Advertisement

Current Microbiology

, Volume 76, Issue 5, pp 566–574 | Cite as

Draft Genome of Burkholderia cenocepacia TAtl-371, a Strain from the Burkholderia cepacia Complex Retains Antagonism in Different Carbon and Nitrogen Sources

  • Fernando Uriel Rojas-Rojas
  • David Sánchez-López
  • Erika Yanet Tapia-García
  • Ivan Arroyo-Herrera
  • Maskit Maymon
  • Ethan Humm
  • Marcel Huntemann
  • Alicia Clum
  • Manoj Pillay
  • Krishnaveni Palaniappan
  • Neha Varghese
  • Natalia Mikhailova
  • Dimitrios Stamatis
  • T. B. K. Reddy
  • Natalia Ivanova
  • Nikos Kyrpides
  • Tanja Woyke
  • Nicole Shapiro
  • Ann M. Hirsch
  • J. Antonio Ibarra
  • Paulina Estrada-de los SantosEmail author
Article

Abstract

Burkholderia cenocepacia TAtl-371 was isolated from the rhizosphere of a tomato plant growing in Atlatlahucan, Morelos, Mexico. This strain exhibited a broad antimicrobial spectrum against bacteria, yeast, and fungi. Here, we report and describe the improved, high-quality permanent draft genome of B. cenocepacia TAtl-371, which was sequenced using a combination of PacBio RS and PacBio RS II sequencing methods. The 7,496,106 bp genome of the TAtl-371 strain is arranged in three scaffolds, contains 6722 protein-coding genes, and 99 RNA only-encoding genes. Genome analysis revealed genes related to biosynthesis of antimicrobials such as non-ribosomal peptides, siderophores, chitinases, and bacteriocins. Moreover, analysis of bacterial growth on different carbon and nitrogen sources shows that the strain retains its antimicrobial ability.

Notes

Acknowledgements

FURR, EYTG, and IAH recipients of a fellowship from CONACYT. JAIG and PES are recipient of SNI, EDI, and COFAA fellowships. We thank Dr. E.O. Lopez-Villegas (Escuela Nacional de Ciencias Biológicas, IPN) for the transmission electron microscopic analysis. The genome sequence was conducted by the U.S. Department of Energy, Joint Genome Institute, a DOE Office of Science User Facility, is supported by the Office of Sciences of the U.S. Department of Energy under the proposal 1572 and Contract No. DE-AC02-05CH11231. Phenotypic analysis was partially funded by Projects SIP 20170492 and SIP 20180117.

Compliance with Ethical Standards

Conflict of interest

The authors have declared no conflict of interest.

Supplementary material

284_2019_1657_MOESM1_ESM.docx (18 kb)
Supplementary material 1 (DOCX 18 KB)

