3 Biotech

, 9:42 | Cite as

Complete genome sequence of Caulobacter flavus RHGG3T, a type species of the genus Caulobacter with plant growth-promoting traits and heavy metal resistance

  • Endong Yang
  • Leni Sun
  • Xiaoyuan Ding
  • Dongdong Sun
  • Jing Liu
  • Weiyun WangEmail author
Genome Reports


Caulobacter flavus RHGG3T, a novel type species in the genus Caulobacter, originally isolated from rhizosphere soil of watermelon (Citrullus lanatus), has the ability to improve the growth of watermelon seedling and tolerate heavy metals. In vitro, C. flavus RHGG3T was able to solubilize phosphate (80.56 mg L−1), produce indole-3-acetic acid (IAA) (11.58 mg L−1) and was resistant to multiple heavy metals (copper, zinc, cadmium, cobalt and lead). Inoculating watermelon with this strain increased shoot and root length by 22.1% and 43.7%, respectively, and the total number of lateral roots by 55.9% compared to non-inoculated watermelon. In this study, we present the complete genome sequence of C. flavus RHGG3T, which was comprised of a single circular chromosome of 5,659,202 bp with a G + C content of 69.25%. An annotation analysis revealed that the C. flavus RHGG3T genome contained 5172 coding DNA sequences, 9 rRNA and 55 tRNA genes. Genes related to plant growth promotion (PGP), such as those associated with phosphate solubilization, nitrogen fixation, IAA, phenazine, volatile compounds, spermidine and cobalamin synthesis, were found in the C. flavus RHGG3T genome. Some genes responsible for heavy metal tolerance were also identified. The genome sequence of strain RHGG3T reported here provides new insight into the molecular mechanisms underlying the promotion of plant growth and the resistance to heavy metals in C. flavus. This study will be valuable for further exploration of the biotechnological applications of strain RHGG3T in agriculture.


Caulobacter flavus RHGG3T Complete genome sequence Plant growth-promoting rhizobacteria Heavy metal resistance 



This study was supported by the National Natural Science Foundation of China (41401275, 31800057), the Anhui Provincial Major Scientific and Technological Special Project (17030701023) and National Agricultural Science and Technology Achievements Transformation Fund (2014GB2C300022).

Compliance with ethical standards

Conflict of interest

The authors declare no conflicts of interest.

Supplementary material

13205_2019_1569_MOESM1_ESM.doc (44 kb)
Supplementary material 1 (DOC 43 KB)


