Skip to main content

Advertisement

Log in

Biochar and organic fertilizer amendments stimulate the dynamics of ammonia oxidizers community in a slightly alkaline soil

  • Original Paper
  • Published:
Arabian Journal of Geosciences Aims and scope Submit manuscript

Abstract

Soil treated with only biochar or organic fertilizer has been extensively documented to influence the soil nitrification process due to its impact on soil characteristics. However, the dynamic response of ammonia oxidizers to the combined application of biochar and organic fertilizer in slightly alkaline soil is yet to be studied. Therefore, this study intended to evaluate the abundance and composition of ammonia-oxidizing bacteria (AOB) and ammonia-oxidizing archaea (AOA) in incubated soil by using quantitative real-time PCR (qPCR) and terminal restriction fragment length polymorphism (T-RFLP) analysis of amoA genes. The incubation lasted 106 days and involved 4 treatments: the control (CK); 2% (w/w) organic fertilizer (O); 2% (w/w) biochar (B); and a combination of 2% (w/w) organic fertilizer and biochar (OB). Our results showed that AOB and AOA abundance increased significantly and changed over time in the biochar-treated soil at late stages of the incubation. AOA abundance increased nearly 19 times more than AOB abundance in the biochar treatment as compared to the control, indicating that biochar is more crucial to promote AOA abundance than AOB abundance. Moreover, T-RFLP analysis showed that the interaction between biochar and organic fertilizer significantly altered AOA community composition over time due to the effect of biochar and organic fertilizer amendments on soluble organic nitrogen (SON). The soil treated with organic fertilizer had the specific community compositions at the end of the incubation, suggesting that organic fertilizer changed the AOB community composition by increasing available phosphorus (AP), available potassium (AK), and total nitrogen (TN). Our findings, therefore, revealed that biochar can improve AOA abundance and composition by enhancing SON, while organic fertilizer can greatly increase AOB by regulating AP, AK, and TN.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Data availability

All data generated or analyzed during this study are included in this published article [and its supplementary information files].

References

  • Abujabhah IS, Bound SA, Doyle R, Bowman JP (2016) Effects of biochar and compost amendments on soil physico-chemical properties and the total community within a temperate agricultural soil. Appl Soil Ecol 98:243–253

    Article  Google Scholar 

  • Agren GI, Wetterstedt JAM, Billberger MFK (2012) Nutrient limitation on terrestrial plant growth - modeling the interaction between nitrogen and phosphorus. New Phytol 194(4):953–960. https://doi.org/10.1111/j.1469-8137.2012.04116.x

    Article  Google Scholar 

  • Albuquerque L, Rosselló-Móra R, Da Costa MS (2014) The family Rhodobiaceae. In The Prokaryotes: Alphaproteobacteria and Betaproteobacteria Vol. 9783642301971, pp. 513–531

  • Altland JE, Locke JC (2012) Biochar affects macronutrient leaching from a soilless substrate. HortScience 47(8):1136–1140

    Article  Google Scholar 

  • Ball PN, Mackenzie MD, Deluca TH, Holben WE (2010) Wildfire and charcoal enhance nitrification and ammonium-oxidizing bacterial abundance in dry montane forest soils. J Environ Qual 39(4):1243–1253

    Article  Google Scholar 

  • Bi Q-F, Chen Q-H, Yang X-R, Li H, Zheng B-X, Zhou W-W, . . . Lin X-Y (2017) Effects of combined application of nitrogen fertilizer and biochar on the nitrification and ammonia oxidizers in an intensive vegetable soil. AMB Express, 7(1):1-9

  • Bingeman CW, Varner JE, Martin WP (1953) The effect of the addition of organic materials on the decomposition of an organic soil. Soil Sci Soc Am J 17(1):34–38

    Article  Google Scholar 

  • Che J, Zhao XQ, Zhou X, Jia ZJ, Shen RF (2015) High pH-enhanced soil nitrification was associated with ammonia-oxidizing bacteria rather than archaea in acidic soils. Appl Soil Ecol 85:21–29. https://doi.org/10.1016/j.apsoil.2014.09.003

