# Draft Genome Sequence of Plant Growth-Promoting Burkholderia sp. Strain BE12, Isolated from the Rhizosphere of Maize

Qassim Esmaeel, Lisa Sanchez, Mathilde Robineau, Stephan Dorey, Christophe Clément, Cédric Jacquard, Essaid Ait Barka

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## To cite this version:

Qassim Esmaeel, Lisa Sanchez, Mathilde Robineau, Stephan Dorey, Christophe Clément, et al.. Draft Genome Sequence of Plant Growth-Promoting Burkholderia sp. Strain BE12, Isolated from the Rhizosphere of Maize. Genome Announcements, 2018, 6 (17), pp.00299-18. 10.1128/genomeA.00299-18. hal-03284652

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Submitted on 12 Jul 2021

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# Draft Genome Sequence of Plant Growth-Promoting *Burkholderia* sp. Strain BE12, Isolated from the Rhizosphere of Maize

Qassim Esmaeel,ª Lisa Sanchez,ª Mathilde Robineau,ª Stephan Dorey,ª Christophe Clément,ª Cédric Jacquard,ª Essaid Ait Barkaª

ªUnité de Résistance Induite et Bioprotection des Plantes–EA 4707, UFR Sciences Exactes et Naturelles, University of Reims-Champagne-Ardenne, Reims, France

**ABSTRACT** *Burkholderia* sp. strain BE12, isolated from a French agricultural soil, possesses antifungal activity against a set of phytopathogenic fungi and has friendly interactions with grapevine. Here, we present the draft genome sequence of BE12, along with genes related to plant growth-promoting traits and siderophores that this strain contains, supporting its plant growth and antifungal activities.

The genus *Burkholderia* comprises more than 90 species that are distributed in a wide range of environments, including water, soil, plants, animals, and humans (1–4). The capacity of *Burkholderia* spp. to live in different ecological niches is due to their large genome size, ranging from 3 to 9 Mb, divided into 3 chromosomes and up to 5 plasmids (5). Several species of *Burkholderia* are well known for their potential role in plant growth promotion and protection in plants against soilborne pathogens (6–8). Thus, the capabilities of *Burkholderia* species to reduce yield losses and promote growth have led to increased interest in the use of *Burkholderia* strains as biocontrol and biostimulant microorganisms in agriculture. The strain described here, *Burkholderia* sp. BE12, was isolated from a French agricultural soil. In dual confrontation assays, this bacterium showed an inhibitory effect against *Botrytis cinerea*, *Fusarium oxysporum*, and *Rhizoctonia solani*.

This strain also has been screened and characterized, in vitro, for its potential plant growth-promoting (PGP) traits, including siderophore production, phosphate solubilization, and the production of phytohormones. An in vivo assay showed that *Burkholderia* sp. BE12 caused a significant increase in growth parameters of grapevine (*Vitis vinifera* L.) and was able to reduce the development of gray mold, caused by *B. cinerea*, on grapevine plantlets (unpublished data).

To better understand the PGP and biocontrol effects of this strain, the whole genome was sequenced. Total DNA was extracted using the Wizard genomic purification DNA kit (Promega Corp., Madison, WI, USA) and sequenced at MicrobesNG (http://www.microbesng.uk) using Illumina MiSeq and HiSeq 2500 technology platforms, with 2 to 250-bp paired-end reads. The closest existing reference genome was determined using Kraken (9), and the reads were mapped using the Burrows-Wheeler Aligner (BWA) MEM algorithm (http://bio-bwa.sourceforge.net) to assess data quality. The reads were assembled by de novo assembly using SPAdes (http://cab.spbu.ru/software/spades/). The draft genome of 7,472,757 bp includes 97 contigs with a GC content of 66.94% and an *N*<sub>50</sub> contig size of 180,386 bp. Gene function prediction was performed by the Rapid Annotations using Subsystems Technology (RAST) server (http://rast.nmpdr.org) (10) followed by an annotation using the SEED database (11), resulting in 71 RNAs and 7,040 coding sequences.

In silico analysis using antiSMASH (12) and RAST revealed the presence of a siderophore gene cluster and genes involved with the production of indole acetic acid (IAA), a plant hormone associated with plant growth (13). Furthermore, the genome se-

**Received** 9 March 2018 **Accepted** 19 March 2018 **Published** 26 April 2018

**Citation** Esmaeel Q, Sanchez L, Robineau M, Dorey S, Clément C, Jacquard C, Barka EA. 2018. Draft genome sequence of plant growth-promoting *Burkholderia* sp. strain BE12, isolated from the rhizosphere of maize. Genome Announc 6:e00299-18. https://doi.org/10.1128/genomeA.00299-18.

**Copyright** © 2018 Esmaeel et al. This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license.

Address correspondence to Essaid Ait Barka, ea.barka@univ-reims.fr.
quence indicates the presence of pyrroloquinoline quinone synthase and glucose dehydrogenase (implicated in the production of gluconic acid) and 2-ketogluconic acid production (involved in mineral phosphate solubilization) (14). The annotated genome also has 15 genes related to *N*-acylhomoserine lactone, which is involved in the quorum-sensing system, and 1 gene related to 1-aminocyclopropane-1-carboxylate (ACC) deaminase, which potentially plays a role in promoting plant growth (15). In addition, the genome has genes contributing to cell wall degradation, such as endoglucanase and cellulase, and motility proteins. All these features may explain the ability of *Burkholderia* sp. BE12 to successfully promote plant growth and protect plants from disease.

