Abstract
Applying industrial waste to soil is one way of closing and linking productive cycles; however, industrial waste often contains pollutants such as salts, heavy metals, or toxic compounds with potentially adverse effects on soil health. The aim of this work was to assess the effects of industrial saline wastewater (ISW) from heparin production as a biobased fertilizer on soil nutrient phytoavailability, soybean development, biological nitrogen fixation, and soil microbial activity in an Oxisol. Five ISW rates (0, 10, 20, 40, and 60 m3 ha−1) were used in experiments under controlled conditions with soybean for 146 days and soil incubation experiments for 47 days. ISW had no negative impact on leaf chlorophyll content, number or dry mass in root nodules, or dry mass in soybean plants. Soil P, K, and Na contents were immediately increased upon ISW application but fell to their initial levels with time (especially those of P and Na). However, plants fertilized with ISW rates above 20 m3 ha−1 produced significantly more pods (31%) and grains (21%), and had greater thousand weight grain and yield (up to 25%), on average than unfertilized plants. By contrast, low ISW rates had no significant effect on ureide content (N biologically fixed). The highest ISW rate (60 m3 ha−1) decreased ureide levels by up to 60% relative to no ISW application. ISW boosted soil microbial activity in proportion to its rate; also, it increased organic carbon availability for soil microorganisms irrespective of rate. ISW from heparin production is thus a potentially effective biobased fertilizer use of which at 20–40 m3 ha−1 in humid areas is recommended to reduce the amounts of synthetic fertilizers needed, and improve soil nutrient availability and soil microbial activity, all without adversely affecting soil health or biological N fixation.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abd Alla MH, Vuong TD, Harper JE (1998) Diferenças genotípicas na resposta de fixação de dinitrogênio ao estresse de NaCl em soja intacta e enxertada. Crop Sci 38:72–77
Adhikari D, Dunham-Cheatham SM, Wordofa DN, Verburg P, Poulson SR, Yang Y (2019) Aerobic respiration of mineral-bound organic carbon in a soil. Sci. Total Environ 651:1253–1260. https://doi.org/10.1016/j.scitotenv.2018.09.271
Akbar M, Yabuno T (1977) Breeding for saline-resistant varieties of rice. Japanese J Breed 27:237–240
Bruning B, Rozema J (2013) Symbiotic nitrogen fixation in legumes: perspectives for saline agriculture. Environ Exp Bot 92:134–133. https://doi.org/10.1016/j.envexpbot.2012.09.001
Chakraborty S, Harris JM (2022) At the crossroads of salinity and rhizobium−legume symbiosis. Mol Plant Microbe In 35:540–553. https://doi.org/10.1094/MPMI-09-21-0231-FI
Chen J, Xiao W, Zheng C, Zhu B (2020) Nitrogen addition has contrasting effects on particulate and mineral-associated soil organic carbon in a subtropical forest. Soil Biol Biochem 142:107708. https://doi.org/10.1016/j.soilbio.2020.107708
Cisneros BJ (2011) Safe sanitation in low economic development areas. In: Nriagu JO (ed) Encyclopedia of Environmental Health. Elsevier, pp 147–200
Córdova SC, Castellano MJ, Dietzel R, Licht MA, Togliatti K, Martinez-Feria R, Archontoulis SV (2019) Soybean nitrogen fixation dynamics in Iowa, USA. Field Crop Res 236:165–176. https://doi.org/10.1016/j.fcr.2019.03.018
CQFS (2016) Manual de adubação e calagem para os estados do Rio Grande do Sul e Santa Catarina, 11th edn. NRS/SBCS, Porto Alegre, Brazil
da Silva EE, de Azevedo PHS, De-Polli, H., 2007. Determinação da respiração basal (RBS) e quociente metabólico do solo (qCO2), Comunicado Técnico EMBRAPA. (Portuguese)
De Oliveira Junior, A., Oliveira, F.A., Castro, C., Jordão, L.T., 2013. Adubação potássica da soja: cuidados no balanço de nutrientes. Informações Agronômicas 1–10. (Portuguese)