  1. Achal V, Savant VV, Reddy MS (2007) Phosphate solubilization by a wild type strain and UV-induced mutants of Aspergillus tubingensis. Soil Biol Biochem 39:695–699CrossRefGoogle Scholar
  2. Alcazar R, Bitrian M, Bartels D, Koncz C, Altabella T, Tiburcio AF (2011) Polyamine metabolic canalization in response to drought stress in Arabidopsis and the resurrection plant Craterostigma plantagineum. Plant Signal Behav 6:243–250CrossRefGoogle Scholar
  3. Ash K, Brown T, Watford T, Scott LE, Stephens C, Ely B (2014) A comparison of the Caulobacter NA1000 and K31 genomes reveals extensive genome rearrangements and differences in metabolic potential. Open Biol 4:140128CrossRefGoogle Scholar
  4. Aziz RK, Bartels D, Best AA, DeJongh M, Disz T, Edwards RA, Formsma K, Gerdes S, Glass EM, Kubal M, Meyer F, Olsen GJ, Olson R, Osterman AL, Overbeek RA, McNeil LK, Paarmann D, Paczian T, Parrello B, Pusch GD, Reich C, Stevens R, Vassieva O, Vonstein V, Wilke A, Zagnitko O (2008) The RAST server: rapid annotations using subsystems technology. BMC Genom 9:75CrossRefGoogle Scholar
  5. Belimov AA, Hontzeas N, Safronova VI, Demchinskaya SV, Piluzza G, Bullitta S, Glick BR (2005) Cadmium-tolerant plant growth-promoting bacteria associated with the roots of Indian mustard (Brassica juncea L. Czern.). Soil Biol Biochem 37:241–250CrossRefGoogle Scholar
  6. Bhattacharyya PN, Jha DK (2012) Plant growth-promoting rhizobacteria (PGPR): emergence in agriculture. World J Microbiol Biotechnol 28:1327–1350CrossRefGoogle Scholar
  7. Chen Y, Shen X, Peng H, Hu H, Wang W, Zhang X (2015) Comparative genomic analysis and phenazine production of Pseudomonas chlororaphis, a plant growth-promoting rhizobacterium. Genom Data 4:33–42CrossRefGoogle Scholar
  8. Chin CS, Alexander DH, Marks P, Klammer AA, Drake J, Heiner C, Clum A, Copeland A, Huddleston J, Eichler EE, Turner SW, Korlach J (2013) Nonhybrid, finished microbial genome assemblies from long-read SMRT sequencing data. Nat Methods 10:563–569CrossRefGoogle Scholar
  9. Delcher AL, Bratke KA, Powers EC, Salzberg SL (2007) Identifying bacterial genes and endosymbiont DNA with Glimmer. Bioinformatics 23:673–679CrossRefGoogle Scholar
  10. He P, Hao K, Blom J, Ruckert C, Vater J, Mao Z, Wu Y, Hou M, He Y, Borriss R (2012) Genome sequence of the plant growth promoting strain Bacillus amyloliquefaciens subsp. plantarum B9601-Y2 and expression of mersacidin and other secondary metabolites. J Biotechnol 164:281–291CrossRefGoogle Scholar
  11. Hu P, Brodie EL, Suzuki Y, McAdams HH, Andersen GL (2005) Whole-genome transcriptional analysis of heavy metal stresses in Caulobacter crescentus. J Biotechnol 187:8437–8449Google Scholar
  12. Krzywinski M, Schein J, Birol I, Connors J, Gascoyne R, Horsman D, Jones SJ, Marra MA (2009) Circos: an information aesthetic for comparative genomics. Genome Res 19:1639–1645CrossRefGoogle Scholar
  13. Lowe TM, Eddy SR (1997) tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 25:955–964CrossRefGoogle Scholar
  14. Moya G, Yan ZF, Won KH, Yang JE, Wang QJ, Kook MC, Yi TH (2017) Caulobacter hibisci sp. nov., isolated from rhizosphere of Hibiscus syriacus L. (Mugunghwa flower). Int J Syst Evol Microbiol 67:3167–3173CrossRefGoogle Scholar
  15. Pereira SIA, Monteiro C, Vega AL, Castro PML (2016) Endophytic culturable bacteria colonizing Lavandula dentata L. plants: isolation, characterization and evaluation of their plant growth-promoting activities. Ecol Eng 87:91–97CrossRefGoogle Scholar
  16. Ping L, Boland W (2004) Signals from the underground: bacterial volatiles promote growth in Arabidopsis. Trends Plant Sci 9(6):263–266CrossRefGoogle Scholar
  17. Qin S, Li J, Chen HH, Zhao GZ, Zhu WY, Jiang CL, Xu LH, Li WJ (2009) Isolation, diversity, and antimicrobial activity of rare Actinobacteria from medicinal plants of tropical rain forests in Xishuangbanna. China Appl Environ Microb 75:6176–6186CrossRefGoogle Scholar
  18. Qin S, Feng WW, Wang TT, Ding P, Xing K, Jiang JH (2017) Plant growth-promoting effect and genomic analysis of the beneficial endophyte Streptomyces sp. KLBMP 5084 isolated from halophyte Limonium sinense. Plant Soil 416:117–132CrossRefGoogle Scholar
  19. Ryu CM, Farag MA, Hu CH, Reddy MS, Wei HX, Pare PW, Kloepper JW (2003) Bacterial volatiles promote growth in Arabidopsis. P Natl Acad Sci USA 100:4927–4932CrossRefGoogle Scholar
  20. Sun LN, Yang ED, Wei JC, Tang XY, Cao YY, Han GM (2015) Caulobacter flavus sp. nov., a stalked bacterium isolated from rhizosphere soil. Int J Syst Evol Microbiol 65:4374–4380CrossRefGoogle Scholar
  21. Sun LN, Yang ED, Hou XT, Wei JC, Yuan ZX, Wang WY (2017) Caulobacter rhizosphaerae sp. nov., a stalked bacterium isolated from rhizosphere soil. Int J Syst Evol Microbiol 67:1771–1776CrossRefGoogle Scholar
  22. Tatusov RL, Galperin MY, Natale DA, Koonin EV (2000) The COG database: a tool for genome-scale analysis of protein functions and evolution. Nucleic Acids Res 28:33–36CrossRefGoogle Scholar
  23. Vaccaro BJ, Lancaster WA, Thorgersen MP, Zane GM, Younkin AD, Kazakov AE, Wetmore KM, Deutschbauer A, Arkin AP, Novichkov PS, Wall JD, Adams MW (2016) Novel metal cation resistance systems from mutant fitness analysis of denitrifying Pseudomonas stutzeri. Appl Environ Microbiol 82:6046–6056CrossRefGoogle Scholar
  24. Wang JF, Zhang YQ, Li Y, Wang XM, Nan WB, Hu YF, Zhang H, Zhao CZ, Wang F, Li P, Shi HY, Bi YR (2015) Endophytic microbes Bacillus sp. LZR216-regulated root development is dependent on polar auxin transport in Arabidopsis seedlings. Plant Cell Rep 34:1075–1087CrossRefGoogle Scholar
  25. Xie SS, Jiang HY, Ding T, Xu QQ, Chai WB, Cheng BJ (2018) Bacillus amyloliquefaciens FZB42 repressed plant miR846 to induce systemic resistance via jasmonic acid-dependent signaling pathway. Mol Plant Pathol 19(7):1612–1623CrossRefGoogle Scholar
  26. Yung MC, Park DM, Overton KW, Blow MJ, Hoover CA, Smit J, Murray SR, Ricci DP, Christen B, Bowman GR, Jiao Y (2015) Transposon mutagenesis paired with deep sequencing of Caulobacter crescentus under uranium stress reveals genes essential for detoxification and stress tolerance. J Bacteriol 197:3160–3172CrossRefGoogle Scholar
  27. Zhang L, Zhong J, Liu H, Xin KY, Chen CQ, Li QQ, Wei YH, Wang Y, Chen F, Shen XH (2017) Complete genome sequence of the drought resistance-promoting endophyte Klebsiella sp. LTGPAF-6F. J Biotechnol 246:36–39CrossRefGoogle Scholar

Copyright information

© King Abdulaziz City for Science and Technology 2019

Authors and Affiliations

  • Endong Yang
    • 1
  • Leni Sun
    • 1
  • Xiaoyuan Ding
    • 1
  • Dongdong Sun
    • 1
  • Jing Liu
    • 1
  • Weiyun Wang
    • 1
    Email author
  1. 1.School of Life ScienceAnhui Agricultural UniversityHefeiPeople’s Republic of China

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