1887

Abstract

We describe two new species of the genus Xanthomonas , represented by yellow mucoid bacterial strains isolated from diseased leaves of watercress (Nasturtium officinale) produced in Florida, USA. One strain was pathogenic on watercress, but not in other species including a range of brassicas; other strains were not pathogenic in any of the tested plants. Data from Biolog carbon source utilization tests and nucleotide sequence data from 16S and gyrB loci suggested that both pathogenic and non-pathogenic strains were related to, yet distinct from, previously described Xanthomonas species. Multilocus sequence analysis and whole genome-wide comparisons of the average nucleotide identity (ANI) of genomes of two strains from watercress showed that these are distinct and share less than 95 % ANI with all other known species; the non-pathogenic strain WHRI 8848 is close to Xanthomonas cassavae (ANI of 93.72 %) whilst the pathogenic strain WHRI 8853 is close to a large clade of species that includes Xanthomonas vesicatoria (ANI ≤90.25 %). Based on these results, we propose that both strains represent new Xanthomonas species named Xanthomonas floridensis sp. nov. (type strain WHRI 8848=ATCC TSD-60=ICMP 21312=LMG 29665=NCPPB 4601) and Xanthomonas nasturtii sp. nov. (type strain WHRI 8853=ATCC TSD-61=ICMP 21313=LMG 29666=NCPPB 4600), respectively. The presence of non-pathogenic Xanthomonas strains in watercress and their interaction with pathogenic strains needs to be further investigated. Although the importance of the new pathogenic species is yet to be determined, the bacterial disease that it causes constitutes a threat to watercress production and its distribution should be monitored.

Loading

Article metrics loading...

/content/journal/ijsem/10.1099/ijsem.0.002189
2017-08-25
2019-10-23
Loading full text...

Full text loading...

/deliver/fulltext/ijsem/67/9/3645.html?itemId=/content/journal/ijsem/10.1099/ijsem.0.002189&mimeType=html&fmt=ahah

