Long-term storage effects of organic amendments as carrier materials on the viability of bacterial strains: Insights from growth analysis and metabolite profiling

Abstract

This study examines the effects of different organic carrier materials, chicken manure, mill mud, and cow manure on the long-term viability and metabolite profiles of rhizobacterial strains Mesorhizobium sp. and Rhizobium sp. Over one year, growth curve analysis revealed significant differences in bacterial proliferation. Mill mud supported the most robust growth, with a doubling of 11 days, compared to chicken and cow manure, which exhibited growth saturation after five to eight months. Non-targeted ¹H-NMR metabolite profiling revealed distinct sugar and amino acid profiles across carriers. Mill mud exhibited a broader range of sugars, including sucrose, maltose, and mannose, while chicken and cow manure primarily contained monosaccharides like glucose, xylose, and mannitol. Amino acids such as lysine and glutamate were higher in chicken manure, followed by cow manure and mill mud. Plant growth-promoting metabolites were detected in all carriers, with Mesorhizobium sp. and Rhizobium sp. enhancing their production by up to 200% in mill mud and cow manure. Both bacterial strains utilized sugars from the carriers, with Mesorhizobium sp. showing more consistent sugar metabolism. These findings suggest that mill mud is an effective carrier for sustaining rhizobacterial viability and enhancing metabolite production, benefiting biofertilizer formulations and soil health.

Graphical abstract

Keywords

agro-byproducts / organic fertilizers / bacterial viability / plant growth promotion / agronomy development / soil health

Highlight

	● Mill mud is the most effective carrier for longterm rhizobacterial viability.
	● Metabolite profiling identified aminoacids and sugars in all treatments.
	● Plant growth metabolites were detected in all organic carrier materials.
	● Mesorhizobium sp. consistently utilized sugars across all carriers.
	● The study aids biofertilizer development to enhance soil health and crop productivity.

References

[1] ABC, 2021. Which poo is right for you? Available at the website of the ABC Australia (accessed Oct. 2024).

[2] Albareda, M., Rodríguez-Navarro, D.N., Camacho, M., Temprano, F.J., 2008. Alternatives to peat as a carrier for rhizobia inoculants: solid and liquid formulations. Soil Biology and Biochemistry40, 2771–2779.

[3] Aloo, B.N., Mbega, E.R., Makumba, B.A., Tumuhairwe, J.B., 2022. Effects of carrier materials and storage temperatures on the viability and stability of three biofertilizer inoculants obtained from potato (Solanum tuberosum L.) rhizosphere. Agriculture12, 140.

[4] Arora, N.K., Khare, E., Maheshwari, D.K., 2010. Plant growth promoting rhizobacteria: Constraints in bioformulation, commercialization, and future strategies. In: Maheshwari, D.K., ed. Plant Growth and Health Promoting Bacteria. Berlin: Springer, 97–116.

[5] Bashan, Y., 1998. Inoculants of plant growth-promoting bacteria for use in agriculture. Biotechnology Advances16, 729–770.

[6] Bashan, Y., de-Bashan, L.E., Prabhu, S.R., Hernandez, J.P., 2014. Advances in plant growth-promoting bacterial inoculant technology: formulations and practical perspectives (1998–2013). Plant and Soil378, 1–33.

[7] Chong, J., Soufan, O., Li, C., Caraus, I., Li, S.Z., Bourque, G., Wishart, D.S., Xia, J.G., 2018. MetaboAnalyst 4.0: towards more transparent and integrative metabolomics analysis. Nucleic Acids Research 46, W486-W494.

[8] Di, D.W., Zhang, C.G., Luo, P., An, C.W., Guo, G.Q., 2016. The biosynthesis of auxin: how many paths truly lead to IAA?. Plant Growth Regulation78, 275–285.

[9] Duca, D., Lorv, J., Patten, C.L., Rose, D., Glick, B.R., 2014. Indole-3-acetic acid in plant–microbe interactions. Antonie van Leeuwenhoek106, 85–125.

[10] El-Ashry, R.M., 2021. Application of animal manure and plant growth-promoting rhizobacteria as effective tools to control soil nematode population and increase crop yield in grapevine orchards. Egyptian Journal of Agronematology20, 34–52.

[11] Eldridge, D.J., Maestre, F.T., Koen, T.B., Delgado-Baquerizo, M., 2018. Australian dryland soils are acidic and nutrient-depleted, and have unique microbial communities compared with other drylands. Journal of Biogeography45, 2803–2814.

[12] Gómez, X., Blanco, D., Lobato, A., Calleja, A., Martínez-Núñez, F., Martin-Villacorta, J., 2011. Digestion of cattle manure under mesophilic and thermophilic conditions: characterization of organic matter applying thermal analysis and ¹H NMR. Biodegradation22, 623–635.

