Skip to main content
Log in

Complete Genome Sequence of Cellulomonas sp. JZ18, a Root Endophytic Bacterium Isolated from the Perennial Desert Tussock-Grass Panicum turgidum

  • Short Communication
  • Published:
Current Microbiology Aims and scope Submit manuscript

Abstract

Cellulomonas sp. JZ18 is a gram-positive, rod shaped bacterium that was previously isolated from the root endosphere of the perennial desert tussock-grass Panicum turgidum. Genome coverage of PacBio sequencing was approximately 199X. Genome assembly generated a single chromosome of 7,421,843 base pairs with a guanine-cytosine (GC) content of 75.60% with 3240 protein coding sequences, 361 pseudo genes, three ribosomal RNA operons, three non-coding RNAs and 45 transfer RNAs. Comparison of JZ18′s genome with type strains from the same genus, using digital DNA–DNA hybridization and average nucleotide identity calculations, revealed that JZ18 might potentially belong to a new species. Functional analysis revealed the presence of genes that may complement previously observed biochemical and plant phenotypes. Furthermore, the presence of a number of enzymes could be of potential use in industrial processes as biocatalysts. Genome sequencing and analysis, coupled with comparative genomics, of endophytic bacteria for their potential plant growth promoting activities under different soil conditions will accelerate the knowledge and applications of biostimulants in sustainable agriculture.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

References

  1. Glazer AN, Nikaido H (2007) Microbial biotechnology: fundamentals of applied microbiology, 2nd edn. Cambridge University Press, Cambridge

    Book  Google Scholar 

  2. Chaudhary P, Kumar NN, Deobagkar DN (1997) The glucanases of Cellulomonas. Biotechnol Adv 15(2):315–331. https://doi.org/10.1016/S0734-9750(97)00010-4

    Article  CAS  PubMed  Google Scholar 

  3. Rapp P, Wagner F (1986) Production and properties of xylan-degrading enzymes from Cellulomonas uda. Appl Environ Microbiol 51(4):746

    Article  CAS  Google Scholar 

  4. Clarke JH, Laurie JI, Gilbert HJ, Hazlewood GP (1991) Multiple xylanases of Cellulomonas fimi are encoded by distinct genes. FEMS Microbiol Lett 83(3):305–309. https://doi.org/10.1111/j.1574-6968.1991.tb04481.x

    Article  CAS  Google Scholar 

  5. Cazemier AE, Verdoes JC, van Ooyen AJJ, Op den Camp HJM (1999) Molecular and biochemical characterization of two xylanase-encoding genes from Cellulomonas pachnodae. Appl Environ Microbiol 65(9):4099

    Article  CAS  Google Scholar 

  6. Rajoka MI, Malik KA (1984) Cellulase and hemicellulase production by Cellulomonas flavigena NIAB 441. Biotechnol Lett 6(9):597–600. https://doi.org/10.1007/BF00135689

    Article  CAS  Google Scholar 

  7. Sami AJ, Akhtar MW (1993) Purification and characterization of two low-molecular weight endoglucanases of Cellulomonas flavigena. Enzyme Microb Technol 15(7):586–592. https://doi.org/10.1016/0141-0229(93)90021-S

    Article  CAS  Google Scholar 

  8. Santiago-Hernández A, Vega-Estrada J, del Carmen M-H, Hidalgo-Lara ME (2007) Purification and characterization of two sugarcane bagasse-absorbable thermophilic xylanases from the mesophilic Cellulomonas flavigena. J Ind Microbiol Biotechnol 34(4):331–338. https://doi.org/10.1007/s10295-006-0202-4

    Article  CAS  PubMed  Google Scholar 

  9. Pérez-Avalos O, Sánchez-Herrera LM, Salgado LM, Ponce-Noyola T (2008) A bifunctional endoglucanase/endoxylanase from Cellulomonas flavigena with potential use in industrial processes at different pH. Curr Microbiol 57(1):39–44. https://doi.org/10.1007/s00284-008-9149-1

