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The Effect of Inoculation of a Diazotrophic Bacterial Consortium on the Indigenous Bacterial Community Structure of Sugarcane Apoplast Fluid

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Abstract

The extracellular space in plants, termed the apoplast, has a pH and sugar content that enables bacterial growth and represents a possible niche for the establishment of endophytic bacteria. Previous studies have investigated the effects of diazotrophic bacteria inoculation in sugarcane varieties, but it has not yet been analyzed how the microbial community of apoplast fluid of sugarcane is affected. High-throughput next generation sequencing of the 16S rRNA gene was used throughout this study to determine the effect of inoculation with a diazotrophic bacteria consortium, previously isolated from sugarcane, on the native bacterial population of sugarcane variety RB867515 grown in the field. The analyses were carried out 450 days after inoculation. The results revealed the presence of 22 phyla, with predominance of Proteobacteria phylum. It was observed that the inoculated consortium changed the indigenous bacterial community structure of sugarcane apoplast fluid by decreasing diversity and evenness, interfering in the composition of rare species. Microbial community composition analysis revealed differences between treatments. The differential abundance test showed there were 43 amplicon sequence variants (ASVs) which were relatively more abundant in the inoculated treatment, with predominance of the Sphingomonas genus. The predicted functions of the most abundant ASVs revealed the presence of genera related to plant growth promotion and protection against phytopathogens. Analysis to evaluate the occurrence of inoculated strains in the recovered data was not conclusive since the ASVs taxonomically close to the inoculated bacteria were observed in low abundance. The present study is the first report to elucidate the bacterial community in sugarcane apoplast fluid using a culture-independent approach. It demonstrated that the diazotrophic bacterial consortium interferes in the natural bacterial community in sugarcane variety RB867515.

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Acknowledgements

We thank Segundo Urquiaga (Embrapa Agrobiologia) and Doãn S. Martins (UFRRJ) for providing the stem sugarcane samples from the field experiment. We are grateful to the students at Embrapa Agrobiologia in the Laboratory of Genetics and Biochemistry (LGB) for their work with apoplast processing and Michelle Z. T. Sfeir and Valter A. de Baura (Universidade Federal do Paraná) for help with Illumina sequencing of the samples.

Funding

This work was partially financed by the projects CNPq/INCT-FBN (573828/2008-3), FAPERJ–CNE (E-26/203.011/2016), and Embrapa MP2 (02.16.05.017.00.00). CMS and NVSR were supported by a fellowship from FAPERJ (E-26/200.952/2018) and (E-26/202.015/2019), respectively; JIB (306011/2017-4) received a fellowship from CNPq.

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  1. Laboratório de Genética e Bioquímica, Embrapa Agrobiologia, Rodovia BR 465, km 7, Seropédica, RJ, CEP 23891-000, Brazil

    Carlos M. Dos-Santos, Náthalia V. S. Ribeiro, Stefan Schwab, José I. Baldani & Marcia S. Vidal

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Contributions

MSV, JIB and SS designed and directed the project. NVSR carried out the experimental analysis. CMD-S performed and interpreted the results of the bioinformatics and statistical analysis. All authors discussed the results and commented on the manuscript. CMD-S wrote the manuscript with support from SS, JIB and MSV. All authors read and approved the final manuscript.

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Correspondence to Marcia S. Vidal.

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Supplementary Information

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Supplementary file1 (XLSX 9 kb) DNA sample evaluation by spectrophotometry and spectrofluorimetry

284_2021_2571_MOESM2_ESM.tif

Supplementary file2 (TIF 2027 kb) Molecular profiles of 16S rRNA gene amplicons obtained using primers 799F and 1492R. Bands with ~1,000 bp and ~700 bp are related to plant (mitochondrial) and bacterial amplicons, respectively. M, 1 kb Plus DNA ladder (Invitrogen); N, PCR negative control; P, PCR positive control (using DNA from a bacterial control)

284_2021_2571_MOESM3_ESM.xlsx

Supplementary file3 (XLSX 273 kb) List of ASVs detected in the present study, respectively number of reads and relatives abundances for each sample, taxonomical classification and its treatment detection

284_2021_2571_MOESM4_ESM.xlsx

Supplementary file4 (XLSX 49 kb) The ASVs differentially abundant observed by DAT. Log2FoldChange values < 0.00 represents low abundant ASVs in the inoculated treatment and > 0.00 more abundant ASVs

284_2021_2571_MOESM5_ESM.xlsx

Supplementary file5 (XLSX 259 kb) Predicted functions capabilities of the more abundant ASVs of the inoculated treatment and the mined genes related to plant growth promotion

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Dos-Santos, C.M., Ribeiro, N.V.S., Schwab, S. et al. The Effect of Inoculation of a Diazotrophic Bacterial Consortium on the Indigenous Bacterial Community Structure of Sugarcane Apoplast Fluid. Curr Microbiol 78, 3079–3091 (2021). https://doi.org/10.1007/s00284-021-02571-0

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