Abstract
Here we report the complete genome sequence of a plant growth-promoting rhizobacterium (PGPR), Paenibacillus polymyxa SQR-21, which consists of one circular chromosome of 5,828,438 bp with 5,024 coding sequences (CDS). The data presented highlight multiple sets of functional genes associated with its plant-beneficial characteristics.
GENOME ANNOUNCEMENT
Paenibacillus polymyxa (formerly Bacillus polymyxa), a Gram-positive, sporulating bacterium, is considered to be a plant growth-promoting rhizobacterium (PGPR) (1, 2). Originally isolated from various environmental samples (3, 4), P. polymyxa has been widely applied in agriculture, industry, medicine, and environmental remediation (5–12). Thus far, only four P. polymyxa genomes, those of P. polymyxa E681 (NC_014483) (13), P. polymyxa SC2 (NC_014622) (14), P. polymyxa M1 (NC_017542) (1), and P. polymyxa CR1 (NC_023037) (15), have been completely sequenced. P. polymyxa SQR-21 was naturally isolated from watermelon rhizosphere. As an outstanding PGPR strain with the ability to produce various antibiotics (16, 17) and colonize rhizospheres (18), SQR-21 has been widely exploited in commercial biofertilizers for plant growth promotion and biological control of soilborne plant pathogens (19, 20). Here, we report the whole-genome sequence of SQR-21 in order to better elucidate its plant-beneficial characteristics and promote its agricultural applications.
Whole-genome sequencing of P. polymyxa SQR-21 was performed with Roche 454 sequencing technology. The constructed library was sequenced by the GS FLX Titanium series chemistry. A total of 1,000,000 sequence reads with average read lengths of 350 to 450 bp (resulting in up to 400 Mb of sequence data) were obtained, representing an average of 70-fold coverage of the genome. The reads were assembled into 19 scaffolds, and the 54 sequence gaps both within and between the scaffolds were filled by sequencing PCR products using an ABI 3730 capillary sequencer.
The complete genome of P. polymyxa SQR-21 is composed of a 5,828,438-bp circular chromosome, with a mean GC content of 45.64%. Based on the genomic data, 5,024 coding sequences (CDS) were predicted by GeneMark (21) and annotated by a BLAST tools search against the GenBank nonredundant protein database (NR), Kyoto Encyclopedia of Genes and Genomes (KEGG), and Clusters of Orthologous Groups (COG). In addition, 111 tRNA loci and 13 rRNA operons were identified with the tRNAscan-SE (22) and RNAmmer 1.2 (23) servers, respectively.
P. polymyxa SQR-21 harbors four nonribosomal peptide synthetase (NRPS) gene clusters, including pmx and fus gene clusters responsible for biosynthesis of polymyxin and fusaricidin, respectively, which reveal high similarities to the published gene clusters (24–26). One polyketide synthetase (PKS) gene cluster, three hybrid PKS-NRPS gene clusters, and three gene clusters relevant to lantibiotic biosynthesis are also present in the SQR-21 genome. Several genes involved in plant growth promotion, including genes responsible for production of indole-3-acetic acid (IAA), 3-hydroxy-2-butanone (acetoin), and 2,3-butanediol, as well as phytase, were identified in the SQR-21 genome. In addition, the genome harbors a set of genes encoding extracellular enzymes involved in the degradation of plant-derived polysaccharides, including xylanase, glucanase, and chitinase. Given the strain specificity and application in agricultural production, the complete genome sequence of P. polymyxa SQR-21 provides useful information for both basic and applied research, which also facilitates the understanding of the functions and evolutions of the Paenibacillus polymyxa genome.
Nucleotide sequence accession number.
The complete sequence of Paenibacillus polymyxa SQR-21 has been deposited in NCBI’s GenBank under the accession number CP006872.
ACKNOWLEDGMENTS
This research was financially supported by the Nature Science Foundation of China (31301845 and 31330069), the Chinese Ministry of Science and Technology (2013AA102802), and the Fundamental Research Funds for the Central Universities (KYZ201307). R.Z. and Q.S. were also supported by the 111 Project (B12009) and the Priority Academic Program Development (PAPD) of Jiangsu Higher Education Institutions.
Footnotes
Citation Li S, Yang D, Qiu M, Shao J, Guo R, Shen B, Yin X, Zhang R, Zhang N, Shen Q. 2014. Complete genome sequence of Paenibacillus polymyxa SQR-21, a plant growth-promoting rhizobacterium with antifungal activity and rhizosphere colonization ability. Genome Announc. 2(2):e00281-14. doi:10.1128/genomeA.00281-14.