References

  1. Bull CT, de Boer SH, Denny TP, Firrao G, Saux MF-L et al. List of new names of plant pathogenic bacteria (2008–2010). J Plant Pathol 2012;94:21–27
    [Google Scholar]
  2. Bull C, de Boer S, Denny T, Firrao G, Fischer-Le Saux M et al. Comprehensive list of names of plant pathogenic bacteria, 1980-2007. J Plant Pathol 2010;92:551–592
    [Google Scholar]
  3. Constantin EC, Cleenwerck I, Maes M, Baeyen S, van Malderghem C et al. Genetic characterization of strains named as Xanthomonas axonopodis pv. dieffenbachiae leads to a taxonomic revision of the X. axonopodis species complex. Plant Pathol 2016;65:792–806 [CrossRef]
    [Google Scholar]
  4. Jacques MA, Arlat M, Boulanger A, Boureau T, Carrere S et al. Using ecology, physiology, and genomics to understand host specificity in Xanthomonas. Ann Rev Phytopathol 2016;54:163–187[CrossRef]
    [Google Scholar]
  5. 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][PubMed]
    [Google Scholar]
  6. Vauterin L, Rademaker J, Swings J. Synopsis on the taxonomy of the genus Xanthomonas. Phytopathology 2000;90:677–682 [CrossRef][PubMed]
    [Google Scholar]
  7. Vauterin L, Hoste B, Kersters K, Swings J. Reclassification of Xanthomonas. Int J Syst Bacteriol 1995;45:472–489 [CrossRef]
    [Google Scholar]
  8. Vicente JG, Everett B, Roberts SJ. Identification of isolates that cause a leaf spot disease of brassicas as Xanthomonas campestris pv. raphani and pathogenic and genetic comparison with related pathovars. Phytopathology 2006;96:735–745 [CrossRef][PubMed]
    [Google Scholar]
  9. Vicente JG, Holub EB. Xanthomonas campestris pv. campestris (cause of black rot of crucifers) in the genomic era is still a worldwide threat to brassica crops. Mol Plant Pathol 2013;14:2–18 [CrossRef][PubMed]
    [Google Scholar]
  10. Hauben L, Vauterin L, Swings J, Moore ER. Comparison of 16S ribosomal DNA sequences of all Xanthomonas species. Int J Syst Bacteriol 1997;47:328–335 [CrossRef][PubMed]
    [Google Scholar]
  11. Parkinson N, Aritua V, Heeney J, Cowie C, Bew J et al. Phylogenetic analysis of Xanthomonas species by comparison of partial gyrase B gene sequences. Int J Syst Evol Microbiol 2007;57:2881–2887 [CrossRef][PubMed]
    [Google Scholar]
  12. Almeida NF, Yan S, Cai R, Clarke CR, Morris CE et al. PAMDB, a multilocus sequence typing and analysis database and website for plant-associated microbes. Phytopathology 2010;100:208–215 [CrossRef][PubMed]
    [Google Scholar]
  13. Young JM, Park DC, Shearman HM, Fargier E. A multilocus sequence analysis of the genus Xanthomonas. Syst Appl Microbiol 2008;31:366–377 [CrossRef][PubMed]
    [Google Scholar]
  14. Denancé N, Lahaye T, Noël LD. Editorial: genomics and effectomics of the crop killer Xanthomonas. Front Plant Sci 2016;7:1–2 [CrossRef][PubMed]
    [Google Scholar]
  15. Ryan RP, Vorhölter FJ, Potnis N, Jones JB, van Sluys MA et al. Pathogenomics of Xanthomonas: understanding bacterium-plant interactions. Nat Rev Microbiol 2011;9:344–355 [CrossRef][PubMed]
    [Google Scholar]
  16. Aritua V, Musoni A, Kabeja A, Butare L, Mukamuhirwa F et al. The draft genome sequence of Xanthomonas species strain Nyagatare, isolated from diseased bean in Rwanda. FEMS Microbiol Lett 2015;362:1–4 [CrossRef][PubMed]
    [Google Scholar]
  17. Jacobs JM, Pesce C, Lefeuvre P, Koebnik R. Comparative genomics of a cannabis pathogen reveals insight into the evolution of pathogenicity in Xanthomonas. Front Plant Sci 2015;6:1–13 [CrossRef][PubMed]
    [Google Scholar]
  18. Pieretti I, Cociancich S, Bolot S, Carrère S, Morisset A et al. Full genome sequence analysis of two isolates reveals a novel Xanthomonas species close to the sugarcane pathogen Xanthomonas albilineans. Genes 2015;6:714–733 [CrossRef][PubMed]
    [Google Scholar]