    Article  Google Scholar 

  • Chen XP, Zhu YG, Xia Y, Shen JP, He JZ (2008) Ammonia-oxidizing archaea: important players in paddy rhizosphere soil? Environ Microbiol 10(8):1978

    Article  Google Scholar 

  • Chen J, Liu X, Zheng J, Zhang B, Lu H, Chi Z, . . . Yu X (2013) Biochar soil amendment increased bacterial but decreased fungal gene abundance with shifts in community structure in a slightly acid rice paddy from Southwest China. Appl Soil Ecol 71:33-44. https://doi.org/10.1016/j.apsoil.2013.05.003

  • Clough TJ, Condron LM (2010) Biochar and the nitrogen cycle: introduction. J Environ Qual 39(4):1218–1223

    Article  Google Scholar 

  • Cook KL, Ritchey EL, Loughrin JH, Haley M, Sistani KR, Bolster CH (2015) Effect of turning frequency and season on composting materials from swine high-rise facilities. Waste Manage 39:86–95. https://doi.org/10.1016/j.wasman.2015.02.019

    Article  Google Scholar 

  • Dai X, Guo Q, Song D, Zhou W, Liu G, Liang G, . . . Liu Z (2021) Long-term mineral fertilizer substitution by organic fertilizer and the effect on the abundance and community structure of ammonia-oxidizing archaea and bacteria in paddy soil of south China. Eur J Soil Biol 103:103288

  • Deenik JL, McClellan T, Uehara G, Antal MJ Jr, Campbell S (2010) Charcoal volatile matter content influences plant growth and soil nitrogen transformations. Soil Sci Soc Am J 74(4):1259–1270. https://doi.org/10.2136/sssaj2009.0115

    Article  Google Scholar 

  • Dempster DN, Gleeson DB, Solaiman ZM, Jones DL, Murphy DV (2012) Decreased soil microbial biomass and nitrogen mineralisation with Eucalyptus biochar addition to a coarse textured soil. Plant Soil 354(1):311–324

    Article  Google Scholar 

  • Fierer N, Schimel J, Holden P (2003) Influence of drying–rewetting frequency on soil bacterial community structure. Microb Ecol 45(1):63–71

    Article  Google Scholar 

  • Fontaine S, Mariotti A, Abbadie L (2003) The priming effect of organic matter: a question of microbial competition? Soil Biol Biochem 35(6):837–843. https://doi.org/10.1016/S0038-0717(03)00123-8

    Article  Google Scholar 

  • Hale L, Luth M, Kenney R, Crowley D (2014) Evaluation of pinewood biochar as a carrier of bacterial strain Enterobacter cloacae UW5 for soil inoculation. Appl Soil Ecol 84:192–199

    Article  Google Scholar 

  • Hammer EC, Forstreuter M, Rillig MC, Kohler J (2015) Biochar increases arbuscular mycorrhizal plant growth enhancement and ameliorates salinity stress. Appl Soil Ecol 96:114–121

    Article  Google Scholar 

  • Hartmann M, Frey B, Mayer J, Mäder P, Widmer F (2015) Distinct soil microbial diversity under long-term organic and conventional farming. ISME J 9(5):1177–1194. https://doi.org/10.1038/ismej.2014.210

    Article  Google Scholar 

  • Hatsu M, Sasaki T, Miyadoh S, Watabe HO, Takeuchi Y, Kodama Y, . . . Kondo S (1990) SF2487, a new polyether antibiotic produced by actinomadura. J Antibiot 43(3):259-266. https://doi.org/10.7164/antibiotics.43.259

  • Hayden HL, Drake J, Imhof M, Oxley APA, Norng S, Mele PM (2010) The abundance of nitrogen cycle genes amoA and nifH depends on land-uses and soil types in South-Eastern Australia. Soil Biol Biochem 42(10):1774–1783

    Article  Google Scholar 

  • He L, Liu Y, Zhao J, Bi Y, Zhao X, Wang S, Xing G (2016) Comparison of straw-biochar-mediated changes in nitrification and ammonia oxidizers in agricultural oxisols and cambosols. Biol Fertil Soils 52(2):137–149