REFERENCES
- 1. Niu B, Rueckert C, Blom J, Wang Q, Borriss R. 2011. The genome of the plant growth-promoting rhizobacterium Paenibacillus polymyxa M-1 contains nine sites dedicated to nonribosomal synthesis of lipopeptides and polyketides. J. Bacteriol. 193:5862–5863. 10.1128/JB.05806-11 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 2. Timmusk S. 2003. Mechanism of action of the plant growth promoting bacterium Paenibacillus polymyxa. Ph.D. thesis Uppsala University, Uppsala, Sweden [Google Scholar]
- 3. Lal S, Romano S, Chiarini L, Signorini A, Tabacchioni S. 2012. The Paenibacillus polymyxa species is abundant among hydrogen-producing facultative anaerobic bacteria in Lake Averno sediment. Arch. Microbiol. 194:345–351. 10.1007/s00203-011-0763-0 [DOI] [PubMed] [Google Scholar]
- 4. McSpadden Gardener BB. 2004. Ecology of Bacillus and Paenibacillus spp. in agricultural systems. Phytopathology 94:1252–1258. 10.1094/PHYTO.2004.94.11.1252 [DOI] [PubMed] [Google Scholar]
- 5. Lal S, Tabacchioni S. 2009. Ecology and biotechnological potential of Paenibacillus polymyxa: a minireview. Indian J. Microbiol. 49:2–10. 10.1007/s12088-009-0008-y [DOI] [PMC free article] [PubMed] [Google Scholar]
- 6. Raza W, Wang Y, Shen QR. 2008. Paenibacillus polymyxa: antibiotics, hydrolytic enzymes and hazard assessment. J. Plant Pathol. 90:419–430 [Google Scholar]
- 7. Niu B, Vater J, Rueckert C, Blom J, Lehmann M, Ru JJ, Chen XH, Wang Q, Borriss R. 2013. Polymyxin P is the active principle in suppressing phytopathogenic Erwinia spp. by the biocontrol rhizobacterium Paenibacillus polymyxa M-1. BMC Microbiol. 13:137. 10.1186/1471-2180-13-137 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 8. Anand R, Grayston S, Chanway C. 2013. N2-fixation and seedling growth promotion of lodgepole pine by endophytic Paenibacillus polymyxa. Microb. Ecol. 66:369–374. 10.1007/s00248-013-0196-1 [DOI] [PubMed] [Google Scholar]
- 9. Haggag WM, Timmusk S. 2008. Colonization of peanut roots by biofilm-forming Paenibacillus polymyxa initiates biocontrol against crown rot disease. J. Appl. Microbiol. 104:961–969. 10.1111/j.1365-2672.2007.03611.x [DOI] [PubMed] [Google Scholar]
- 10. Yu B, Sun J, Bommareddy RR, Song L, Zeng AP. 2011. Novel (2R,3R)-2,3-butanediol dehydrogenase from potential industrial strain Paenibacillus polymyxa ATCC 12321. Appl. Environ. Microbiol. 77:4230–4233. 10.1128/AEM.02998-10 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 11. He Z, Kisla D, Zhang L, Yuan C, Green-Church KB, Yousef AE. 2007. Isolation and identification of a Paenibacillus polymyxa strain that coproduces a novel lantibiotic and polymyxin. Appl. Environ. Microbiol. 73:168–178. 10.1128/AEM.02023-06 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 12. Ariza A, Eklöf JM, Spadiut O, Offen WA, Roberts SM, Besenmatter W, Friis EP, Skjøt M, Wilson KS, Brumer H, Davies G. 2011. Structure and activity of Paenibacillus polymyxa xyloglucanase from glycoside hydrolase family 44. J. Biol. Chem. 286:33890–33900. 10.1074/jbc.M111.262345 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 13. Kim JF, Jeong H, Park SY, Kim SB, Park YK, Choi SK, Ryu CM, Hur CG, Ghim SY, Oh TK, Kim JJ, Park CS, Park SH. 2010. Genome sequence of the polymyxin-producing plant-probiotic rhizobacterium Paenibacillus polymyxa E681. J. Bacteriol. 192:6103–6104. 10.1128/JB.00983-10 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 14. Ma M, Wang C, Ding Y, Li L, Shen D, Jiang X, Guan D, Cao F, Chen H, Feng R, Wang X, Ge Y, Yao L, Bing X, Yang X, Li J, Du B. 2011. Complete genome sequence of Paenibacillus polymyxa Sc2, a strain of plant growth-promoting rhizobacterium with broad-spectrum antimicrobial activity. J. Bacteriol. 