1887

Abstract

pv. () is a serious pathogen causing bacterial blight disease in rice. Population genomic studies have revealed that rampant inter-strain rather than inter-lineage differences are contributing to the evolutionary success of this pathogen. Here, we report the complete genome sequence of BXO1, a strain of belonging to a dominant lineage from India. A complete genome-based investigation revealed the presence of two plasmids, pBXO1-1 (66.7 kb) and pBXO1-2 (25.6 kb). The pBXO1-1 plasmid encodes 71 genes, 38 of which encode hypothetical proteins of unknown function. However, these hypothetical genes possess atypical GC content, pointing towards their acquisition and movement through horizontal gene transfer. Interestingly, pBXO1-2 encodes a type IV secretion system (T4SS), which is known to play an important role in the conjugative transfer of genetic material, and also provides fitness to pathogenic bacteria for their enhanced survival. Neither plasmid has been reported previously in any other complete genome published to date. Our analysis also revealed that the pBXO1-2 plasmid is present in str. GPE PC73, which is known to cause leaf scald, a lethal disease in sugarcane. Our complete genome sequence analysis of BXO1 has provided us with detailed insights into the two novel strain-specific plasmids, in addition to decoding their functional capabilities, which were not assessable when using the draft genome sequence of the strain. Overall, our study has revealed the mobility of a novel T4SS in two pathogenic species of that infect the vascular tissues of two economically important monocot plants, i.e. rice and sugarcane.

Loading

Article metrics loading...

/content/journal/acmi/10.1099/acmi.0.000063
2019-09-19
2019-10-23
Loading full text...

Full text loading...

/deliver/fulltext/acmi/10.1099/acmi.0.000063/acmi000063.html?itemId=/content/journal/acmi/10.1099/acmi.0.000063&mimeType=html&fmt=ahah