    Article  Google Scholar 

  • Hu YL, Wu FP, Zeng DH, Chang SX (2014) Wheat straw and its biochar had contrasting effects on soil C and N cycling two growing seasons after addition to a Black Chernozemic soil planted to barley. Biol Fertil Soils 50(8):1291–1299

    Article  Google Scholar 

  • IUSS WG (2014) World reference base for soil resources 2014 international soil classification system for naming soils and creating legends for soil maps. FAO, Rome

  • Jia W, Qin W, Zhang Q, Wang X, Ma Y, Chen Q (2018) Evaluation of crop residues and manure production and their geographical distribution in China. J Clean Prod 188:954–965

    Article  Google Scholar 

  • Joseph S, Taylor P (2014) The production and application of biochar in soils. Adv Biorefineries 525–555

  • Khamna S, Yokota A, Lumyong S (2009) Actinomycetes isolated from medicinal plant rhizosphere soils: diversity and screening of antifungal compounds, indole-3-acetic acid and siderophore production. World J Microbiol Biotechnol 25(4):649–655. https://doi.org/10.1007/s11274-008-9933-x

    Article  Google Scholar 

  • Kim J-S, Sparovek G, Longo RM, De Melo WJ, Crowley D (2007) Bacterial diversity of terra preta and pristine forest soil from the Western Amazon. Soil Biol Biochem 39(2), 684–690. Retrieved from http://www.sciencedirect.com/science/article/pii/S0038071706003683

  • Lehmann J (2007) Biochar for mitigating climate change: carbon sequestration in the black. Paper presented at the Forum Geoöekologie

    Google Scholar 

  • Leininger S, Urich T, Schloter M, Schwark L, Qi J, Nicol G W, . . . Schleper C (2006) Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature 442(7104):806-809

  • Lichtfouse E (2009) Organic farming, pest control and remediation of soil pollutants. Springer

    Google Scholar 

  • Long X, Chen C, Xu Z, Oren R, He J-Z (2012) Abundance and community structure of ammonia-oxidizing bacteria and archaea in a temperate forest ecosystem under ten-years elevated CO 2. Soil Biol Biochem 46:163–171

    Article  Google Scholar 

  • Marks EA, Alcañiz JM, Domene X (2014) Unintended effects of biochars on short-term plant growth in a calcareous soil. Plant Soil 385(1–2):87–105

    Article  Google Scholar 

  • Mendum TA, Sockett RE, Hirsch PR (1999) Use of molecular and isotopic techniques to monitor the response of autotrophic ammonia-oxidizing populations of the β subdivision of the class Proteobacteria in arable soils to nitrogen fertilizer. Appl Environ Microbiol 65(9):4155–4162. Retrieved from https://www.scopus.com/inward/record.uri?eid=2-s2.0-0032874459&partnerID=40&md5=4f8eb3d6c6cca78bf315626eea002790

  • Mertens J, Broos K, Wakelin SA, Kowalchuk GA, Springael D, Smolders E (2009) Bacteria, not archaea, restore nitrification in a zinc-contaminated soil. ISME J 3(8):916–923. https://doi.org/10.1038/ismej.2009.39

    Article  Google Scholar 

  • Ning Q, Gu Q, Shen J, Lv X, Yang J (2015) Effects of nitrogen deposition rates and frequencies on the abundance of soil nitrogen-related functional genes in temperate grassland of northern China. J Soils Sediments 15(3):694–704

    Article  Google Scholar 

  • Olsen S R (1954) Estimation of available phosphorus in soils by extraction with sodium bicarbonate: United States Department Of Agriculture; Washington

  • Pearson K (1896) Mathematical contributions to the theory of evolution. III. Regression, heredity and panmixia. Phil Trans r Soc Lond A 187:253–318

    Article  Google Scholar 

  • Perez PG, Ye J, Wang S, Wang XL, Huang DF (2014) Analysis of the occurrence and activity of diazotrophic communities in organic and conventional horticultural soils. Appl Soil Ecol 79(5):37–48. Retrieved from http://www.sciencedirect.com/science/article/pii/S092913931400081X