References

  1. 1.
    Estrada-de los Santos P, Rojas-Rojas FU, Tapia-García EY, Vásquez-Murrieta MS, Hirsch AM (2016) To split or not to split: an opinion on dividing the genus Burkholderia. Ann Microbiol 66:1303–1314CrossRefGoogle Scholar
  2. 2.
    Estrada-de los Santos P, Vinuesa P, Martínez-Aguilar L, Hirsch AM, Caballero-Mellado J (2013) Phylogenetic analysis of Burkholderia species by multilocus sequence analysis. Curr Microbiol 67:51–60CrossRefGoogle Scholar
  3. 3.
    Sawana A, Adeolu M, Gupta RS (2014) Molecular signatures and phylogenomic 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 environmental species. Front Genet 5:429CrossRefGoogle Scholar
  4. 4.
    Dobritsa AP, Samadpour M (2016) Transfer of eleven Burkholderia species to the genus Paraburkholderia and proposal of Caballeronia gen. nov., a new genus to accommodate twelve species of Burkholderia and Paraburkholderia. Int J Syst Evol Microbiol 66:2836–2846CrossRefGoogle Scholar
  5. 5.
    Lopes-Santos L, Castro DBA, Ferreira-Tonin M, Corrêa DBA, Weir BS, Park D, Ottoboni LMM, Neto JR, Destéfano SAL (2017) Reassessment of the taxonomic position of Burkholderia andropogonis and description of Robbsia andropogonis gen. nov., comb. nov. Anton Leeuw Int J G 110:727–736CrossRefGoogle Scholar
  6. 6.
    Estrada-de los Santos P, Palmer M, Chávez-Ramírez B, Beukes C, Steenkamp ET, Briscoe L, Khan N, Maluk M, Lafos M, Humm E, Arrabit M, Crook M, Gross E, Simon MF, dos Reis Jr FB, Whitman WB, Shapiro N, Poole PS, Hirsch AM, Venter SN, James EK (2018) Whole gnome analysies suggests that Burkholderia sensu lato contains two additional novel genera (Mycetohabitnas gen. nov., and Trinickia gen. nov.): implications for the evolution of diazotrophy and nodulation in the Burkholderiaceae. Genes 9:389CrossRefGoogle Scholar
  7. 7.
    Martina P, Leguizamon M, Prieto CI, Sousa SA, Montanaro P, Draghi WO, Stämmler M, Bettiol M, de Carvalho CCCR, Palau J (2017) Burkholderia puraquae sp. nov., a novel species of the Burkholderia cepacia complex isolated from hospital settings and agricultural soils. Int J Syst Evol Microbiol 68:14–20CrossRefGoogle Scholar
  8. 8.
    Coenye T, Vandamme P, Govan JRW, LiPuma JJ (2001) Taxonomy and identification of the Burkholderia cepacia complex. J Clin Microbiol 39:3427–3436CrossRefGoogle Scholar
  9. 9.
    Compant S, Nowak J, Coenye T, Clement C, Ait Barka E (2008) Diversity and occurrence of Burkholderia spp. in the natural environment. FEMS Microbiol Rev 32:607–626CrossRefGoogle Scholar
  10. 10.
    Depoorter E, Bull MJ, Peeters C, Coenye T, Vandamme P, Mahenthiralingam E (2016) Burkholderia: an update on taxonomy and biotechnological potential as antibiotic producers. Appl Microbiol Biotechnol 100:5215–5229CrossRefGoogle Scholar
  11. 11.
    Caballero-Mellado J, Onofre-Lemus J, Estrada-de los Santos P, Martínez-Aguilar L (2007) The tomato rhizosphere, an environment rich in nitrogen-fixing Burkholderia species with capabilities of interest for agriculture and bioremediation. Appl Environ Microbiol 73:5308–5319CrossRefGoogle Scholar
  12. 12.
    Rojas-Rojas FU, Salazar-Gomez A, Vargas-Díaz ME, Vásquez-Murrieta MS, Hirsch AM, De Mot R, Ghequire MGK, Ibarra JA, Estrada-de los Santos P (2018) Broad-spectrum antimicrobial activity by Burkholderia cenocepacia TAtl-371, a strain isoalted from the tomato rhizosphere. Microbiology 164:1072–1086CrossRefGoogle Scholar
  13. 13.
    Guindon S (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assesing the performance of PhyML 3.0. Syst Biol 59:221–224CrossRefGoogle Scholar
  14. 14.
    Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2016) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729CrossRefGoogle Scholar
  15. 15.
    Eid J, Fehr A, Gray J, Luong K, Lyle J, Otto G, Peluso P, Rank D, Baybayan P, Bettman B et al (2009) Real-time DNA sequencing from single polymerase molecules. Science 323:133–138CrossRefGoogle Scholar
  16. 16.