Dexler ILC, Pietro AL, Yeh D (2011) Wastewater constituents. In: Remediation of polluted water, vol 3. Elsevier Inc, pp 7–29. https://doi.org/10.1016/B978-0-12-382182-9.00043-8
Fink JR, Inda AV, Bavaresco J, Barróm V, Torrent J, Bayer C (2016) Adsorption and desorption of phosphorus in subtropical soils as affected by management system and mineralogy. Soil Till Res 155:62–68. https://doi.org/10.1016/j.still.2015.07.017
Fink J, Sánchez-Rodríguez AR, Frosi G, Eckert D, Bonetti JA, Bastiani K, Lavratti A, Inda AV, Zanquetti A (2021) Industrial saline wastewater in a corn−soybean rotation to enhance crop yield without compromising soil health in a subtropical soil. J Environ Manage 296. https://doi.org/10.1016/j.jenvman.2021.113341
Hao T, Zhu Q, Zeng M, Shen J, Shi X, Liu X, Zhang F, de Vries W (2020) Impacts of nitrogen fertilizer type and application rate on soil acidification rate under a wheat−maize double cropping system. J Environ Manage 270:110888. https://doi.org/10.1016/j.jenvman.2020.110888
Hoornweg D, Bhada-Tata P (2012) What a waste: a global review of solid waste management. World Bank, Washington, DC
Hungria M, Araujo RS (1994) Manual de métodos empregados em estudso de microbiologia agrícola. EMBRAPA
Hungria, M., Campo, R.J., Mendes, I.C., 2001. Fixação biológica do nitrogênio na cultura da soja, Embrapa Soja. Circular Técnica 35. (Portuguese)
IAPAR, 2019. Médias históricas para Palmas−Paraná [WWW Document]. http://www.iapar.br/arquivos/Image/monitoramento/Medias_Historicas/Palmas.htm (Last accessed 09.25.2020). (Portuguese)
Kaminski J, Gatiboni LC, Rheinheimer DS, Martins JR, Santos JS, Tissot CA (2002) Estimativa da acidez potencial em solos e dua implicação no cálculo da necessidade de calcário. Rev Bras Ciência do Soloncia do Solo 26:1107–1113
Kaza S, Yao L, Bhada-Tata P, Van Woerden F (2018) What a waste 2.0 — a global snapshot of solid waste management to 2050. World Bank Group, Washington. https://doi.org/10.1596/978-1-4648-1329-0
Khajeh-Hosseini M, Powell AA, Bingham IJ (2003) The interaction between salinity stress and seed vigour during germination of soyabean seeds. Seed Sci Technol 31:715–725. https://doi.org/10.15258/sst.2003.31.3.20
Klein A, Keyster M, Ludidi N (2015) Response of soybean nodules to exogenously applied caffeic acid during NaCl-induced salinity. S Afr J Bot 96:13–18. https://doi.org/10.1016/j.sajb.2014.10.016
Lavallee JM, Soong JL, Cotrufo MF (2020) Conceptualizing soil organic matter into particulate and mineral-associated forms to address global change in the 21st century. Glob Chang Biol 26:261–273. https://doi.org/10.1111/gcb.14859
Li K, Niu M, Bai W, Yang Z, Li G (2021) Water-dominated negative effects of nitrogen enrichment on soil respiration in a temperate steppe. Appl Soil Ecol 165:104023. https://doi.org/10.1016/j.apsoil.2021.104023
Liu Y, Zhao C, Guo J, Zhang L, Xuan J, Chen A, You C (2021) Short-term phosphorus addition augments the effects of nitrogen addition on soil respiration in a typical steppe. Sci Total Environ 761:143211. https://doi.org/10.1016/j.scitotenv.2020.143211
Lo Cascio M, Morillas L, Ochoa-Hueso R, Munzi S, Roales J, Hasselquist NJ, Manrique E, Spano D, Jaoudé RA, Mereu S (2017) Contrasting effects of nitrogen addition on soil respiration in two Mediterranean ecosystems. Environ Sci Pollut Res 24:26160–26171. https://doi.org/10.1007/s11356-017-8852-5
Lorenzen CJ (1967) Determination of chlorophyll and pheo-pigments: spectrophotometric equations. Limnol Oceanogr 12:343–346. https://doi.org/10.4319/lo.1967.12.2.0343
