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Cyanobacterial biofertilizer inoculation has a distinctive effect on the key genes of carbon and nitrogen cycling in paddy rice

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Abstract

Cyanobacterial biofertilizers provide soil fertility and productivity gains at varying levels in paddy rice cultivation. The colonization and influences of introduced strains in different soil types with characteristic compositions of native cyanobacteria remain largely unknown. In this work, seven paddy rice soils with the composition of indigenous cyanobacteria described by amplicon sequencing analysis were inoculated with the cyanobacterial biofertilizer. The microbial abundance and the cyanophage concentrations were evaluated under light-dark or continuous dark cycles using quantitative polymerase chain reaction (qPCR) assays. The copies of cyanobacterial-16S rRNA gene markers varied from 5.65 × 106 to 9.22 × 107 g-1 soil, and their abundance increased significantly in the inoculated soils. The cyanophage concentrations, quantified using the capsid assembly protein gene g20 in the soils tested, ranged from 3.04 × 108 to 9.24× 108 g-1 soil on 30 days after incubation. There were significant increases in the abundance of the nifH gene copies, about 1.54×105 to 1.35×106 g-1, in the inoculated soils, albeit with soil type-specific responses. The gene markers of C and N cycling (i.e., cbbL and nifH, respectively), taxonomic markers (of archaea, bacteria, and cyanobacteria), and cyanophage-specific gene copies showed strong and positive correlation with the cyanobacterial biofertilizer inoculation. However, the genes related to nitrification (bacterial and archaeal amoA) and denitrification (nirS, nirK, narG, and nosZ) were clustered together in the uninoculated soils. The rice rhizospheres in three representative paddy soil types, using metatranscriptomics analysis, showed distinctive colonization by cyanobacteria, with several members yet to be described. These results indicate the potential for improving cyanobacterial biofertilizers for their contributions to plant growth and fertility gains in a soil-specific way.

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Availability of data and materials

Datasets that support the findings of qPCR analysis and amplicon sequencing in this study are available from the corresponding author [B. R.], upon reasonable request. Datasets that support the findings of metatranscriptomics analysis in the study are available in the online repositories. The names of the repository(ies) and accession number(s) can be found below: https://www.ncbi.nlm.nih.gov/sra/PRJNA1003687

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Acknowledgments

The authors thank Dr. Gerard Abraham for providing the cyanobacterial cultures, and the Division of Microbiology, ICAR-Indian Agricultural Research Institute, New Delhi, and the National Phytotron Facility (NPF), ICAR-IARI, New Delhi for the necessary facilities to conduct the experiments.

B. K. acknowledges the IARI Senior Scholarship for her doctoral studies. P. S. thanks the Graduate School, ICAR-IARI for the internship. R. S., S.G., and S. K. thank the Graduate School for the fellowships. B. R. thanks the funding agencies for their support for the projects on 'Soil microbiome modulation strategies to enhance nitrogen acquisition efficiency in rice (ICAR-NRM. 11(16)/2015-AFC(8))' and 'Archaeal- and anaerobic ammonia oxidative processes of nitrogen cycling in oxic and anoxic soils (SERB/SR/S0/PS/164/2010).'

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  1. Preeti Sharma

    Present address: Institute for Informatics, Data Science & Biostatistics, Washington University School of Medicine in St. Louis, Washington University in St. Louis, St. Louis, USA

Authors and Affiliations

  1. Division of Microbiology, ICAR-Indian Agricultural Research Institute, New Delhi, India

    Babanpreet Kour, Preeti Sharma, S. Ramya, K Sudheer & Balasubramanian Ramakrishnan

  2. Division of Agronomy, ICAR-Indian Agricultural Research Institute, New Delhi, India

    Sandeep Gawdiya

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Contributions

B. K.: Conducting experiments, sample processing, data collection, data analysis, statistical analysis, and writing-original draft.

P. S.: Sample collection, soil physicochemical analysis, and contributed to writing the results section.

R. S.: Analyses, reviewing, and editing of the manuscript.

S. G.: Soil physicochemical analysis and editing of manuscript.

S. K.: Sample processing, analyses, and editing of the manuscript.

B. R.: Funding, Research supervision, methodology, data validation, reviewing and editing of the manuscript.

* All authors reviewed the manuscript.

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Correspondence to Balasubramanian Ramakrishnan.

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Kour, B., Sharma, P., Ramya, S. et al. Cyanobacterial biofertilizer inoculation has a distinctive effect on the key genes of carbon and nitrogen cycling in paddy rice. J Appl Phycol (2024). https://doi.org/10.1007/s10811-024-03230-0

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