    Article  CAS  PubMed  Google Scholar 

  10. Lisov AV, Belova OV, Lisova ZA, Vinokurova NG, Nagel AS, Andreeva-Kovalevskaya ZI, Budarina ZI, Nagornykh MO, Zakharova MV, Shadrin AM, Solonin AS, Leontievsky AA (2017) Xylanases of Cellulomonas flavigena: expression, biochemical characterization, and biotechnological potential. AMB Express 7(1):5. https://doi.org/10.1186/s13568-016-0308-7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Marquez-Santacruz HA, Hernandez-Leon R, Orozco-Mosqueda MC, Velazquez-Sepulveda I, Santoyo G (2010) Diversity of bacterial endophytes in roots of Mexican husk tomato plants (Physalis ixocarpa) and their detection in the rhizosphere. Genet Mol Res 9(4):2372–2380. https://doi.org/10.4238/vol9-4gmr921

    Article  CAS  PubMed  Google Scholar 

  12. Zinniel DK, Lambrecht P, Harris NB, Feng Z, Kuczmarski D, Higley P, Ishimaru CA, Arunakumari A, Barletta RG, Vidaver AK (2002) Isolation and characterization of endophytic colonizing bacteria from agronomic crops and prairie plants. Appl Environ Microbiol 68(5):2198. https://doi.org/10.1128/AEM.68.5.2198-2208.2002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Egamberdieva D (2008) Plant growth promoting properties of rhizobacteria isolated from wheat and pea grown in loamy sand soil. Turk J Biol 32(1):9–15

    Google Scholar 

  14. Egamberdiyeva D, Höflich G (2002) Root colonization and growth promotion of winter wheat and pea by Cellulomonas spp. at different temperatures. Plant Growth Regul 38(3):219–224. https://doi.org/10.1023/A:1021538226573

    Article  CAS  Google Scholar 

  15. Duy MV, Hoi NT, Ve NB, Thuc LV, Trang NQ (2016) Recent trends in PGPR research for sustainable crop productivity. In: Sayyed RZ, Reddy MS, Al-Turki AI (eds) 4th Asian PGPR conference proceedings, Hanoi, Vietnam, 3-6 May, 2015.

  16. Takegawa K, Yamaguchi S, Miki S, Jikibara T, Iwahara S (1991) Purification and characterization of a novel lyase from Cellulomonas sp. that degrades Fusarium and Gibberella acidic polysaccharides. Agric Biol Chem 55(8):1969–1975. https://doi.org/10.1080/00021369.1991.10870925

    Article  CAS  PubMed  Google Scholar 

  17. Eida AA, Ziegler M, Lafi FF, Michell CT, Voolstra CR, Hirt H, Saad MM (2018) Desert plant bacteria reveal host influence and beneficial plant growth properties. PLoS ONE 13(12):e0208223. https://doi.org/10.1371/journal.pone.0208223

    Article  PubMed  PubMed Central  Google Scholar 

  18. Haft DH, DiCuccio M, Badretdin A, Brover V, Chetvernin V, O’Neill K, Li W, Chitsaz F, Derbyshire MK, Gonzales NR, Gwadz M, Lu F, Marchler GH, Song JS, Thanki N, Yamashita RA, Zheng C, Thibaud-Nissen F, Geer LY, Marchler-Bauer A, Pruitt KD (2017) RefSeq: an update on prokaryotic genome annotation and curation. Nucleic Acids Res 46(D1):D851–D860. https://doi.org/10.1093/nar/gkx1068

    Article  CAS  PubMed Central  Google Scholar 

  19. Tatusova T, DiCuccio M, Badretdin A, Chetvernin V, Nawrocki EP, Zaslavsky L, Lomsadze A, Pruitt KD, Borodovsky M, Ostell J (2016) NCBI prokaryotic genome annotation pipeline. Nucleic Acids Res 44(14):6614–6624. https://doi.org/10.1093/nar/gkw569