Lu H, Lashari MS, Liu X, Ji H, Li L, Zheng J, Kibue GW, Joseph S, Pan G (2015) Changes in soil microbial community structure and enzyme activity with amendment of biochar−manure compost and pyroligneous solution in a saline soil from Central China. Eur J Soil Biol 70:67–76. https://doi.org/10.1016/j.ejsobi.2015.07.005
Miransari M, Smith DL (2007) Overcoming the stressful effects of salinity and acidity on soybean nodulation and yields using signal molecule genistein under field conditions. J Plant Nutr 30:1967–1992. https://doi.org/10.1080/01904160701700384
Murphy J, Riley JP (1962) A modified single solution method for the determination of phosphate in natural waters. Anal Chim Acta 27:31–36. https://doi.org/10.1057/9781137461131
Nelson DW, Sommers LE (1996) Total carbon, organic carbon and organic matter. In: SPARKS DL (ed) Methods of soil analysis: chemical methods, vol 3. SSSA, Madison, WI, pp 961–1010
Raiesi F, Sadeghi E (2019) Interactive effect of salinity and cadmium toxicity on soil microbial properties and enzyme activities. Ecotox Environ Safe 168:221–229. https://doi.org/10.1016/j.ecoenv.2018.10.079
Raza S, Zamanian K, Ullah S, Kuzyakov Y, Virto I, Zhou J (2021) Inorganic carbon losses by soil acidification jeopardize global efforts on carbon sequestration and climate change mitigation. J Clean Prod 315. https://doi.org/10.1016/j.jclepro.2021.128036
Santachiara G, Salvagiotti F, Rotundo JL (2019) Nutritional and environmental effects on biological nitrogen fixation in soybean: a meta-analysis. Field Crop Res 240:106–115. https://doi.org/10.1016/j.fcr.2019.05.006
Shaaban M, Wu Y, Núñez-Delgado A, Kuzyakov Y, Peng Q, Lin S, Hu R (2023) Enzyme activities and organic matter mineralization in response to application of gypsum, manure and rice straw in saline and sodic soils. Environ Res 224:115393. https://doi.org/10.1016/j.envres.2023.115393
Shi S, Tian L, Nasir F, Bahadur A, Batool A, Luo S, Yang F, Wang Z, Tian C (2019) Response of microbial communities and enzyme activities to amendments in saline-alkaline soils. Appl Soil Ecol 135:16–24. https://doi.org/10.1016/j.apsoil.2018.11.003
Singleton PW, El Swaify SA, Bohlool BB (1982) Effect of salinity on rhizobium growth and survival. Appl. Environ. Microb. 44:884–890. https://doi.org/10.1128/aem.44.4.884-890.1982
Soil Survey Staff (2014) Keys to soil taxonomy, 12th edn. United States Department of Agriculture/Natural Resources Conservation Service, Washington, DC
Straathof AL, Chincarini R, Comans RNJ, Hoffland E (2014) Dynamics of soil dissolved organic carbon pools reveal both hydrophobic and hydrophilic compounds sustain microbial respiration. Soil Biol Biochem 79:109–116. https://doi.org/10.1016/j.soilbio.2014.09.004
Tedesco MJ, Gianello C, Bissani CA, Bohnen H, Volkweiss SJ (1995) Análises de solo, planta e outros materiais, 2nd edn. UFRGS, Porto Alegre
Teixeira, P.C., Donagemma, G.K., Fontana, A., Teixeira, W.G. (Eds.), 2017. Manual de métodos e análise de solo, 3rd ed. EMBRAPA, Rio de Janeiro. (Portuguese)
Ustohalova V (2011) Management and export of wastes: human health implications. In: Nriagu JO (ed) Encyclopedia of Environmental Health. Elsevier, pp 603–611
Van Corp, C.L., Vosburgh, F. Schubert, R.L., 1992. Protein hydrolysate derived from mucosa tissue. United State Patent no. 5607840
Vogels GD, Van Der Drift C (1970) Differential analyses of glyoxylate derivatives. Anal Biochem 33:143–157. https://doi.org/10.1016/0003-2697(70)90448-3
WWAP (United Nations World Water Assessment Program) (2017) Wastewater: the untapped resource. In: World Water Development Report 2017. UNESCO, Paris
Xie W, Zhang Y, Li J, Wei S, Li X, Yu H, Guan B (2021) Straw application coupled with N and P supply enhanced microbial biomass, enzymatic activity, and carbon use efficiency in saline soil. Appl Soil Ecol 168:104128. https://doi.org/10.1016/j.apsoil.2021.104128
