Skip to main content

Advertisement

SpringerLink
Log in

Fertilization with inorganic and organic nutrients changes diazotroph community composition and N-fixation rates

  • Soils, Sec 5 • Soil and Landscape Ecology • Research Article
  • Published:
Journal of Soils and Sediments Aims and scope Submit manuscript

Abstract

Purpose

Nitrogen fixation by free-living diazotrophs from the atmosphere is an important pathway for nitrogen input into the soil. However, there is little information regarding soil diazotrophic community composition and diversity under long-term fertilization in rice paddy ecosystems.

Materials and methods

Using the 15N2-tracing method and nifH gene as a molecular marker, we investigated the abundance, structure, and activity of soil diazotrophic community in soil at a 30-year-old filed experimental site treated with four different fertilizer management practices: control (non-fertilization), chemical NPK fertilizers, NPK plus rice straw (NPK+RS), or NPK plus chicken manure (NPK+OM).

Results and discussion

Among all the treatments, the NPK+OM treatment significantly improved the soil nutritional status. Fertilization increased both bacteria and nifH gene abundances, with the highest values (p < 0.05) found in the NPK+OM treatment. The potential nitrogen fixation rate ranged from 14.6 to 118 μg kg−1 day−1, and the highest rates (p < 0.05) were also observed in the NPK+OM treatment. Long-term chemical NPK fertilization decreased the diversity of diazotrophic community, whereas NPK+RS and NPK+OM treatments maintained the diversity of diazotrophic community. Long-term fertilization changed diazotrophic community as compared to non-fertilization, but there were no significant differences among fertilized treatments. Most nifH sequences were closely linked to Alphaproteobacteria, which was dominated by the genera Bradyrhizobium. Relatively higher Cyanobacteria abundances were observed in the unfertilized soil as compared with fertilized soil.

Conclusions

Our results suggest that long-term fertilization increased the abundance of diazotrophs and changed their community structure, and combined use of chicken manure and chemical NPK fertilizers can significantly improve the activity of diazotrophic community.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Bahulikar RA, Torres-Jerez I, Worley E, Craven K, Udvardi MK (2014) Diversity of nitrogen-fixing bacteria associated with switchgrass in the native tallgrass prairie of Northern Oklahoma. Appl Environ Microbiol 80:5636–5643

    Article  Google Scholar 

  • Bei Q, Liu G, Tang H, Cadisch G, Rasche F, Xie Z (2013) Heterotrophic and phototrophic 15N2 fixation and distribution of fixed 15N in a flooded rice–soil system. Soil Biol Biochem 59:25–31

    Article  CAS  Google Scholar 

  • Berthrong ST, Yeager CM, Gallegos-Graves L, Steven B, Eichorst SA, Jackson RB, Kuske CR (2014) Nitrogen fertilization has a stronger effect on soil nitrogen-fixing bacterial communities than elevated atmospheric CO2. Appl Environ Microbiol 80:3103–3112

    Article  Google Scholar 

  • Biddle JF, Fitz-Gibbon S, Schuster SC, Brenchley JE, House CH (2008) Metagenomic signatures of the Peru Margin subseafloor biosphere show a genetically distinct environment. Proc Natl Acad Sci U S A 105:10583–10588

    Article  CAS  Google Scholar 

  • Boddey RM, de Oliveira OC, Urquiaga S, Reis VM, de Olivares FL, VLD B, Döbereiner J (1995) Biological nitrogen fixation associated with sugar cane and rice: contributions and prospects for improvement. In: Ladha JK, Peoples MB (eds) Management of biological nitrogen fixation for the development of more productive and sustainable agricultural systems: extended versions of papers presented at the Symposium on Biological Nitrogen Fixation for Sustainable Agriculture at the 15th Congress of Soil Science, Acapulco, Mexico, 1994. Springer Netherlands, Dordrecht, pp 195–209

  • Buckley DH, Huangyutitham V, Hsu S-F, Nelson TA (2008) 15N2–DNA–stable isotope probing of diazotrophic methanotrophs in soil. Soil Biol Biochem 40:1272–1283

    Article  CAS  Google Scholar 

  • Chaintreuil C, Giraud E, Prin Y, Lorquin J, Bâ A, Gillis M, de Lajudie P, Dreyfus B (2000) Photosynthetic bradyrhizobia are natural endophytes of the African wild rice Oryza breviligulata. Appl Environ Microbiol 66:5437–5447

    Article  CAS  Google Scholar 

  • Chinnadurai C, Gopalaswamy G, Balachandar D (2014) Long term effects of nutrient management regimes on abundance of bacterial genes and soil biochemical processes for fertility sustainability in a semi-arid tropical Alfisol. Geoderma 232-234:563–572