  • Posmanik R, Gross A, Nejidat A (2014) Effect of high ammonia loads emitted from poultry-manure digestion on nitrification activity and nitrifier-community structure in a compost biofilter. Ecol Eng 62:140–147. https://doi.org/10.1016/j.ecoleng.2013.10.033

    Article  Google Scholar 

  • Prayogo C, Jones JE, Baeyens J, Bending GD (2014) Impact of biochar on mineralisation of C and N from soil and willow litter and its relationship with microbial community biomass and structure. Biol Fertil Soils 50(4):695–702

    Article  Google Scholar 

  • Prommer J, Wanek W, Hofhansl F, Trojan D, Offre P, Urich T, . . . Soja G (2014) Biochar decelerates soil organic nitrogen cycling but stimulates soil nitrification in a temperate arable field trial. Plos One 9(1):e86388

  • Prosser JI, Nicol GW (2008) Relative contributions of archaea and bacteria to aerobic ammonia oxidation in the environment. Environ Microbiol 10(11):2931–2941. https://doi.org/10.1111/j.1462-2920.2008.01775.x

    Article  Google Scholar 

  • Prost K, Borchard N, Siemens J, Kautz T, Séquaris JM, Möller A, Amelung W (2013) Biochar affected by composting with farmyard manure. J Environ Qual 42(1):164

    Article  Google Scholar 

  • Rigby D, Cáceres D (2001) Organic farming and the sustainability of agricultural systems. Agric Syst 68(1):21–40

    Article  Google Scholar 

  • Rotthauwe J-H, Witzel K-P, Liesack W (1997) The ammonia monooxygenase structural gene amoA as a functional marker: molecular fine-scale analysis of natural ammonia-oxidizing populations. Appl Environ Microbiol 63(12):4704–4712

    Article  Google Scholar 

  • Saxena J, Rana G, Pandey M (2013) Impact of addition of biochar along with Bacillus sp. on growth and yield of French beans. Sci Hortic 162:351–356

    Article  Google Scholar 

  • Schauss K, Focks A, Leininger S, Kotzerke A, Heuer H, Thiele‐Bruhn S, . . . Smalla K (2009) Dynamics and functional relevance of ammonia‐oxidizing archaea in two agricultural soils. Environ Microbiol 11(2):446-456

  • Schimel JP, Bennett J (2004) Nitrogen mineralization: challenges of a changing paradigm. Ecology 85(3):591–602. Retrieved from https://www.scopus.com/inward/record.uri?eid=2-s2.0-1642465463&partnerID=40&md5=cf0026578905a3ca7e3d3b6fedc3e997

  • Seufert V, Ramankutty N, Foley JA (2012) Comparing the yields of organic and conventional agriculture. Nature 485(7397):229

    Article  Google Scholar 

  • Shen X-Y, Zhang L-M, Shen J-P, Li L-H, Yuan C-L, He J-Z (2011) Nitrogen loading levels affect abundance and composition of soil ammonia oxidizing prokaryotes in semiarid temperate grassland. J Soils Sediments 11(7):1243

    Article  Google Scholar 

  • Shi Y, Liu X, Zhang Q, Gao P, Ren J (2020) Biochar and organic fertilizer changed the ammonia-oxidizing bacteria and archaea community structure of saline–alkali soil in the North China Plain. J Soils Sediments 20(1):12–23

    Article  Google Scholar 

  • Singh BP, Hatton BJ, Singh B, Cowie AL, Kathuria A, Pignatello J, Katz BG (2010) Influence of biochars on nitrous oxide emission and nitrogen leaching from two contrasting soils. J Environ Qual 39(4):1224–1235

    Article  Google Scholar 

  • Soam S, Borjesson P, Sharma PK, Gupta RP, Tuli DK, Kumar R (2017) Life cycle assessment of rice straw utilization practices in India. Biores Technol 228:89–98