[13] GRDC, 2014. Use of manures [Online]. Available at the website of Grains Research and Development Corporation.

[14] Hardy, K., Knight, J.D., 2021. Evaluation of biochars as carriers for Rhizobium leguminosarum. Canadian Journal of Microbiology67, 53–63.

[15] Hatcher, P.G., 1987. Chemical structural studies of natural lignin by dipolar dephasing solid-state ¹³C nuclear magnetic resonance. Organic Geochemistry11, 31–39.

[16] Haygarth, P.M., Bardgett, R.D., Condron, L.M., 2013. Nitrogen and phosphorus cycles and their management. In: Gregory, P.J., Nortcliff, S., eds. Soil Conditions and Plant Growth. Hoboken: Wiley-Blackwell, 132–159.

[17] Hungria, M., Franchini, J.C., Campo, R.J., Graham, P.H., 2005. The importance of nitrogen fixation to soybean cropping in South America. In: Werner, D., Newton, W.E., eds. Nitrogen Fixation in Agriculture, Forestry, Ecology, and the Environment. Dordrecht: Springer, 25–42.

[18] Kalayu, G., 2019. Phosphate solubilizing microorganisms: promising approach as biofertilizers. International Journal of Agronomy2019, 4917256.

[19] Khavazi, K., Rejali, F., Seguin, P., Miransari, M., 2007. Effects of carrier, sterilisation method, and incubation on survival of Bradyrhizobium japonicum in soybean (Glycine max L.) inoculants. Enzyme and Microbial Technology41, 780–784.

[20] Kim, H.K., Choi, Y.H., Verpoorte, R., 2010. NMR-based metabolomic analysis of plants. Nature Protocols5, 536–549.

[21] Laliberté, E., Grace, J.B., Huston, M.A., Lambers, H., Teste, F.P., Turner, B.L., Wardle, D.A., 2013. How does pedogenesis drive plant diversity? Trends in Ecology & Evolution 28, 331–340.

[22] Larsen, J., Rezaei Rashti, M., Esfandbod, M., Chen, C.R., 2024. Organic amendments improved soil properties and native plants’ performance in an Australian degraded land. Soil Research62, SR22252.

[23] Li, Y.T., Shabir, R., Rashti, M.R., Megharaj, M., Chen, C.R., 2023. Cow manure compost-based products as alternative rhizobial carrier materials. Land Degradation & Development34, 4768–4780.

[24] Liu, X.Y., Milla, R., Granshaw, T., Van Zwieten, L., Rashti, M.R., Esfandbod, M., Chen, C.R. 2021. Responses of soil nutrients and microbial activity to the mill-mud application in a compaction-affected sugarcane field. Soil Research60, 385–398.

[25] Lobo, C.B., Juárez Tomás, M.S., Viruel, E., Ferrero, M.A., Lucca, M.E., 2019. Development of low-cost formulations of plant growth-promoting bacteria to be used as inoculants in beneficial agricultural technologies. Microbiological Research219, 12–25.

[26] López-López, A., Rogel, M.A., Ormeño-Orrillo, E., Martínez-Romero, J., Martínez-Romero, E., 2010. Phaseolus vulgaris seed-borne endophytic community with novel bacterial species such as Rhizobium endophyticum sp. nov. Systematic and Applied Microbiology33, 322–327.

[27] McClerklin, S.A., Lee, S.G., Harper, C.P., Nwumeh, R., Jez, J.M., Kunkel, B.N., 2018. Indole-3-acetaldehyde dehydrogenase-dependent auxin synthesis contributes to virulence of Pseudomonas syringae strain DC3000. PLoS Pathogens14, e1006811.

[28] Molina, R., Rivera, D., Mora, V., López, G., Rosas, S., Spaepen, S., Vanderleyden, J., Cassán, F., 2018. Regulation of IAA biosynthesis in Azospirillum brasilense under environmental stress conditions. Current Microbiology75, 1408–1418.

[29] Norton, R.M., 2016. Nitrogen management to optimise canola production in Australia. Crop and Pasture Science67, 419–438.

[30] Ojuederie, O.B., Olanrewaju, O.S., Babalola, O.O., 2019. Plant growth promoting rhizobacterial mitigation of drought stress in crop plants: implications for sustainable agriculture. Agronomy9, 712.

[31] Peoples, M.B., Brockwell, J., Herridge, D.F., Rochester, I.J., Alves, B.J.R., Urquiaga, S., Boddey, R.M., Dakora, F.D., Bhattarai, S., Maskey, S.L., Sampet, C., Rerkasem, B., Khan, D.F., Hauggaard-Nielsen, H., Jensen, E.S., 2009. The contributions of nitrogen-fixing crop legumes to the productivity of agricultural systems. Symbiosis48, 1–17.