    Article  CAS  Google Scholar 

  • Demba Diallo M, Willems A, Vloemans N, Cousin S, Vandekerckhove TT, De Lajudie P, Neyra M, Vyverman W, Gillis M, Van der Gucht K (2004) Polymerase chain reaction denaturing gradient gel electrophoresis analysis of the N2-fixing bacterial diversity in soil under Acacia tortilis ssp. raddiana and Balanites aegyptiaca in the dryland part of Senegal. Environ Microbiol 6:400–415

    Article  Google Scholar 

  • Diez B, Bergman B, Pedros-Alio C, Anto M, Snoeijs P (2012) High cyanobacterial nifH gene diversity in Arctic seawater and sea ice brine. Env Microbiol Rep 4:360–366

    Article  CAS  Google Scholar 

  • Dixon R, Kahn D (2004) Genetic regulation of biological nitrogen fixation. Nat Rev Microbiol 2:621–631

    Article  CAS  Google Scholar 

  • Estrella Alcaman M, Fernandez C, Delgado A, Bergman B, Diez B (2015) The cyanobacterium Mastigocladus fulfills the nitrogen demand of a terrestrial hot spring microbial mat. ISME J 9:2290–2303

    Article  CAS  Google Scholar 

  • Ferrando L, Fernandez Scavino A (2015) Strong shift in the diazotrophic endophytic bacterial community inhabiting rice (Oryza sativa) plants after flooding. FEMS Microbiol Ecol 91:fiv104

  • Fuentes-Ramírez LE, Caballero-Mellado J, Sepúlveda J, Martínez-Romero E (1999) Colonization of sugarcane by Acetobacter diazotrophicus is inhibited by high N-fertilization. FEMS Microbiol Ecol 29:117–128

    Article  Google Scholar 

  • Ge Y, Priester JH, Mortimer M, Chang CH, Ji Z, Schimel JP, Holden PA (2016) Long-term effects of multiwalled carbon nanotubes and graphene on microbial communities in dry soil. Environ Sci Technol 50:3965–3974

    Article  CAS  Google Scholar 

  • Gonzalez Perez P, Ye J, Wang S, Wang X, Huang D (2014) Analysis of the occurrence and activity of diazotrophic communities in organic and conventional horticultural soils. Appl Soil Ecol 79:37–48

    Article  Google Scholar 

  • Hai B, Diallo NH, Sall S, Haesler F, Schauss K, Bonzi M, Assigbetse K, Chotte JL, Munch JC, Schloter M (2009) Quantification of key genes steering the microbial nitrogen cycle in the rhizosphere of sorghum cultivars in tropical agroecosystems. Appl Environ Microbiol 75:4993–5000

    Article  CAS  Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT, Nucleic acids symposium series, vol c1979-c2000. Information Retrieval Ltd, London, pp 95–98

    Google Scholar 

  • Hsu SF, Buckley DH (2009) Evidence for the functional significance of diazotroph community structure in soil. ISME J 3:124–136

    Article  CAS  Google Scholar 

  • Hui T (2012) Effects of long-term fertilization on nifH gene diversity in agricultural black soil. Afr J of Microbiol Res 6:2695–2666

    Google Scholar 

  • Izquierdo JA, Klaus N (2015) Variation in diazotrophic community structure in forest soils reflects land use history. Soil Biol Biochem 80:1–8

    Article  CAS  Google Scholar 

  • Keuter A, Veldkamp E, Corre MD (2014) Asymbiotic biological nitrogen fixation in a temperate grassland as affected by management practices. Soil Biol Biochem 70:38–46

    Article  CAS  Google Scholar 

  • Ladha JK, Reddy PM (2003) Nitrogen fixation in rice systems: state of knowledge and future prospects. Plant Soil 252:151–167

    Article  CAS  Google Scholar 

  • Ladha JK, de Bruijn FJ, Malik KA (1997) Introduction: assessing opportunities for nitrogen fixation in rice—a frontier project. Plant Soil 194:1–10

    Article  CAS  Google Scholar 

  • Lema KA, Willis BL, Bourne DG (2012) Corals form characteristic associations with symbiotic nitrogen-fixing bacteria. Appl Environ Microbiol 78:3136–3144

    Article  CAS  Google Scholar 

  • Liang Y, Pan F, He X, Chen X, Su Y (2016) Effect of vegetation types on soil arbuscular mycorrhizal fungi and nitrogen-fixing bacterial communities in a karst region. Environ Sci Pollut R 23:18482–18491

    Article  CAS  Google Scholar 

  • Maclean JL (2002) Rice almanac: source book for the most important economic activity on earth. International Rice Research Institute, Laguna

    Book  Google Scholar 

  • Mårtensson L, Díez B, Wartiainen I, Zheng W, El-Shehawy R, Rasmussen U (2009) Diazotrophic diversity, nifH gene expression and nitrogenase activity in a rice paddy field in Fujian, China. Plant Soil 325:207–218

