemke R, McConkey B, Zentner R (2006) Seasonal and long-term resource-related variations in soil microbial communities in wheat-based rotations of the Canadian prairie. Soil Biol Biochem 38(8):2104–2116. https://doi.org/10.1016/j.soilbio.2006.01.011
He JZ, Zheng Y, Chen CR, He YQ, Zhang LM (2008) Microbial composition and diversity of an upland red soil under long-term fertilization treatments as revealed by culture-dependent and culture-independent approaches. J Soils Sediments 8(5):349–358. https://doi.org/10.1007/s11368-008-0025-1
He D, Xiang XJ, He JS, Wang C, Cao GM, Adams J, Chu HY (2016) Composition of the soil fungal community is more sensitive to phosphorus than nitrogen addition in the alpine meadow on the Qinghai-Tibetan Plateau. Biol Fert Soils 52(8):1059–1072. https://doi.org/10.1007/s00374-016-1142-4
Huang J, Hu B, Qi K, Chen W, Pang X, Bao W, Tian G (2016) Effects of phosphorus addition on soil microbial biomass and community composition in a subalpine spruce plantation. Eur J Soil Biol 72:35–41. https://doi.org/10.1016/j.ejsobi.2015.12.007
Illmer P, Barbato A, Schinner F (1995) Solubilization of hardly-soluble AlPO4 with P-solubilizing microorganisms. Soil Biol Biochem 27(3):265–270. https://doi.org/10.1016/0038-0717(94)00205-F
Jia JX, Li ZP, Liu M, Che YP (2010) Effects of glucose addition on N transformations in paddy soils with a gradient of organic C content in subtropical China. Agr Sci China 9(9):1309–1316. https://doi.org/10.1016/S1671-2927(09)60222-4
Khan KS, Joergensen RG (2012) Relationships between P fractions and the microbial biomass in soils under different land use management. Geoderma 173-174:274–281. https://doi.org/10.1016/j.geoderma.2011.12.022
Kuramae E, Gamper H, Jv V, Kowalchuk G (2011) Soil and plant factors driving the community of soil-borne microorganisms across chronosequences of secondary succession of chalk grasslands with a neutral pH. FEMS Microbiol Ecol 77(2):285–294. https://doi.org/10.1111/j.1574-6941.2011.01110.x
Kwasna H (2001) Fungi in the rhizosphere of common oak and its stumps and their possible effect on infection by Armillaria. Appl Soil Ecol 17(3):215–227. https://doi.org/10.1016/S0929-1393(01)00137-8
Kwasna H (2004) Natural shifts in communities of rhizosphere fungi of common oak after felling. Plant Soil 264(1/2):209–218. https://doi.org/10.1023/B:PLSO.0000047752.41575.c7
Lagos LM, Acuña JJ, Maruyama F, Ogram A, Mora ML, Jorquera MA (2016) Effect of phosphorus addition on total and alkaline phosphomonoesterase-harboring bacterial populations in ryegrass rhizosphere microsites. Biol Fert Soils 52(7):1007–1019. https://doi.org/10.1007/s00374-016-1137-1
Lauber CL, Strickland MS, Bradford MA, Fierer N (2008) The influence of soil properties on the structure of bacterial and fungal communities across land-use types. Soil Biol Biochem 40(9):2407–2415. https://doi.org/10.1016/j.soilbio.2008.05.021
Li J, Li Z, Wang F, Zou B, Chen Y, Zhao J, Mo Q, Li Y, Li X, Xia H (2015) Effects of nitrogen and phosphorus addition on soil microbial community in a secondary tropical forest of China. Biol Fert Soils 51(2):207–215. https://doi.org/10.1007/s00374-014-0964-1
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(1):31–38. https://doi.org/10.1016/j.soilbio.2011.08.017
Liu L, Zhang T, Gilliam FS, Gundersen P, Zhang W, Chen H, Mo J (2013) Interactive effects of nitrogen and phosphorus on soil microbial communities in a tropical forest. PLoS One 8(4):e61188. https://doi.org/10.1371/journal.pone.0061188
Lin XG, Feng YZ, Zhang HY, Chen RR, Wang JH, Zhang JB, Chu HY (2012) Long-term balanced fertilization decreases arbuscular mycorrhizal fungal diversity in an arable soil in North China revealed by 454 pyrosequencing. Environ Sci Technol 46(11):5764–5771. https://doi.org/10.1021/es3001695
Lu R, Shi Z, Shi J (2000) Nutrient balance of agroecosystem in six provinces in southern China. Sci Agr Sin 33:63–67