  19. Triplett LR, Verdier V, Campillo T, van Malderghem C, Cleenwerck I et al. Characterization of a novel clade of Xanthomonas isolated from rice leaves in Mali and proposal of Xanthomonas maliensis sp. nov. Antonie van Leeuwenhoek 2015;107:869–881 [CrossRef][PubMed]
    [Google Scholar]
  20. Fogarty MC, Hughes CM, Burke G, Brown JC, Davison GW. Acute and chronic watercress supplementation attenuates exercise-induced peripheral mononuclear cell DNA damage and lipid peroxidation. Br J Nutr 2013;109:293–301 [CrossRef][PubMed]
    [Google Scholar]
  21. Payne C, Clarkson GJJ, Rothwell S, Taylor G. Diversity in global gene expression and morphology across a watercress (Nasturtium officinale R. Br.) germplasm collection: first steps to breeding. Hortic Res 2005;2:15029[CrossRef]
    [Google Scholar]
  22. CABI Datasheet Report for Nasturtium Officinale Watercress In: CABI, ed; 2017;www.cabi.org/isc/datasheet/35646
    [Google Scholar]
  23. Mchugh JJ, Fukuda SK, Takeda KY. 1987; Hawaii watercress production. Research Extension Series 088 p. 8www.ctahr.hawaii.edu/oc/freepubs/pdf/RES-088.pdf
  24. Strandberg JO, Tucker CA. Diseases of watercress in Florida. Fla Agric Exp Stn J Ser 1968;3105:194–196
    [Google Scholar]
  25. Walsh JA, Phelps K. Development and evaluation of a technique for screening watercress (Rorippa nasturtium-aquaticum) for resistance to watercress yellow spot virus and crook-root fungus (Spongospora subterranea f. sp. nasturtii). Plant Pathol 1991;40:212–220 [CrossRef]
    [Google Scholar]
  26. Mchugh JJ, Constantinides JN. 2004; Pest management strategic plan for watercress production in Hawaii. p.45 Workshop Summarywww.ipmcenters.org/pmsp/pdf/HIwatercress.pdf
  27. King EO, Ward MK, Raney DE. Two simple media for the demonstration of pyocyanin and fluorescin. J Lab Clin Med 1954;44:301–307[PubMed]
    [Google Scholar]
  28. Stolp H, Starr MP. Bacteriophage reactions and speciation of phytopathogenic xanthomonads. J Phytopathol 1964;51:442–478 [CrossRef]
    [Google Scholar]
  29. Feltham RK, Power AK, Pell PA, Sneath PA. A simple method for storage of bacteria at–76 degrees C. J Appl Bacteriol 1978;44:313–316 [CrossRef][PubMed]
    [Google Scholar]
  30. Vicente JG, Conway J, Roberts SJ, Taylor JD. Identification and origin of Xanthomonas campestris pv. campestris races and related pathovars. Phytopathology 2001;91:492–499 [CrossRef][PubMed]
    [Google Scholar]
  31. Jiang H, Dong H, Zhang G, Yu B, Chapman LR et al. Microbial diversity in water and sediment of Lake Chaka, an athalassohaline lake in northwestern China. Appl Environ Microbiol 2006;72:3832–3845 [CrossRef][PubMed]
    [Google Scholar]
  32. Andrews S. 2016; FastQC: a quality control tool for high throughput sequence data. www.bioinformatics.babraham.ac.uk/projects/fastqc/
  33. Krueger F. 2016; A wrapper tool around Cutadapt and FastQC to consistently apply quality and adapter trimming to FastQ files, with some extra functionality for MspI-digested RRBS-type (Reduced Representation Bisufite-Seq) libraries. www.bioinformatics.babraham.ac.uk/projects/trim_galore/
  34. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 2012;19:455–477 [CrossRef][PubMed]
    [Google Scholar]
  35. Boetzer M, Henkel CV, Jansen HJ, Butler D, Pirovano W. Scaffolding pre-assembled contigs using SSPACE. Bioinformatics 2011;27:578–579 [CrossRef][PubMed]
    [Google Scholar]
  36. Gurevich A, Saveliev V, Vyahhi N, Tesler G. QUAST: quality assessment tool for genome assemblies. Bioinformatics 2013;29:1072–1075 [CrossRef][PubMed]
    [Google Scholar]
  37. Delcher AL, Phillippy A, Carlton J, Salzberg SL. Fast algorithms for large-scale genome alignment and comparison. Nucleic Acids Res 2002;30:2478–2483 [CrossRef][PubMed]
    [Google Scholar]
  38. Richter M, Rosselló-Móra R. Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci USA 2009;106:19126–19131 [CrossRef][PubMed]
    [Google Scholar]