    Article  Google Scholar 

  • Soman C, Li D, Wander MM, Kent AD (2016) Long-term fertilizer and crop-rotation treatments differentially affect soil bacterial community structure. Plant Soil 1–15

  • Song Y, Zhang X, Ma B, Chang SX, Gong J (2014) Biochar addition affected the dynamics of ammonia oxidizers and nitrification in microcosms of a coastal alkaline soil. Biol Fertil Soils 50(2):321–332. Retrieved from http://download.springer.com/static/pdf/192/art%253A10.1007%252Fs00374-013-0857-8.pdf?originUrl=http%3A%2F%2Flink.springer.com%2Farticle%2F10.1007%2Fs00374-013-0857-8&token2=exp=1484491372~acl=%2Fstatic%2Fpdf%2F192%2Fart%25253A10.1007%25252Fs00374-013-0857-8.pdf%3ForiginUrl%3Dhttp%253A%252F%252Flink.springer.com%252Farticle%252F10.1007%252Fs00374-013-0857-8*~hmac=fd8d6f3001517ec7d1bca3d51033da4f827b3b02332dc9d5f41842230936dad9

  • Strauss SL, Reardon CL, Mazzola M (2014) The response of ammonia-oxidizer activity and community structure to fertilizer amendment of orchard soils. Soil Biol Biochem 68(1):410–418

    Article  Google Scholar 

  • Sun D, Hale L, Crowley D (2016) Nutrient supplementation of pinewood biochar for use as a bacterial inoculum carrier. Biol Fertil Soils 52(4):1–8

    Article  Google Scholar 

  • Sun X, Han X, Ping F, Zhang L, Zhang K, Chen M, Wu W (2018) Effect of rice-straw biochar on nitrous oxide emissions from paddy soils under elevated CO2 and temperature. Sci Total Environ 628:1009–1016

    Article  Google Scholar 

  • Tago K, Okubo T, Shimomura Y, Kikuchi Y, Hori T, Nagayama A, Hayatsu M (2015) Environmental factors shaping the community structure of ammonia-oxidizing bacteria and archaea in sugarcane field soil. Microbes Environ 30(1):21–28

    Article  Google Scholar 

  • Tourna M, Freitag TE, Nicol GW, Prosser JI (2008) Growth, activity and temperature responses of ammonia-oxidizing archaea and bacteria in soil microcosms. Environ Microbiol 10(5):1357–1364

    Article  Google Scholar 

  • Trupiano D, Cocozza C, Baronti S, Amendola C, Vaccari FP, Lustrato G, . . . Scippa GS (2017) The effects of biochar and its combination with compost on lettuce (Lactuca sativa L.) growth, soil properties, and soil microbial activity and abundance. Int J Agron 2017

  • Van Miegroet H, Cole D (1984) The impact of nitrification on soil acidification and cation leaching in a red alder ecosystem. J Environ Qual 13(4):586–590

    Article  Google Scholar 

  • Van Zwieten L, Singh BP, Kimber SWL, Murphy DV, Macdonald LM, Rust J, Morris S (2014) An incubation study investigating the mechanisms that impact N2O flux from soil following biochar application. Agr Ecosyst Environ 191:53–62. https://doi.org/10.1016/j.agee.2014.02.030

    Article  Google Scholar 

  • Verhamme DT, Prosser JI, Nicol GW (2011) Ammonia concentration determines differential growth of ammonia-oxidising archaea and bacteria in soil microcosms. ISME J 5(6):1067–1071. https://doi.org/10.1038/ismej.2010.191

    Article  Google Scholar 

  • Walker C B, De La Torre J, Klotz M, Urakawa H, Pinel N, Arp D, . . . Gollabgir A (2010) Nitrosopumilus maritimus genome reveals unique mechanisms for nitrification and autotrophy in globally distributed marine crenarchaea. Proc Natl Acad Sci 107(19):8818-8823

  • Wang S, Pablo GP, Ye J, Huang DF (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(2):493–503. Retrieved from <Go to ISI>://WOS:000300014300010

  • Warncke D, Brown J (1998) Potassium and other basic cations. Recommended chemical soil test procedures for the North Central Region(1001):31