Xu M, Shang H (2016) Contribution of soil respiration to the global carbon equation. J Plant Physiol 203:16–28. https://doi.org/10.1016/j.jplph.2016.08.007
Yahya KE, Jia Z, Luo W, YuanChun H, Ame MA (2022) Enhancing salt leaching efficiency of saline-sodic coastal soil by rice straw and gypsum amendments in Jiangsu coastal area. Ain Shams Eng J 13:101721. https://doi.org/10.1016/j.asej.2022.101721
Yan N, Marschner P, Cao W, Zuo C, Quin W (2015) Influence of salinity and water content on soil microorganisms. Int Soil Wat Conserv Res 3:316–323. https://doi.org/10.1016/j.iswcr.2015.11.003
Yang J, Zhan C, Li Y, Zhou D, Yu Y, Yu J (2018) Effect of salinity on soil respiration in relation to dissolved organic carbon and microbial characteristics of a wetland in the Liaohe River estuary Northeast China. Sci Total Environ 642:946–953. https://doi.org/10.1016/j.scitotenv.2018.06.121
Yang C, Lv D, Jiang S, Lin H, Sun J, Li K, Sun J (2021) Soil salinity regulation of soil microbial carbon metabolic function in the Yellow River Delta China. Sci Total Environ 790:148258. https://doi.org/10.1016/j.scitotenv.2021.148258
Zaman M, Shahid SA, Heng L (2018) Guideline for salinity assessment, mitigation and adaptation using nuclear and related techniques. https://doi.org/10.1007/978-3-319-96190-3
Zhang C, Sale PWG, Tang C (2016) Cadmium uptake by Carpobrotus rossii (Haw.) Schwantes under different saline conditions. Environ Sci Pollut Res 23:13480–13488. https://doi.org/10.1007/s11356-016-6508-5
Funding
Partial financial support was received from the National Council for Scientific and Technological Development (Universal Edital-2018 − Process 409613/ 2018-5) and the Federal Institute of Paraná in the form of fellowships to Agronomy students (Edital Unificado-Pesquisa-2019 and PROEPI No. 04/ 2018) by Dr. Jessé Fink. In addition, Dr. Antonio Rafael Sánchez-Rodríguez received financial support from the Spanish State Research Agency of the Spanish Ministry of Science and Innovation, the European Regional Development Fund (Project PID2020-118503RB-C22), and the Severo Ochoa and María de Maeztu Programs for Centers and Units of Excellence in R&D (Ref. CEX2019-000968-M).
Author information
Authors and Affiliations
Contributions
Jessé Fink: conceptualization; methodology; investigation; re-sources; formal analysis; writing — original draft; writing — review and editing; supervision; project administration; funding acquisition.
Antonio Rafael Sánchez-Rodríguez: methodology; investigation; formal analysis; writing — original draft; writing — review and editing; funding acquisition.
Alan Lavratti: investigation; formal analysis; writing — original draft.
Kayn Bastiani: methodology; investigation; formal analysis; writing — original draft.
Daniel Stanck: investigation; formal analysis; writing — original draft.
Kelyn Henkemaier: investigation; formal analysis; writing — original draft.
Gustavo Frosi: methodology; investigation; formal analysis; writing — original draft.
Clovis Pierozan Junior: methodology; investigation.
Alberto Vasconcellos Inda: conceptualization; writing — review and editing.
Aline Zanquetti: resources.
Corresponding author
Ethics declarations
Conflict of Interest
The authors declare no competing interests.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) 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.
About this article
Cite this article
Fink, J., Sánchez-Rodríguez, A.R., Lavratti, A. et al. Phosphorus and Potassium Cycling, Biological Nitrogen Fixation in Soybean, and Soil Microbial Activity in an Oxisol Fertilized with Wastewater from Heparin Production. J Soil Sci Plant Nutr 23, 4438–4449 (2023). https://doi.org/10.1007/s42729-023-01361-w
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s42729-023-01361-w