  39. Martínez-García PM, Ramos C, Rodríguez-Palenzuela P. T346Hunter: a novel web-based tool for the prediction of type III, type IV and type VI secretion systems in bacterial genomes. PLoS One 2015;10:e0119317 [CrossRef][PubMed]
    [Google Scholar]
  40. Cesbron S, Briand M, Essakhi S, Gironde S, Boureau T et al. Comparative genomics of pathogenic and nonpathogenic strains of Xanthomonas arboricola unveil molecular and evolutionary events linked to pathoadaptation. Front Plant Sci 2015;6:1126 [CrossRef][PubMed]
    [Google Scholar]
  41. Essakhi S, Cesbrona S, Fischer-Le Saux M, Bonneau S, Jacques MA et al. Phylogenetic and VNTR analysis identified non-pathogenic lineages within Xanthomonas arboricola lacking the canonical type three secretion system. Appl Environ Microbiol 2015;81:5395–5410[CrossRef]
    [Google Scholar]
  42. de Campos SB, Youn JW, Farina R, Jaenicke S, Jünemann S et al. Changes in root bacterial communities associated to two different development stages of canola (Brassica napus L. var oleifera) evaluated through next-generation sequencing technology. Microb Ecol 2013;65:593–601 [CrossRef][PubMed]
    [Google Scholar]
  43. Takahashi H, Sekiguchi H, Ito T, Sasahara M, Hatanaka N et al. Microbial community profiles in intercellular fluid of rice. J Gen Plant Pathol 2011;77:121–131 [CrossRef]
    [Google Scholar]
  44. Vorholt JA. Microbial life in the phyllosphere. Nat Rev Microbiol 2012;10:828–840 [CrossRef][PubMed]
    [Google Scholar]
  45. Adriko J, Aritua V, Mortensen CN, Tushemereirwe WK, Mulondo AL et al. Biochemical and molecular tools reveal two diverse Xanthomonas groups in bananas. Microbiol Res 2016;183:109–116 [CrossRef][PubMed]
    [Google Scholar]
  46. Sheridan GEC, Claxton JR, Clarkson JM, Blakesley D. Genetic diversity within commercial populations of watercress (Rorippa nasturtium-aquaticum), and between allied Brassicaceae inferred from RAPD-PCR. Euphytica 2001;122:319–325 [CrossRef]
    [Google Scholar]
  47. Ramkumar G, Lee SW, Weon H-Y, Kim B-Y, Lee YH. First report on the whole genome sequence of Pseudomonas cichorii strain JBC1 and comparison with other Pseudomonas species. Plant Pathol 2015;64:63–70 [CrossRef]
    [Google Scholar]
  48. Kwon SW, Kim JS, Park IC, Yoon SH, Park DH et al. Pseudomonas koreensis sp. nov., Pseudomonas umsongensis sp. nov. and Pseudomonas jinjuensis sp. nov., novel species from farm soils in Korea. Int J Syst Evol Microbiol 2003;53:21–27 [CrossRef][PubMed]
    [Google Scholar]
  49. Paulsen IT, Press CM, Ravel J, Kobayashi DY, Myers GS et al. Complete genome sequence of the plant commensal Pseudomonas fluorescens Pf-5. Nat Biotechnol 2005;23:873–878 [CrossRef][PubMed]
    [Google Scholar]
  50. Opio AF, Allen DJ, Teri JM. Pathogenic variation in Xanthomonas campestris pv. phaseoli, the causal agent of common bacterial blight in Phaseolus beans. Plant Pathol 1996;45:1126–1133 [CrossRef]
    [Google Scholar]
  51. Trébaol G, Gardan L, Manceau C, Tanguy JL, Tirilly Y et al. Genomic and phenotypic characterization of Xanthomonas cynarae sp. nov., a new species that causes bacterial bract spot of artichoke (Cynara scolymus L.). Int J Syst Evol Microbiol 2000;50:1471–1478 [CrossRef][PubMed]
    [Google Scholar]
  52. Hamza AA, Robene-Soustrade I, Jouen E, Lefeuvre P, Chiroleu F et al. MultiLocus sequence analysis- and amplified fragment length polymorphism-based characterization of xanthomonads associated with bacterial spot of tomato and pepper and their relatedness to Xanthomonas species. Syst Appl Microbiol 2012;35:183–190 [CrossRef][PubMed]
    [Google Scholar]
  53. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol 2013;30:2725–2729 [CrossRef][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/ijsem/10.1099/ijsem.0.002189
Loading
/content/journal/ijsem/10.1099/ijsem.0.002189
Loading

Data & Media loading...

Supplements

Supplementary File 1

PDF

Most Cited This Month

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