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Valorization of animal bone waste for agricultural use through biomass co-pyrolysis and bio-augmentation

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Abstract

Thermal treatment of animal bone waste (i.e., pyrolysis) is an alternative technology to sustainably manage slaughterhouse waste for agricultural uses. However, concentration of plant-available phosphorus (P) is limited in thermally treated animal bone (i.e., bone char). This study, therefore, aimed to develop sustainable methods to increase the P fertilizer value of animal bone waste through co-pyrolysis of animal bone with lignocellulose agricultural waste and bio-augmentation. Four types of bone chars were produced using two different pyrolysis temperatures (450°C and 850°C) and pyrolysis techniques (conventional and co-pyrolysis). These bone chars were then bio-augmented with four different phosphate solubilizing microorganisms (PSM). In vitro and incubation experiments were conducted to assess the fertilizing value of the products. The result showed that co-pyrolysis of animal bone with lignocellulose agricultural waste combined with bio-augmentation increased P solubility by 133–167%, at the lower production temperature. P solubility decreased considerably at a higher production temperature. However, it was increased by 16- to 21-fold when co-pyrolysis was coupled with bio-augmentation. Addition of co-pyrolyzed bone char enriched with PSM and organic carbon to soil increased P availability by 34 to 48% and PSM survival rate by 22 to 76%. The findings demonstrated that co-pyrolysis combined with bio-augmentation could be an efficient and low-cost strategy to improve the agricultural use of animal bone and to reduce the dependency on chemical fertilizer. This study has a significant importance particularly for developing countries, where the use of chemical fertilizer is limited due to its high price; and slaughterhouse waste has created an environmental concern.

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Abbreviations

CFU:

colony forming unit

CYA:

Czapek yeast extract agar

EC:

electrical conductivity

LC-OCD:

liquid chromatography organic carbon detection

NBRIP:

National Botanical Research Institute’s phosphate

OA:

organic acid

PSM:

phosphate solubilizing microorganisms

SEM:

scanning electron microscopy

WEOC:

water-extractable organic carbon

XRD:

powder X-ray diffraction

YEA:

yeast extract agar

References

  1. Klinglmair M, Lemming C, Jensen LS, Rechberger H, Astrup TF, Scheutz C (2015) Phosphorus in Denmark: national and regional anthropogenic flows. Resour Conserv Recycl 105:311–324. https://doi.org/10.1016/j.resconrec.2015.09.019

    Article  Google Scholar 

  2. Chowdhury RB, Moore GA, Weatherley AJ, Arora M (2017) A novel substance flow analysis model for analysing multi-year phosphorus flow at the regional scale. Sci Total Environ 572:1269–1280. https://doi.org/10.1016/j.scitotenv.2015.10.055

    Article  Google Scholar 

  3. Cordell D, White S (2011) Peak phosphorus: clarifying the key issues of a vigorous debate about long-term phosphorus security. Sustainability 3:2027–2049. https://doi.org/10.3390/su3102027

    Article  Google Scholar 

  4. Chowdhury RB, Moore GA, Weatherley AJ (2018) A multi-year phosphorus flow analysis of a key agricultural region in Australia to identify options for sustainable management. Agric Syst 161:42–60. https://doi.org/10.1016/j.agsy.2017.12.005

    Article  Google Scholar 

  5. Simons A, Solomon D, Chibssa W (2014) Filling the phosphorus fertilizer gap in developing countries. Nat Geosci 7:3. https://doi.org/10.1038/ngeo2049

    Article  Google Scholar 

  6. Ahmed, M., Nigussie, A., Addisu, S., Belay, B., Sato, S. (2021) Valorization of animal bone into phosphorus biofertilizer: effects of animal species, thermal processing method, and production temperature on phosphorus availability, Soil Science and Plant Nutrition, https://doi.org/10.1080/00380768.2021.1945403

  7. Christel W, Bruun S, Magid J, Jensen LS (2014) Phosphorus availability from the solid fraction of pig slurry is altered by composting or thermal treatment. Bioresour Technol 169:543–551. ISSN 0960-8524. https://doi.org/10.1016/j.biortech.2014.07.030

    Article  Google Scholar 

  8. Glæsner N, Hansen HCB, Hu Y, Bekiaris G, Bruun S (2019) Low crystalline apatite in bone char produced at low temperature ameliorates phosphorus-deficient soils. Chemosphere 223:723–730. https://doi.org/10.1016/j.chemosphere.2019.02.048

