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Genomic characterization of Nitrospirillum amazonense strain CBAmC, a nitrogen-fixing bacterium isolated from surface-sterilized sugarcane stems

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Abstract

Nitrospirillum amazonense is a nitrogen-fixing bacterium that shows potential to promote plant growth when inoculated into sugarcane and rice plants. This microorganism has been the subject of biochemical and genetic characterization to elucidate important functions related to host plant interaction and growth promotion, including the determination of draft genome sequences of two strains, Y2 and CBAmC, the second of which is the aim of the present study. CBAmC has been isolated from sugarcane (Saccharum spp.), and is currently used in a sugarcane consortium inoculant with four other nitrogen-fixing bacterial strains. The present paper describes a significant improvement in the genome sequence and assembly for the N. amazonense strain CBAmC, and determination for the first time of a complete genome sequence for this bacterial species, using PacBio technology. The analysis of the genomic data obtained allowed the discovery of genes coding for metabolic pathways and cellular structures that may be determinant for the success of the bacterial establishment and colonization into the host sugarcane plant, besides conferring important characteristics to the inoculant. These include genes for the use of sucrose and N-glycans, biosynthesis of autoinducer molecules, siderophore production and acquisition, auxin and polyamine biosynthesis, flagellum, σ-fimbriae, a variety of secretion systems, and a complete denitrification system. Concerning genes for nitrogenase and auxiliary proteins, it was possible to corroborate literature data that in N. amazonense these probably had originated from horizontal gene transfer, from bacteria of the Rhizobiales order. The complete genomic sequence of the CBAmC strain of N. amazonense revealed that the bacterium harbors four replicons, including three chromosomes and one chromid, a profile that coincides with that of other two strains, according to literature data, suggesting that as a replicon pattern for the species. Finally, results of phylogenomic analyses in this work support the recent reclassification of the species, separating it from the Azospirillum genus. More importantly, results of the present work shall guide subsequent studies on strain CBAmC as well as the development of a sugarcane inoculant.

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Acknowledgements

The authors acknowledge Jean L. Simões-Araújo for bioinformatics hints, Marcia S. Vidal for preparing genomic DNA for Illumina sequencing, Marcia R. R. Coelho, Ederson da C. Jesus and Alexandre C. Baraúna for suggestions on phylogenomic analyses, Hugo R. Borges de Freitas for bioinformatics support, and M. Christine Saraiva Barbosa for making Fig. 2.

Funding

This study was funded by The National Council for Scientific and Technological Development (CNPq-“National Institute of Science and Technology of Biological Nitrogen Fixation”, Grant No. 573.828/2008-3, J.I.B. Grant “Universal” No. 476254/2013-2, and J.I.B. research fellowship no. 304750/2013), Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro (Faperj – J.I.B. “Cientista do Nosso Estado” research fellowship no. E-26/102.312/2013, and S.S. Grant “Desenvolvimento Científico e Tecnológico Regional” no. E-26/110.235/2011), Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES-L.A.T. doctorate fellowship, call CAPES/Embrapa no. 015/2014), and Brazilian Agricultural Research Corporation (Embrapa).

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Authors and Affiliations

  1. Instituto Nacional de Ciência e Tecnologia da Fixação Biológica de Nitrogênio, CNPq, Curitiba, Brazil

    Stefan Schwab, Leonardo Araujo Terra & José Ivo Baldani

  2. Embrapa Agrobiologia, Rodovia BR 465, km 7, Seropédica, RJ, 23891-000, Brazil

    Stefan Schwab, Leonardo Araujo Terra & José Ivo Baldani

  3. Pró-Reitoria de Pesquisa e Pós-Graduação, Universidade Federal Rural do Rio de Janeiro, Rodovia BR 465, km 7, Seropédica, RJ, 23890-000, Brazil

    Leonardo Araujo Terra

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  1. Stefan Schwab
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Correspondence to Stefan Schwab.

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Stefan Schwab declares that he has no conflict of interest. Leonardo Araujo Terra declares that he has no conflict of interest. José Ivo Baldani declares that he has no conflict of interest.

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This article does not contain any studies with human participants or animals performed by any of the authors.

Additional information

Communicated by S. Hohmann.

Electronic supplementary material

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Supplementary Table S1

Genome annotation data for N. amazonense strain CBAmC according to RAST and NCBI (XLSX 7798 KB)

Supplementary Table S2

Phylogenomics analysis data (XLSX 37 KB)

Supplementary Table S3

Detailed description of potential genomic islands on the four replicons of N. amazonense strain CBAmC according to IslandViewer 4 (XLSX 49 KB)

Supplementary Table S4

Interesting functions potentially exerted / proteins synthesized by N. amazonense strain CBAmC, according to further genomic datamining (PDF 274 KB)

Supplementary Figure S1

Electronic micrographs of N. amazonense strain CBAmC after growth on BMS medium, exhibiting intracellular granules of poly-β-hydroxybutyrate (PHB) (DOCX 132 KB)

Supplementary Figure S2

Synteny between the ordered contigs of strain Y2 and each of the four CBAmC replicons (DOCX 129 KB)

Supplementary Figure S3

Phylogenetic trees obtained with representative strains of the Nitrospirillum-Niveispirillum-Rhodocista-Azospirillum-Skermanella clade, and Bradyrhizobium and Rhodospirillum as external group (DOCX 196 KB)

Supplementary Figure S4

Genome size and percent GC of the Nitrospirillum–Niveispirillum–Rhodocista–Azospirillum–Skermanella clade in comparison with 7293 finished bacterial genomes (DOCX 704 KB)

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Schwab, S., Terra, L.A. & Baldani, J.I. Genomic characterization of Nitrospirillum amazonense strain CBAmC, a nitrogen-fixing bacterium isolated from surface-sterilized sugarcane stems. Mol Genet Genomics 293, 997–1016 (2018). https://doi.org/10.1007/s00438-018-1439-0

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