**Accession number(s).** This whole-genome shotgun project has been deposited in GenBank under the accession no. PREY00000000. The version described in this paper is the first version, PREY01000000.

## ACKNOWLEDGMENTS

This work was supported by the University of Reims Champagne-Ardenne and the INTERREGV program (BioScreen project).

We thank MicrobesNG, supported by the BBSRC (grant BB/L024209/1), for genome sequencing.

## REFERENCES

1. Eberl L, Vandamme P. 2016. Members of the genus *Burkholderia*: good and bad guys. F1000Res 5:1007. https://doi.org/10.12688/f1000research.8221.1.

2. Depoorter E, Bull MJ, Peeters C, Coenye T, Vandamme P, Mahenthiral-ingam E. 2016. *Burkholderia*: an update on taxonomy and biotechnolog-ical potential as antibiotic producers. Appl Microbiol Biotechnol 100: 5215–5229. https://doi.org/10.1007/s00253-016-7520-x.

3. Sawana A, Adeolu M, Gupta RS. 2014. Molecular signatures and phylog-enomic analysis of the genus *Burkholderia*: proposal for division of this genus into the emended genus *Burkholderia* containing pathogenic organisms and a new genus *Paraburkholderia* gen. nov. harboring en-vironmental species. Front Genet 5 https://doi.org/10.3389/fgene.2014.00429.

4. Compant S, Nowak J, Coenye T, Clément C, Ait Barka E. 2008. Diversity and occurrence of *Burkholderia* spp. in the natural environment. FEMS Microbiol Rev 32:607–626. https://doi.org/10.1111/j.1574-6976.2008.00113.x.

5. Esmaeel Q, Pupin M, Kieu NP, Chataigné G, Béchet M, Deravel J, Krier F, Höfte M, Jacques P, Leclère V. 2016. *Burkholderia* genome mining for nonribosomal peptide synthetases reveals a great potential for novel siderophores and lipopeptides synthesis. MicrobiologyOpen 5:512–526. https://doi.org/10.1002/mbo3.347.

6. Esmaeel Q, Pupin M, Jacques P, Leclère V. 2017. Nonribosomal peptides and polyketides of *Burkholderia*: new compounds potentially implicated in biocontrol and pharmaceuticals. Environ Sci Pollut Res https://doi.org/10.1007/s11356-017-9166-3.

7. Paungfoo-Lonhienne C, Lonhienne TG, Yeoh YK, Webb RI, Laksh-manan P, Chan CX, Lim PE, Ragan MA, Schmidt S, Hugenholtz P. 2014. A new species of *Burkholderia* isolated from sugarcane roots pro-motes plant growth. Microb Biotechnol 7:142–154. https://doi.org/10.1111/1751-7915.12105.

8. Kim S, Lowman S, Hou G, Nowak J, Flinn B, Mei C. 2012. Growth promotion and colonization of switchgrass (*Panicum virgatum*) cv.

Alamo by bacterial endophyte *Burkholderia phytofirmans* strain PsJN. Biotechnol Biofuels 5:37. https://doi.org/10.1186/1754-6834-5-37.

9. Wood DE, Salzberg SL. 2014. Kraken: ultrafast metagenomic sequence classification using exact alignments. Genome Biol 15:R46. https://doi.org/10.1186/gb-2014-15-3-r46.

10. Aziz RK, Bartels D, Best AA, DeJongh M, Disz T, Edwards RA, Formsma K, Gerdes S, Glass EM, Kubal M, Meyer F, Olsen GJ, Olson R, Osterman AL, Overbeek RA, McNeil LK, Paarmann D, Paczian T, Parrello B, Pusch GD, Reich C, Stevens R, Vassieva O, Vonstein V, Wilke A, Zagnitko O. 2008. The RAST server: Rapid Annotations using Subsystems Technology. BMC Genomics 9:75. https://doi.org/10.1186/1471-2164-9-75.

11. Disz T, Akhter S, Cuevas D, Olson R, Overbeek R, Vonstein V, Stevens R, Edwards RA. 2010. Accessing the SEED genome databases via Web services API: tools for programmers. BMC Bioinformatics 11:319. https://doi.org/10.1186/1471-2105-11-319.

12. Weber T, Blin K, Duddela S, Krug D, Kim HU, Bruccoleri R, Lee SY, Fischbach MA, Müller R, Wohlleben W, Breitling R, Takano E, Medema MH. 2015. antiSMASH 3.0—a comprehensive resource for the genome mining of biosynthetic gene clusters. Nucleic Acids Res 43:W237–W243. https://doi.org/10.1093/nar/gkv437.

13. Malhotra S, Mishra V, Karmakar S, Sharma RS. 2017. Environmental predictors of indole acetic acid producing rhizobacteria at fly ash dumps: nature-based solution for sustainable restoration. Front Environ Sci 5 https://doi.org/10.3389/fenvs.2017.00059.

14. Chhabra S, Brazil D, Morrissey J, Burke JI, O’Gara F, Dowling DN. 2013. Characterization of mineral phosphate solubilization traits from a barley rhizosphere soil functional metagenome. MicrobiologyOpen 2:717–724. https://doi.org/10.1002/mbo3.110.

15. Govindasamy V, Senthilkumar M, Gaikwad K, Annapurna K. 2008. Isola-tion and characterization of ACC deaminase gene from two plant growth-promoting rhizobacteria. Curr Microbiol 57:312–317. https://doi.org/10.1007/s00284-008-9195-8.