    Article  Google Scholar 

  9. Zwetsloot MJ, Lehmann J, Solomon D (2014) Recycling slaughterhouse waste into fertilizer: how do pyrolysis temperature and biomass additions affect phosphorus availability and chemistry? J Sci Food Agric 95(281-288):390. https://doi.org/10.1002/jsfa.6716

    Article  Google Scholar 

  10. Richardson AE (2001) Prospects for using soil microorganisms to improve the acquisition of phosphorus by plants. Aust J Plant Physiol 28:897–906. https://doi.org/10.1071/PP01093

    Article  Google Scholar 

  11. Tarafdar JC, Rao AV, Kumar P (1995) Role of phosphate producing fungi on the growth and nutrition of clusterbean (Cyamopsis tetragonoloba (L.) Taub). J Arid Environ 29(3):331–337. https://doi.org/10.1016/S0140-1963(05)80112-0

    Article  Google Scholar 

  12. Yeomans JC, Bremner JM (1988) A rapid and precise method for routine determination of organic carbon in soil. Commun Soil Sci Plant Anal 19(13):1467–1476. https://doi.org/10.1080/00103628809368027

    Article  Google Scholar 

  13. Enders, A., Sori, S., Lehmann, J., Singh, B. (2017) Total elemental analysis of metal and nutrient in biochar. In Biochar: a guide to analytical methods (ed. Singh, B., Camps-Arbestein, M. & Lehmann, J.) 95 – 108 (CRS Press, 2017)

  14. Rajan SSS, Brown MW, Boyes MK et al (1992) Extractable phosphorus to predict agronomic effectiveness of ground and unground phosphate rocks. Fertilizer Research 32:291–302. https://doi.org/10.1007/BF01050366

    Article  Google Scholar 

  15. Chinu, K., Marjo, Ch. E., Joseph, S. D. Singh, B (2017) Dissolved organic carbon and LC-OCD of biochar. In Biochar: a guide to analytical methods (ed. Singh, B., Camps-Arbestein, M. & Lehmann, J.) 64 – 73 (CRS Press, 2017)

  16. Raymond NS, Stöver DM, Peltre C, Nielsen HH, Jensen LS (2018) Use of Penicillium bilaiae to improve phosphorus bioavailability of thermally treated sewage sludge – a potential novel biofertilizer. Process Biochem 69:169–177. https://doi.org/10.1016/j.procbio.2018.03.021

    Article  Google Scholar 

  17. Nautiyal CS (1999) An efficient microbiological growth medium for screening phosphate solubilizing microorganisms. FEMS Microbiol Lett 170:265–270. https://doi.org/10.1111/j.1574-6968.1999.tb13383.x

    Article  Google Scholar 

  18. Baskin T, Orr T, Jercinovic M, Yoshida M (2014) Sample preparation for scanning electron microscopy: the surprising case of freeze drying from tertiary butanol. Microscopy Today 22(3):36–39. https://doi.org/10.1017/S1551929514000522

    Article  Google Scholar 

  19. Tigist M., Gebermedihin A., Nigussie A., Amsalu N., Milkiyas A. (2020) Short-term application of biochar increases the amount of fertilizer required to obtain potential yield and reduces marginal agronomic efficiency in high phosphorus-fixing soils. Biochar; https://doi.org/10.1007/s42773-020-00059-x

  20. IUSS Working Group WRS. (2014) World Reference Base for Soil Resource 2014. International soil classification system for naming soils and creating legends for soil map. World Soil Resource Report No. 106. FAO, Rome.

  21. Trevors JT, Cook S (1992) A comparison of plating media and diluents for enumeration of anaerobic bacteria in a loam soil. J Microbiol Methods 14:271–275. ISSN 0167-7012. https://doi.org/10.1016/0167-7012(92)90060-H

    Article  Google Scholar 

  22. Tingting Q., Yang Q., Jun D.C. F, Dong F., Zhou Y. (2019) Transformation of phosphorus in sewage sludge biochar mediated by a phosphate-solubilizing microorganism, Chemical Engineering Journal, Volume 359, 1573-1580, ISSN 1385-8947, https://doi.org/10.1016/j.cej.2018.11.015.