Malý S, Královec J, Hampel D (2009) Effects of long-term mineral fertilization on microbial biomass, microbial activity, and the presence of r- and K-strategists in soil. Biol Fert Soils 45(7):753–760. https://doi.org/10.1007/s00374-009-0388-5
Pansu M, Gautheyrou J (2006) Handbook of soil analysis: mineralogical, organic and inorganic methods. Springer, Berlin Heidelberg, Berlin. https://doi.org/10.1007/978-3-540-31211-6
Rice WA, Olsen PE, Leggett ME (1994) Co-culture of rhizobium meliloti and a phosphorus-solubilizing fungus (Penicillium bilaii) in sterile peat. Soil Biol Biochem 27:703–705
Ryazanova LP, Suzina NE, Kulakovskaya TV (2009) Phosphate accumulation of Acetobacter xylinum. Arch Microbiol 191(5):467–471. https://doi.org/10.1007/s00203-009-0470-2
Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS, Huttenhower C (2011) Metagenomic biomarker discovery and explanation. Genome Biol 12(6):R60. https://doi.org/10.1186/gb-2011-12-6-r60
Schachtman DP, Reid RJ, Ayling SM (1998) Phosphorus uptake by plants: from soil to cell. Plant Physiol 116(2):447–453. https://doi.org/10.1104/pp.116.2.447
Schmidt P, Bálint M, Greshake B, Bandow C, Römbke J, Schmitt I (2013) Illumina metabarcoding of a soil fungal community. Soil Biol Biochem 65:128–132. https://doi.org/10.1016/j.soilbio.2013.05.014
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
Siciliano SD, Palmer AS, Winsley T, Lamb E, Bissett A, Brown MV, Dorst J, Ji M, Ferrari BC, Grogan P, Chu H, Snape I (2014) Soil fertility is associated with fungal and bacterial richness, whereas pH is associated with community composition in polar soil microbial communities. Soil Biol Biochem 78:10–20. https://doi.org/10.1016/j.soilbio.2014.07.005
Sigler L, Lumley TC, Currah RS (2000) New species and records of saprophytic ascomycetes (Myxotrichaceae) from decaying logs in the boreal forest. Mycoscience 41(5):495–502. https://doi.org/10.1007/BF02461670
Tan H, Barret M, Mooij MJ, Rice O, Morrissey JP, 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. Biol Fert Soils 49(6):661–672. https://doi.org/10.1007/s00374-012-0755-5
Thirukkumaran CM, Parkinson D (2000) Microbial respiration, biomass, metabolic quotient and litter decomposition in a lodgepole pine forest floor amended with nitrogen and phosphorous fertilizers. Soil Biol Biochem 32(1):59–66. https://doi.org/10.1016/S0038-0717(99)00129-7
Wakelin SA, Condron LM, Gerard E, Dignam BEA, Black A, O’Callaghan M (2017) Long-term P fertilisation of pasture soil did not increase soil organic matter stocks but increased microbial biomass and activity. Biol Fert Soils 53(5):511–521. https://doi.org/10.1007/s00374-017-1212-2
Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microb 73(16):5261–5267. https://doi.org/10.1128/AEM.00062-07
White T, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis M, Gelfand D, Shinsky J, White T (eds) PCR protocols: a guide to methods and applications. Academic Press, San Diego, pp 315–322
Zhang B, Li G (1998) Roles of soil organisms on the enhancement of plant availability of soil phosphorus. Acta Pedol Sin 35:104–111
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(2-3):84–91. https://doi.org/10.1016/j.apsoil.2006.12.001
Acknowledgements
The present study was funded by the National Basic Research Program of China [grant 2014CB441003], the National Nature Science Foundation of China [grant 41201242], and the “135” plan and field frontier project [grant ISSASIP1642].
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
ESM 1
(DOCX 13 kb)
Rights and permissions
About this article
Cite this article
Liu, M., Liu, J., Chen, X. et al. Shifts in bacterial and fungal diversity in a paddy soil faced with phosphorus surplus. Biol Fertil Soils 54, 259–267 (2018). https://doi.org/10.1007/s00374-017-1258-1
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00374-017-1258-1