References

  1. Mishra D, Vishnupriya MR, Anil MG, Konda K, Raj Y et al. Pathotype and genetic diversity amongst Indian isolates of Xanthomonas oryzae pv. oryzae. PLoS One 2013;8:e81996 [CrossRef]
    [Google Scholar]
  2. Patil PB, Bogdanove AJ, Sonti RV. The role of horizontal transfer in the evolution of a highly variable lipopolysaccharide biosynthesis locus in xanthomonads that infect rice, citrus and crucifers. BMC Evol Biol 2007;7:243 [CrossRef]
    [Google Scholar]
  3. Midha S, Bansal K, Kumar S, Girija AM, Mishra D et al. Population genomic insights into variation and evolution of Xanthomonas oryzae pv. oryzae. Sci Rep 2017;7:40694 [CrossRef]
    [Google Scholar]
  4. Gochez AM, Huguet-Tapia JC, Minsavage GV, Shantaraj D, Jalan N et al. Pacbio sequencing of copper-tolerant Xanthomonas citri reveals presence of a chimeric plasmid structure and provides insights into reassortment and shuffling of transcription activator-like effectors among X. citri strains. BMC Genomics 2018;19:16 [CrossRef]
    [Google Scholar]
  5. Álvarez-Álvarez R, Rodríguez-García A, Martínez-Burgo Y, Robles-Reglero V, Santamarta I et al. A 1.8-Mb-reduced Streptomyces clavuligerus genome: relevance for secondary metabolism and differentiation. Appl Microbiol Biotechnol 2014;98:2183–2195 [CrossRef]
    [Google Scholar]
  6. Bansal K, Kumar S, Patil PB. Complete genome sequence reveals evolutionary dynamics of an emerging and variant pathovar of Xanthomonas euvesicatoria. Genome Biol Evol 2018;10:3104-3109 [CrossRef]
    [Google Scholar]
  7. Nakanaga K, Ogura Y, Toyoda A, Yoshida M, Fukano H et al. Naturally occurring a loss of a giant plasmid from Mycobacterium ulcerans subsp. shinshuense makes it non-pathogenic. Sci Rep 2018;8:8218 [CrossRef]
    [Google Scholar]
  8. Li R, Xie M, Dong N, Lin D, Yang X et al. Efficient generation of complete sequences of MDR-encoding plasmids by rapid assembly of MinION barcoding sequencing data. Gigascience 2018;7:gix132 [CrossRef]
    [Google Scholar]
  9. Carpenter SCD, Mishra P, Ghoshal C, Dash PK, Wang L et al. A Strain of an Emerging Indian Xanthomonas oryzae pv. oryzae Pathotype Defeats the Rice Bacterial Blight Resistance Gene xa13 Without Inducing a Clade III SWEET Gene and Is Nearly Identical to a Recent Thai Isolate. Front Microbiol 2018;9:2703 [CrossRef]
    [Google Scholar]
  10. Pieretti I, Royer M, Barbe V, Carrere S, Koebnik R et al. The complete genome sequence of Xanthomonas albilineans provides new insights into the reductive genome evolution of the xylem-limited Xanthomonadaceae. BMC Genomics 2009;10:616 [CrossRef]
    [Google Scholar]
  11. MacLean RC, San Millan A. Microbial evolution: towards resolving the plasmid paradox. Curr Biol 2015;25:R764–R767 [CrossRef]
    [Google Scholar]
  12. Grohmann E, Christie PJ, Waksman G, Backert S. Type IV secretion in gram-negative and Gram-positive bacteria. Mol Microbiol 2018;107:455–471 [CrossRef]
    [Google Scholar]
  13. Souza DP, Oka GU, Alvarez-Martinez CE, Bisson-Filho AW, Dunger G et al. Bacterial killing via a type IV secretion system. Nat Commun 2015;6:6453 [CrossRef]
    [Google Scholar]
  14. Engledow AS, Medrano EG, Mahenthiralingam E, LiPuma JJ, Gonzalez CF et al. Involvement of a plasmid-encoded type IV secretion system in the plant tissue watersoaking phenotype of Burkholderia cenocepacia. J Bacteriol 2004;186:6015–6024 [CrossRef]
    [Google Scholar]
  15. da Silva ACR, Ferro JA, Reinach FC, Farah CS, Furlan LR et al. Comparison of the genomes of two Xanthomonas pathogens with differing host specificities. Nature 2002;417:459–463 [CrossRef]
    [Google Scholar]
  16. Hauben L et al. Comparison of 16S ribosomal DNA sequences of all Xanthomonas species. International Journal of Systematic and Evolutionary Microbiology 1997;47:328–335
    [Google Scholar]
  17. Rademaker JL, Hoste B, Louws FJ, Kersters K, Swings J et al. Comparison of AFLP and rep-PCR genomic fingerprinting with DNA-DNA homology studies: Xanthomonas as a model system. Int J Syst Evol Microbiol 2000;50:665–677 [CrossRef]
    [Google Scholar]
  18. Parkinson N, Cowie C, Heeney J, Stead D. Phylogenetic structure of Xanthomonas determined by comparison of gyrB sequences. Int J Syst Evol Microbiol 2009;59:264–274 [CrossRef]
    [Google Scholar]
  19. Wick RR, Judd LM, Gorrie CL, Holt KE. Unicycler: resolving bacterial genome assemblies from short and long sequencing reads. PLoS Comput Biol 2017;13:e1005595 [CrossRef]
    [Google Scholar]
  20. Walker BJ, Abeel T, Shea T, Priest M, Abouelliel A et al. Pilon: an integrated tool for comprehensive microbial variant detection and genome assembly improvement. PLoS One 2014;9:e112963 [CrossRef]
    [Google Scholar]
  21. Parks DH, Imelfort M, Skennerton CT, Hugenholtz P, Tyson GW et al. CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res 2015;25:1043–1055 [CrossRef]
    [Google Scholar]
  22. Bushnell B. BBMap: a fast, accurate, splice-aware aligner. 2014
  23. Carver T, Thomson N, Bleasby A, Berriman M, Parkhill J et al. DNAPlotter: circular and linear interactive genome visualization. Bioinformatics 2009;25:119–120 [CrossRef]
    [Google Scholar]
  24. Johnson M, Zaretskaya I, Raytselis Y, Merezhuk Y, McGinnis S et al. Ncbi blast: a better web interface. Nucleic Acids Res 2008;36:W5–W9 [CrossRef]
    [Google Scholar]
  25. Varani AM, Siguier P, Gourbeyre E, Charneau V, Chandler M et al. ISsaga is an ensemble of web-based methods for high throughput identification and semi-automatic annotation of insertion sequences in prokaryotic genomes. Genome Biol 2011;12:R30 [CrossRef]
    [Google Scholar]
  26. Grau J, Reschke M, Erkes A, Streubel J, Morgan RD et al. AnnoTALE: bioinformatics tools for identification, annotation, and nomenclature of tales from Xanthomonas genomic sequences. Sci Rep 2016;6:21077 [CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/acmi/10.1099/acmi.0.000063
Loading
/content/journal/acmi/10.1099/acmi.0.000063
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error