  • Wei W, Isobe K, Shiratori Y, Nishizawa T, Ohte N, Otsuka S, Senoo K (2014) N2O emission from cropland field soil through fungal denitrification after surface applications of organic fertilizer. Soil Biol Biochem 69:157–167

    Article  Google Scholar 

  • Wertz S, Leigh AK, Grayston SJ (2012) Effects of long-term fertilization of forest soils on potential nitrification and on the abundance and community structure of ammonia oxidizers and nitrite oxidizers. FEMS Microbiol Ecol 79(1):142–154

    Article  Google Scholar 

  • Wessén E, Nyberg K, Jansson JK, Hallin S (2010) Responses of bacterial and archaeal ammonia oxidizers to soil organic and fertilizer amendments under long-term management. Appl Soil Ecol 45(3):193–200. Retrieved from http://ac.els-cdn.com/S0929139310000661/1-s2.0-S0929139310000661-main.pdf?_tid=1cf92762-db2e-11e6-9681-00000aab0f26&acdnat=1484490358_270d7fbd07a269cdc14ce467d1e60e9f

  • Wu Y, Lu L, Wang B, Lin X, Zhu J, Cai Z, . . . Jia Z (2011) Long-term field fertilization significantly alters community structure of ammonia-oxidizing bacteria rather than archaea in a paddy soil. Soil Sci Soc Am J 75(4):1431-1439

  • Xu HL (2006) Nature farming in Japan: Research Signpost

  • Yao H, Gao Y, Nicol GW, Campbell CD, Prosser JI, Zhang L, . . . Singh BK (2011) Links between ammonia oxidizer community structure, abundance, and nitrification potential in acidic soils. Appl Environ Microbiol 77(13):4618-4625

  • Ye J, Zhang R, Nielsen S, Joseph SD, Huang D, Thomas T (2016) A combination of biochar–mineral complexes and compost improves soil bacterial processes, soil quality, and plant properties. Front Microbiol 7

  • Zhang K, Chen L, Li Y, Brookes PC, Xu J, Luo Y (2017) The effects of combinations of biochar, lime, and organic fertilizer on nitrification and nitrifiers. Biol Fertil Soils 53(1):77–87

    Article  Google Scholar 

  • Zhang K, Chen L, Li Y, Brookes PC, Xu J, Luo Y (2016) The effects of combinations of biochar, lime, and organic fertilizer on nitrification and nitrifiers. BiolFertil Soils 1–11

  • Zheng H, Wang Z, Deng X, Herbert S, Xing B (2013) Impacts of adding biochar on nitrogen retention and bioavailability in agricultural soil. Geoderma 206:32–39. https://doi.org/10.1016/j.geoderma.2013.04.018

    Article  Google Scholar 

  • Zimmerman AR, Gao B, Ahn MY (2011) Positive and negative carbon mineralization priming effects among a variety of biochar-amended soils. Soil Biol Biochem 43(6):1169–1179

    Article  Google Scholar 

Download references

Acknowledgements

The authors are thankful to Shanghai Jiao Tong University, Shanghai China for providing facilities to conduct these experiments. We are also grateful to the anonymous reviewers and editor for the detailed critical comments which led to many improvements of the article.

Funding

This work was financially supported by the Natural Science Foundation of China (project number:42007048) and Shanghai Pujiang Project (project number: 20PJ1405300). The chemical analyses were carried out at the Instrumental Analysis Center of Shanghai Jiao Tong University.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Xinxin Liu or Nan Hui.

Ethics declarations

Ethics approval

Animals and humans/parts are not used in this article.

Conflict of interest

The authors declare that they have no competing interests.

Additional information

Responsible Editor: Amjad Kallel

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 24 KB)

Rights and permissions

Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Khalid, M., Rahman, S.u., Liu, X. et al. Biochar and organic fertilizer amendments stimulate the dynamics of ammonia oxidizers community in a slightly alkaline soil. Arab J Geosci 15, 1612 (2022). https://doi.org/10.1007/s12517-022-10916-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s12517-022-10916-7

Keywords

Navigation