  23. Bashan Y, Kamnev AA, de-Bashan, L.E. (2013) Tricalcium phosphate is inappropriate as a universal selection factor for isolating and testing phosphate-solubilizing bacteria that enhance plant growth: a proposal for an alternative procedure. Biol Fertil Soils 49:465–479. https://doi.org/10.1007/s00374-012-0737-7

    Article  Google Scholar 

  24. Mendes GO, Moreira De Freitas AL, Liparini Pereira O, Ribeiro Da Silva I, Vassilev NB, Dutra Costa M (2014) Mechanisms of phosphate solubilization by fungal isolates when exposed to different P sources. Ann Microbiol 64:239–249. https://doi.org/10.1007/s13213-013-0656-3

    Article  Google Scholar 

  25. Jacoby R, Peukert M, Succurro A, Koprivova A, Kopriva S (2017) The role of soil microorganisms in plant mineral nutrition current knowledge and future directions. Front Plant Sci 8:1–19. https://doi.org/10.3389/fpls.2017.01617

    Article  Google Scholar 

  26. Scervino J, Papinutti V, Godoy M, Rodriguez M, Della Monica I, Recchi M, Pettinari M, Godeas A (2011) Medium pH, carbon and nitrogen concentrations modulate the phosphate solubilization efficiency of P. purpurogenum through organic acid production. J Appl Microbiol 110(5):1215–1223. https://doi.org/10.1111/j.1365-2672.2011.04972.x

    Article  Google Scholar 

  27. Stefanoni Rubio PJ, Godoy MS, Della Mónica IF, Pettinari MJ, Godeas AM, Scervino JM (2016) Carbon and nitrogen sources influence tricalcium phosphate solubilization and extracellular phosphatase activity by Talaromyces flavus. Curr Microbiol 72:41–47. https://doi.org/10.1007/s00284-015-0914-7

    Article  Google Scholar 

  28. Lehmann, J., Matthias C. Rillig, Janice Thies, Caroline A. Masiello, William C. Hockaday, David Crowley (2011) Biochar effects on soil biota – a review, Soil Biology and Biochemistry, Volume 43, Issue 9, 1812-1836, ISSN 0038-0717, https://doi.org/10.1016/j.soilbio.2011.04.022.

  29. Noyce GL, Basiliko N, Fulthorpe R, Sackett TE, Thomas SC (2015) Soil microbial response over 2 years following biochar addition to a north temperate forest. Biol Fertil Soils 51:649–659. https://doi.org/10.1007/s00374-015-1010-7

    Article  Google Scholar 

  30. Zhang L, Jing Y, Xiang Y, Zhang R, Lu H (2018) Responses of soil microbial community structure changes and activities to biochar addition: a meta-analysis. Sci Total Environ 643:926–935. https://doi.org/10.1016/j.scitotenv.2018.06.231

    Article  Google Scholar 

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Acknowledgements

This work has been conducted as part of a PhD thesis project supported by Private University Research Branding Project (PLANE3T) funded by MEXT, Japan, and supported by Science and Technology Research Partnership for Sustainable Development (SATREPS; Grant Number JPMJSA2005) funded by Japan Science and Technology Agency (JST)/Japan International Cooperation Agency (JICA). Animal (sheep) bones were supplied from local restaurants in Tokyo, Japan.

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Authors and Affiliations

  1. Graduate School of Science and Engineering, Soka University, Tokyo, Japan

    Milkiyas Ahmed & Shinjiro Sato

  2. College of Agriculture and Veterinary Medicine, Jimma University, Jimma, Ethiopia

    Milkiyas Ahmed & Abebe Nigussie

  3. College of Agriculture and Environmental Science, Bahir Dar University, Bahir Dar, Ethiopia

    Solomon Addisu

  4. College of Agriculture, Food and Climate Sciences, Injibara University, Injibara, Ethiopia

    Berhanu Belay

  5. Soil and Crop Sciences, School of Integrative Plant Science, Cornell University, Ithaca, NY, USA

    Johannes Lehmann

Authors
  1. Milkiyas Ahmed
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  2. Abebe Nigussie
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  3. Solomon Addisu
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  4. Berhanu Belay
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  5. Johannes Lehmann
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  6. Shinjiro Sato
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Contributions

Milkiyas Ahmed, Shinjiro Sato, and Abebe Nigussie conceived the idea, designed the study, and conducted the statistical analyses. Shinjiro Sato, Solomon Addis, Berhanu Belay, and Johannes Lehmann supervised the development and progress of the work. Milkiyas Ahmed wrote the draft manuscript, and all the authors contributed equally to editing the manuscript. All the authors gave their final approval for publication and have no competing interests or conflict of interest.

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Correspondence to Shinjiro Sato.

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Ahmed, M., Nigussie, A., Addisu, S. et al. Valorization of animal bone waste for agricultural use through biomass co-pyrolysis and bio-augmentation. Biomass Conv. Bioref. 13, 12823–12832 (2023). https://doi.org/10.1007/s13399-021-02100-w

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  • DOI: https://doi.org/10.1007/s13399-021-02100-w

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