193:311–312. 10.1128/JB.01234-10 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 15. Eastman AW, Weselowski B, Nathoo N, Yuan Z-C. 2014. Complete genome sequence of Paenibacillus polymyxa CR1, a plant growth-promoting bacterium isolated from the corn rhizosphere exhibiting potential for biocontrol, biomass degradation, and biofuel production. Genome Announc. 2(1):e01218-13. 10.1128/genomeA.01218-13 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 16. Li S, Zhang R, Wang Y, Zhang N, Shao J, Qiu M, Shen B, Yin X, Shen Q. 2013. Promoter analysis and transcription regulation of fus gene cluster responsible for fusaricidin synthesis of Paenibacillus polymyxa SQR-21. Appl. Microbiol. Biotechnol. 97:9479–9489. 10.1007/s00253-013-5157-6 [DOI] [PubMed] [Google Scholar]
- 17. Raza W, Yang XM, Wu HS, Wang Y, Xu YC, Shen QR. 2009. Isolation and characterisation of fusaricidin-type compound-producing strain of Paenibacillus polymyxa SQR-21 active against Fusarium oxysporum f. sp. nevium. Eur. J. Plant Pathol. 125:471–483. 10.1007/s10658-009-9496-1 [DOI] [Google Scholar]
- 18. Ling N, Zhang WW, Tan SY, Huang QW, Shen QR. 2012. Effect of the nursery application of bioorganic fertilizer on spatial distribution of Fusarium oxysporum f. sp. niveum and its antagonistic bacterium in the rhizosphere of watermelon. Appl. Soil Ecol. 59:13–19. 10.1016/j.apsoil.2012.05.001 [DOI] [Google Scholar]
- 19. Ling N, Xue C, Huang QW, Yang XM, Xu YC, Shen QR. 2010. Development of a mode of application of bioorganic fertilizer for improving the biocontrol efficacy to Fusarium wilt. BioControl 55:673–683. 10.1007/s10526-010-9290-1 [DOI] [Google Scholar]
- 20. Wu HS, Yang XN, Fan JQ, Miao WG, Ling N, Xu YC, Huang QW, Shen QR. 2009. Suppression of fusarium wilt of watermelon by a bio-organic fertilizer containing combinations of antagonistic microorganisms. BioControl 54:287–300. 10.1007/s10526-008-9168-7 [DOI] [Google Scholar]
- 21. Borodovsky M, Mills R, Besemer J, Lomsadze A. 2003. Prokaryotic gene prediction using GeneMark and GeneMark.hmm. Curr. Protoc. Bioinformatics 1:4.5.1–4.5.16. 10.1002/0471250953.bi0405s01 [DOI] [PubMed] [Google Scholar]
- 22. Lowe TM, Eddy SR. 1997. tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res. 25:955–964. 10.1093/nar/25.5.0955 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 23. Lagesen K, Hallin P, Rødland EA, Staerfeldt HH, Rognes T, Ussery DW. 2007. RNAmmer: consistent and rapid annotation of ribosomal RNA genes. Nucleic Acids Res. 35:3100–3108. 10.1093/nar/gkm160 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 24. Choi SK, Park SY, Kim R, Kim SB, Lee CH, Kim JF, Park SH. 2009. Identification of a polymyxin synthetase gene cluster of Paenibacillus polymyxa and heterologous expression of the gene in Bacillus subtilis. J. Bacteriol. 191:3350–3358. 10.1128/JB.01728-08 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 25. Choi SK, Park SY, Kim R, Lee CH, Kim JF, Park SH. 2008. Identification and functional analysis of the fusaricidin biosynthetic gene of Paenibacillus polymyxa E681. Biochem. Biophys. Res. Commun. 365:89–95. 10.1016/j.bbrc.2007.10.147 [DOI] [PubMed] [Google Scholar]
- 26. Li J, Jensen SE. 2008. Nonribosomal biosynthesis of fusaricidins by Paenibacillus polymyxa PKB1 involves direct activation of a d-amino acid. Chem. Biol. 15:118–127. 10.1016/j.chembiol.2007.12.014 [DOI] [PubMed] [Google Scholar]