    Article  Google Scholar 

  • Mirza BS, Potisap C, Nüsslein K, Bohannan BJM, Rodrigues JLM (2013) Response of free-living nitrogen-fixing microorganisms to land use change in the Amazon rainforest. Appl Environ Microbiol 80:281–288

    Article  Google Scholar 

  • Okubo T et al (2012) Complete genome sequence of Bradyrhizobium sp. S23321: insights into symbiosis evolution in soil oligotrophs. Microbes Environ 27:306–315

    Article  Google Scholar 

  • Olsen SR (1954) Estimation of available phosphorus in soils by extraction with sodium bicarbonate. United States Department Of Agriculture, Washington

    Google Scholar 

  • Pan FX, Chapman SJ, Li YY, Yao HY (2017) Straw amendment to paddy soil stimulates denitrification but biochar amendment promotes anaerobic ammonia oxidation. J Soils Sediments 17:2428–2437

    Article  CAS  Google Scholar 

  • Piromyou P, Greetatorn T, Teamtisong K, Okubo T, Shinoda R, Nuntakij A, Tittabutr P, Boonkerd N, Minamisawa K, Teaumroong N (2015) Preferential association of endophytic bradyrhizobia with different rice cultivars and its implications for rice endophyte evolution. Appl Environ Microbiol 81:3049–3061

    Article  CAS  Google Scholar 

  • Poly F, Ranjard L, Nazaret S, Gourbiere F, Monrozier LJ (2001) Comparison of nifH gene pools in soils and soil microenvironments with contrasting properties. Appl Environ Microbiol 67:2255–2262

    Article  CAS  Google Scholar 

  • Reardon CL, Gollany HT, Wuest SB (2014) Diazotroph community structure and abundance in wheat–fallow and wheat–pea crop rotations. Soil Biol Biochem 69:406–412

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Reed SC, Cleveland CC, Townsend AR (2011) Functional ecology of free-living nitrogen fixation: a contemporary perspective. Annu Rev Ecol Evol S 42:489–512

    Article  Google Scholar 

  • Rodrigues Coelho MR, De Vos M, Carneiro NP, Marriel IE, Paiva E, Seldin L (2008) Diversity of nifH gene pools in the rhizosphere of two cultivars of sorghum (Sorghum bicolor) treated with contrasting levels of nitrogen fertilizer. FEMS Microbiol Lett 279:15–22

    Article  Google Scholar 

  • Santi C, Bogusz D, Franche C (2013) Biological nitrogen fixation in non-legume plants. Ann Bot 111:743–767

    Article  CAS  Google Scholar 

  • Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541

    Article  CAS  Google Scholar 

  • Shen C, Xiong J, Zhang H, Feng Y, Lin X, Li X, Liang W, Chu H (2013) Soil pH drives the spatial distribution of bacterial communities along elevation on Changbai Mountain. Soil Biol Biochem 57:204–211

    Article  CAS  Google Scholar 

  • Shu W, Pablo GP, Jun Y, Danfeng H (2012) Abundance and diversity of nitrogen-fixing bacteria in rhizosphere and bulk paddy soil under different duration of organic management. World J Microbiol Biotechnol 28:493–503

    Article  Google Scholar 

  • Su JQ, Ding LJ, Xue K, Yao HY, Quensen J, Bai SJ, Wei WX, Wu JS, Zhou J, Tiedje JM, Zhu YG (2015) Long-term balanced fertilization increases the soil microbial functional diversity in a phosphorus-limited paddy soil. Mol Ecol 24:136–150

    Article  CAS  Google Scholar 

  • Sun R, Guo X, Wang D, Chu H (2015a) Effects of long-term application of chemical and organic fertilizers on the abundance of microbial communities involved in the nitrogen cycle. Appl Soil Ecol 95:171–178

    Article  Google Scholar 

  • Sun R, Zhang X-X, Guo X, Wang D, Chu H (2015b) Bacterial diversity in soils subjected to long-term chemical fertilization can be more stably maintained with the addition of livestock manure than wheat straw. Soil Biol Biochem 88:9–18

    Article  CAS  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    Article  CAS  Google Scholar 

  • Tan Z, Hurek T, Reinhold-Hurek B (2003) Effect of N-fertilization, plant genotype and environmental conditions on nifH gene pools in roots of rice. Environ Microbiol 5:1009–1015

    Article  CAS  Google Scholar 

  • Team RC (2016) A language and environment for statistical computing. R Foundation for statistical computing 2015, Vienna, Austria

    Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  CAS  Google Scholar 

  • Van Nguyen N, Ferrero A (2006) Meeting the challenges of global rice production. Paddy Water Environ 4:1–9