[32] Peoples, M.B., Giller, K.E., Jensen, E.S., Herridge, D.F., 2021. Quantifying country-to-global scale nitrogen fixation for grain legumes: I. Reliance on nitrogen fixation of soybean, groundnut and pulses. Plant and Soil469, 1–14.

[33] Perera, I.A., Abinandan, S., Subashchandrabose, R.S., Venkateswarlu, K., Naidu, R., Megharaj, M., 2021. Microalgal–bacterial consortia unveil distinct physiological changes to facilitate growth of microalgae. FEMS Microbiology Ecology97, fiab012.

[34] Reza, M. T., Freitas, A., Yang, X.K., Hiibel, S., Lin, H.F., Coronella, C.J., 2016. Hydrothermal carbonization (HTC) of cow manure: carbon and nitrogen distributions in HTC products. Environmental Progress & Sustainable Energy35, 1002–1011.

[35] Ruíz-Valdiviezo, V.M., Canseco, L.M.C.V., Suárez, L.A.C., Gutiérrez-Miceli, F.A., Dendooven, L., Rincón-Rosales, R., 2015. Symbiotic potential and survival of native rhizobia kept on different carriers. Brazilian Journal of Microbiology46, 735–742.

[36] Santos, M.S., Nogueira, M.A., Hungria, M., 2019. Microbial inoculants: reviewing the past, discussing the present and previewing an outstanding future for the use of beneficial bacteria in agriculture. AMB Express9, 205.

[37] Shabir, R., Li, Y.T., Megharaj, M., Chen, C.R., 2024. Pyrolysis temperature affects biochar suitability as an alternative rhizobial carrier. Biology and Fertility of Soils60, 681–697.

[38] Shabir, R., Li, Y.T., Zhang, L.Y., Chen, C.R., 2023. Biochar surface properties and chemical composition determine the rhizobial survival rate. Journal of Environmental Management326, 116594.

[39] Shi, Q.S., Shi, W.Y., Kong, H.M., Jia, Y.F., Ni, L., Li, F.Y., Chen, Y.H., Ying, X., Zhang, J.J., Xu, P.P., 2021. Organic slow-release fertilizer prepared from livestock and poultry manure and straws as raw materials. CN Patent CN112624866A.

[40] Sivaram, A.K., Abinandan, S., Chen, C.R., Venkateswartlu, K., Megharaj, M., 2023. Microbial inoculant carriers: Soil health improvement and moisture retention in sustainable agriculture. Advances in Agronomy180, 35–91.

[41] Soni, R., Suyal, D.C., Yadav, A.N., Goel, R., 2022. Trends of Applied Microbiology for Sustainable Economy. London: Academic Press.

[42] Sosanwo, O.A., Fawcett, A.H., Apperley, D., 1995. ¹³C CP-MAS NMR spectra of tropical hardwoods. Polymer International36, 247–259.

[43] Stewart, W.M., Dibb, D.W., Johnston, A.E., Smyth, T.J., 2005. The contribution of commercial fertilizer nutrients to food production. Agronomy Journal97, 1–6.

[44] Sun, L.T., Wang, Y., Ma, D.X., Wang, L.L., Zhang, X.M., Ding, Y.Q., Fan, K., Xu, Z., Yuan, C.B., Jia, H.Z., Ren, Y.L., Ding, Z.T., 2022. Differential responses of the rhizosphere microbiome structure and soil metabolites in tea (Camellia sinensis) upon application of cow manure. BMC Microbiology22, 55.

[45] Trenkel, M.E., 1997. Improving fertilizer use efficiency: controlled-release and stabilized fertilizers in agriculture. Paris: International Fertilizer Industry Association, 151.

[46] Vitousek, P.M., Porder, S., Houlton, B.Z., Chadwick, O.A., 2010. Terrestrial phosphorus limitation: mechanisms, implications, and nitrogen-phosphorus interactions. Ecological Applications20, 5–15.

[47] Wang, K., He, C., You, S.J., Liu, W.J., Wang, W., Zhang, R.J., Qi, H.H., Ren, N.Q., 2015. Transformation of organic matters in animal wastes during composting. Journal of Hazardous Materials300, 745–753.

[48] Wardle, D.A., Walker, L.R., Bardgett, R.D., 2014. Ecosystem properties and forest decline in contrasting long-term chronosequences. Science305, 509–513.

[49] Wu, S.C., Cao, Z.H., Li, Z.G., Cheung, K.C., Wong, M.H., 2005. Effects of biofertilizer containing N-fixer, P and K solubilizers and AM fungi on maize growth: a greenhouse trial. Geoderma125, 155–166.

RIGHTS & PERMISSIONS

Higher Education Press