    Rojas-Rojas FU, Tapia-García EY, Maymon M, Humm E, Huntemann M, Clum A, Pillay M, Pananiappan K, Varghese N, Mikhailova N, Stamatis D, Reddy TBK, Markowitz V, Ivanova N, Kyrpides N, Woyke T, Shapiro N, Hirsch AM, Estrada-de los Santos P (2017) Draft genome of Paraburkholderia caballeronis TNe-841T, a free-living, nitrogen-fixing, tomato plant-associated bacterium. Stand Genom Sci 12:80CrossRefGoogle Scholar
  17. 17.
    Darling AE, Mau B, Perna NT (2010) progressiveMauve: multiple genome alignment with gene gain, loss and rearrangement. PLoS ONE 25:e11147CrossRefGoogle Scholar
  18. 18.
    Esmaeel Q, Pupin M, Kieu NP, Chataigne G, Bechet M, Deravel J, Krier F, Hofte M, Jacques P, Leclere V (2016) Burkholderia genome mining for nonribosomal peptide synthetases reveals a great potential for novel siderophores and lipopeptides synthesis. Microbiologyopen 5:512–526CrossRefGoogle Scholar
  19. 19.
    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 Int 25:29794–29807CrossRefGoogle Scholar
  20. 20.
    Deng P, Foxfire A, Xu J, Baird SM, Jia J, Delgado KH, Shin R, Smith L, Lu S-E (2017) The siderophore product ornibactin is required for the bactericidal activity of Burkholderia contaminans MS14. Appl Environ Microbiol 83:e00051–e00017CrossRefGoogle Scholar
  21. 21.
    Snyder AB, Worobo RW (2014) Chemical and genetic characterization of bacteriocins: antimicrobial peptides for food safety. J Sci Food Agric 94:28–44CrossRefGoogle Scholar
  22. 22.
    Ghequire MG, De Canck E, Wattiau P, Van Winge I, Loris R, Coenye T, De Mot R (2013) Antibacterial activity of a lectin-like Burkholderia cenocepacia protein. Microbiologyopen 2:566–575CrossRefGoogle Scholar
  23. 23.
    Yao GW, Duarte I, Le TT, Carmody L, LiPuma JJ, Young R, Gonzalez CF (2017) A broad-host-range tailocin from Burkholderia cenocepacia. Appl Environ Microbiol 83:e03414–e03416Google Scholar
  24. 24.
    Bhattacharya D, Nagpure A, Gupta RK (2007) Bacterial chitinases: properties and potential. Crit Rev Biotechnol 27:21–28CrossRefGoogle Scholar
  25. 25.
    Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410CrossRefGoogle Scholar
  26. 26.
    Richter M, Rosselló-Móra R (2009) Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci USA 106:19126–19131CrossRefGoogle Scholar
  27. 27.
    LiPuma JJ, Spilker T, Coenye T, Gonzalez CF (2002) An epidemic Burkholderia cepacia complex strain identified in soil. Lancet 359:2002–2003CrossRefGoogle Scholar
  28. 28.
    Coenye T, Spilker T, Van Schoor A, LiPuma J, Vandamme P (2004) Recovery of Burkholderia cenocepacia strain PHDC from cystic fibrosis patients in Europe. Thorax 59:952–954CrossRefGoogle Scholar
  29. 29.
    Baldwin A, Mahenthiralingam E, Drevinek P, Vandamme P, Govan JR, Waine DJ, LiPuma JJ, Chiarini L, Dalmastri C, Henry DA (2007) Environmental Burkholderia cepacia complex isolates from human infections. Emerg Infect Dis 13:458–461CrossRefGoogle Scholar
  30. 30.
    Coenye T, LiPuma JJ (2003) Population structure analysis of Burkholderia cepacia genomovar III: varying degrees of genetic recombination characterize major clonal complexes. Microbiology 149:77–88CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • Fernando Uriel Rojas-Rojas
    • 1
  • David Sánchez-López
    • 1
  • Erika Yanet Tapia-García
    • 1
  • Ivan Arroyo-Herrera
    • 1
  • Maskit Maymon
    • 2
  • Ethan Humm
    • 2
  • Marcel Huntemann
    • 3
  • Alicia Clum
    • 3
  • Manoj Pillay
    • 3
  • Krishnaveni Palaniappan
    • 3
  • Neha Varghese
    • 3
  • Natalia Mikhailova
    • 3
  • Dimitrios Stamatis
    • 3
  • T. B. K. Reddy
    • 3
  • Natalia Ivanova
    • 3
  • Nikos Kyrpides
    • 3
  • Tanja Woyke
    • 3
  • Nicole Shapiro
    • 3
  • Ann M. Hirsch
    • 2
    • 4
  • J. Antonio Ibarra
    • 1
  • Paulina Estrada-de los Santos
    • 1
    Email author
  1. 1.Instituto Politécnico NacionalEscuela Nacional de Ciencias BiológicasCiudad de MéxicoMexico
  2. 2.Department of Molecular, Cell and Developmental BiologyUniversity of California-Los AngelesLos AngelesUSA
  3. 3.DOE Joint Genome InstituteWalnut CreekUSA
  4. 4.Molecular Biology InstituteUniversity of California-Los AngelesLos AngelesUSA

Personalised recommendations