    Article  Google Scholar 

  • Wang J, Zhang D, Zhang L, Li J, Raza W, Huang Q, Shen Q (2016) Temporal variation of diazotrophic community abundance and structure in surface and subsoil under four fertilization regimes during a wheat growing season. Agric Ecosyst Environ 216:116–124

    Article  CAS  Google Scholar 

  • Wang C, Zhou J, Liu J, Du D (2017) Responses of soil N-fixing bacteria communities to invasive species over a gradient of simulated nitrogen deposition. Ecol Eng 98:32–39

    Article  Google Scholar 

  • Wartiainen I, Eriksson T, Zheng W, Rasmussen U (2008) Variation in the active diazotrophic community in rice paddy—nifH PCR-DGGE analysis of rhizosphere and bulk soil. Appl Soil Ecol 39:65–75

    Article  Google Scholar 

  • Wegner CE, Liesack W (2015) Microbial community dynamics during the early stages of plant polymer breakdown in paddy soil. Environ Microbiol 18:2825–2842

    Article  Google Scholar 

  • Xie GH, Cai MY, Tao GC, Steinberger Y (2003) Cultivable heterotrophic N2-fixing bacterial diversity in rice fields in the Yangtze River Plain. Biol Fertil Soils 37:29–38

    CAS  Google Scholar 

  • Yeoh YK, Paungfoo-Lonhienne C, Dennis PG, Robinson N, Ragan MA, Schmidt S, Hugenholtz P (2016) The core root microbiome of sugarcanes cultivated under varying nitrogen fertilizer application. Environ Microbiol 18:1338–1351

    Article  Google Scholar 

  • Yousuf B, Kumar R, Mishra A, Jha B (2014) Differential distribution and abundance of diazotrophic bacterial communities across different soil niches using a gene-targeted clone library approach. FEMS Microbiol Lett 360:117–125

    Article  CAS  Google Scholar 

  • Zhalnina K, de Quadros PD, Gano KA, Davis-Richardson A, Fagen JR, Brown CT, Giongo A, Drew JC, Sayavedra-Soto LA, Arp DJ, Camargo FA, Daroub SH, Clark IM, McGrath SP, Hirsch PR, Triplett EW (2013) Ca. Nitrososphaera and Bradyrhizobium are inversely correlated and related to agricultural practices in long-term field experiments. Front Microbiol 4:104

    Article  Google Scholar 

  • Zhalnina K, Dias R, de Quadros PD, Davis-Richardson A, Camargo FA, Clark IM, McGrath SP, Hirsch PR, Triplett EW (2015) Soil pH determines microbial diversity and composition in the park grass experiment. Microb Ecol 69:395–406

    Article  CAS  Google Scholar 

  • Zhao J, Ni T, Li J, Lu Q, Fang Z, Huang Q, Zhang R, Li R, Shen B, Shen Q (2016) Effects of organic–inorganic compound fertilizer with reduced chemical fertilizer application on crop yields, soil biological activity and bacterial community structure in a rice–wheat cropping system. Appl Soil Ecol 99:1–12

    Article  Google Scholar 

Download references

Funding information

This work was supported by the National Natural Science Foundation of China (41525002, 41471206), the Strategic Priority Research Program of the Chinese Academy of Sciences (XDB15020301), and the Ningbo Municipal Science and Technology Bureau (2015C10031).

Author information

Authors and Affiliations

  1. Key Laboratory of Urban Environment and Health, Institute of Urban Environment, Chinese Academy of Sciences, Xiamen, 361021, People’s Republic of China

    Hongkai Liao, Yaying Li & Huaiying Yao

  2. Key Laboratory of Urban Environmental Processes and Pollution Control, Ningbo Urban Environment Observation and Research Station-NUEORS, Chinese Academy of Sciences, Ningbo, 315800, People’s Republic of China

    Hongkai Liao, Yaying Li & Huaiying Yao

  3. University of Chinese Academy of Sciences, Beijing, 100049, People’s Republic of China

    Hongkai Liao

  4. Research Center for Environmental Ecology and Engineering, School of Environmental Ecology and Biological Engineering, Wuhan Institute of Technology, Wuhan, 430073, People’s Republic of China

    Huaiying Yao

Authors
  1. Hongkai Liao
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yaying Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Huaiying Yao
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Yaying Li or Huaiying Yao.

Additional information

Responsible editor: Jizheng He

Electronic supplementary material

ESM 1

(DOCX 356 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Liao, H., Li, Y. & Yao, H. Fertilization with inorganic and organic nutrients changes diazotroph community composition and N-fixation rates. J Soils Sediments 18, 1076–1086 (2018). https://doi.org/10.1007/s11368-017-1836-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11368-017-1836-8

Keywords

Search

Navigation