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Kanehisa M, Sato Y, Kawashima M, Furumichi M, Tanabe M (2016) KEGG as a reference resource for gene and protein annotation. Nucleic Acids Res 44(D1):D457–D462. https://doi.org/10.1093/nar/gkv1070

    Article  CAS  PubMed  Google Scholar 

  21. 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(W1):W237–W243. https://doi.org/10.1093/nar/gkv437

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25(17):3389–3402. https://doi.org/10.1093/nar/25.17.3389

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Eida AA, Alzubaidy HS, de Zélicourt A, Synek L, Alsharif W, Lafi FF, Hirt H, Saad MM (2019) Phylogenetically diverse endophytic bacteria from desert plants induce transcriptional changes of tissue-specific ion transporters and salinity stress in Arabidopsis thaliana. Plant Sci 280:228–240. https://doi.org/10.1016/j.plantsci.2018.12.002

    Article  CAS  PubMed  Google Scholar 

  24. Richter M, Rosselló-Móra R, Oliver Glöckner F, Peplies J (2015) JSpeciesWS: a web server for prokaryotic species circumscription based on pairwise genome comparison. Bioinformatics 32(6):929–931. https://doi.org/10.1093/bioinformatics/btv681

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Meier-Kolthoff JP, Göker M (2019) TYGS is an automated high-throughput platform for state-of-the-art genome-based taxonomy. Nat Commun 10(1):2182. https://doi.org/10.1038/s41467-019-10210-3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Meier-Kolthoff JP, Auch AF, Klenk H-P, Göker M (2013) Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinform 14(1):60. https://doi.org/10.1186/1471-2105-14-60

    Article  Google Scholar 

  27. Shi Y-L, Sun Y, Ruan Z-Y, Su J, Yu L-Y, Zhang Y-Q (2020) Cellulomonastelluris sp. nov., an endoglucanase-producing actinobacterium isolated from Badain Jaran desert sand. Int J Syst Evol Microbiol 70(1):631–635. https://doi.org/10.1099/ijsem.0.003806

    Article  CAS  PubMed  Google Scholar 

  28. Tian Z, Lu S, Jin D, Yang J, Pu J, Lai X-H, Ren Z-h, Wu X-M, Li J, Wang S, Xu J (2020) Cellulomonas shaoxiangyii sp. nov., isolated from faeces of Tibetan antelope (Pantholops hodgsonii) on the Qinghai–Tibet Plateau. Int J Syst Evol Microbiol 70(4):2204–2210. https://doi.org/10.1099/ijsem.0.003939

    Article  CAS  PubMed  Google Scholar 

  29. Baerson SR, Schröder J, Cook D, Rimando AM, Pan Z, Dayan FE, Noonan BP, Duke SO (2010) Alkylresorcinol biosynthesis in plants. Plant Signal Behav 5(10):1286–1289. https://doi.org/10.4161/psb.5.10.13062

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Stasiuk M, Kozubek A (2010) Biological activity of phenolic lipids. Cell Mol Life Sci 67(6):841–860. https://doi.org/10.1007/s00018-009-0193-1

    Article  CAS  PubMed  Google Scholar 

  31. Ortega MJ, PantojaDelosReyesZubía JJCE (2017) 5-alkylresorcinol derivatives from the Bryozoan Schizomavella mamillata: Isolation, synthesis, and antioxidant activity. Mar Drugs 15(11):344. https://doi.org/10.3390/md15110344

    Article  CAS  PubMed Central  Google Scholar 

  32. Lu L, Rong W, Massart S, Zhang Z (2018) Genome-wide identification and expression analysis of cutinase gene family in Rhizoctonia cerealis and functional study of an active cutinase RcCUT1 in the fungal–wheat interaction. Front Microbiol. https://doi.org/10.3389/fmicb.2018.01813

    Article  PubMed  PubMed Central  Google Scholar 

  33. Schäfer W (1993) The role of cutinase in fungal pathogenicity. Trends Microbiol 1(2):69–71. https://doi.org/10.1016/0966-842X(93)90037-R

    Article  PubMed  Google Scholar 

  34. Yang Y, Zhang Y, Li B, Yang X, Dong Y, Qiu D (2018) A Verticillium dahliae pectate lyase induces plant immune responses and contributes to virulence. Front Plant Sci. https://doi.org/10.3389/fpls.2018.01271

    Article  PubMed  PubMed Central  Google Scholar 

  35. Kovtunovych G, Lar O, Kamalova S, Kordyum V, Kleiner D, Kozyrovska N (1999) Correlation between pectate lyase activity and ability of diazotrophic Klebsiella oxytoca VN 13 to penetrate into plant tissues. Plant Soil 215(1):1–6. https://doi.org/10.1023/A:1004790122353

    Article  CAS  Google Scholar 

  36. Bai Y, Müller DB, Srinivas G, Garrido-Oter R, Potthoff E, Rott M, Dombrowski N, Münch PC, Spaepen S, Remus-Emsermann M, Hüttel B, McHardy AC, Vorholt JA, Schulze-Lefert P (2015) Functional overlap of the Arabidopsis leaf and root microbiota. Nature 528(7582):364–369. https://doi.org/10.1038/nature16192

    Article  CAS  PubMed  Google Scholar 

  37. Pio TF, Macedo GA (2009) Cutinases: properties and industrial applications. Adv Appl Microbiol. 66:77–95. https://doi.org/10.1016/S0065-2164(08)00804-6

  38. Chen S, Tong X, Woodard RW, Du G, Wu J, Chen J (2008) Identification and characterization of bacterial cutinase. J Biol Chem 283(38):25854–25862. https://doi.org/10.1074/jbc.M800848200

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Madeira JV, Contesini FJ, Calzado F, Rubio MV, Zubieta MP, Lopes DB, de Melo RR (2017) Chapter 18—Agro-industrial residues and microbial enzymes: an overview on the eco-friendly bioconversion into high value-added products. In: Brahmachari G (ed) Biotechnology of microbial enzymes. Academic Press, Cambridge, pp 475–511. https://doi.org/10.1016/B978-0-12-803725-6.00018-2

    Chapter  Google Scholar 

  40. Lefort V, Desper R, Gascuel O (2015) FastME 2.0: A comprehensive, accurate, and fast distance-based phylogeny inference program. Mol Biol Evol 32(10):2798–2800. https://doi.org/10.1093/molbev/msv150

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Farris JS (1972) Estimating phylogenetic trees from distance matrices. Am Nat 106(951):645–668

    Article  Google Scholar 

Download references

Acknowledgements

The work presented is part of the DARWIN21 project (http://www.darwin21.org/), with the objective to improve sustainable agriculture on arid lands by exploiting microbes isolated from pioneer desert plants that are able to survive in extreme environmental conditions. The authors would thank all members of Hirt lab, CDA management team and the Bioscience Core Labs in KAUST for the technical assistance and for their help in many aspects of this work.

Funding

The work was funded by KAUST baseline research project BAS/1/1062-01-01 of H.H.

Author information

Authors and Affiliations

Authors

Contributions

AE performed the, gDNA extraction and taxonomic analysis. SB performed genome assembly, gene prediction, annotation of genome data, IA integrated all bioinformatics databases and facilitated all genomic annotation platforms. AE, MS, and HH wrote the manuscript. MS, and HH conceived the overall study.

Corresponding author

Correspondence to Heribert Hirt.

Ethics declarations

Conflict of interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file 1 (DOCX 109 kB)

Supplementary file 2 (XLSX 25 kB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Eida, A.A., Bougouffa, S., Alam, I. et al. Complete Genome Sequence of Cellulomonas sp. JZ18, a Root Endophytic Bacterium Isolated from the Perennial Desert Tussock-Grass Panicum turgidum. Curr Microbiol 78, 1135–1141 (2021). https://doi.org/10.1007/s00284-021-02429-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00284-021-02429-5

Navigation