Skip to main content
SpringerLink
Log in

A diguanylate cyclase regulates biofilm formation in Rhodococcus sp. NJ-530 from Antarctica

  • Original Article
  • Published:
3 Biotech Aims and scope Submit manuscript

Abstract

Biofilms represent a protective survival mode in which bacteria adapt themselves to the natural environment for survival purposes. Biofilm formation is regulated by 3,5-cyclic diguanylic acid (c-di-GMP), which is a universal second messenger molecule in bacteria. Diguanylate cyclase (DGC) catalyses c-di-GMP intracellular synthesis, which plays important roles in bacterial adaptation to the natural environment. In this study, the DGC gene was first cloned from Antarctic Rhodococcus sp. NJ-530. DGC contained 948 nucleotides and encoded 315 amino acids with a molecular weight of 34.6 KDa and an isoelectric point of 5.58. qRT–PCR demonstrated that the DGC expression level was significantly affected by lower salinity and temperature. Consistently, more biofilm formation occurred under the same stress. It has been shown that Rhodococcus sp. NJ-530 can adapt to the extreme environment in Antarctica, which is closely related to biofilm formation. These results provide an important reference for studying the adaptive mechanism of Antarctic microorganisms to this extreme environment.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  • An ML, Zheng Z, Qu CF, Wang XX, Chen H, Shi CL, Miao JL (2018) The first (6–4) photolyase with DNA damage repair activity from the Antarctic microalga Chlamydomonas sp. ICE-L. Mutat Res 809:13–19

    CAS  PubMed  Google Scholar 

  • Azevedo NF, Pinto AR, Reis NM, Vieira MJ, Keevil CW (2006) Shear stress, temperature, and inoculation concentration influence the adhesion of water-stressed Helicobacter pylori to stainless steel 304 and polypropylene. Appl Environ Microbiol 72(4):2936–2941

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bazire A, Diab F, Jebbar M, Haras D (2007) Influence of high salinity on biofilm formation and benzoate assimilation by Pseudomonas aeruginosa. J Ind Microbiol Biotechnol 34(1):5–8

    CAS  PubMed  Google Scholar 

  • Berlanga M, Guerrero R (2016) Living together in biofilms: the microbial cell factory and its biotechnological implications. Microb Cell Fact 15(1):165–175

    PubMed  PubMed Central  Google Scholar 

  • Bolter M (2004) Ecophysiology of psychrophilic and psychrotolerant microorganisms. Cell Mol Biol (Noisy-le-Grand, France) 50(5):563–573

  • Cady NC, McKean KA, Behnke J, Kubec R, Mosier AP, Kasper SH, Burz DS, Musah RA (2012) Inhibition of biofilm formation, quorum sensing and infection in Pseudomonas aeruginosa by natural products-inspired organosulfur compounds. PLoS ONE 7(6):e38492

    CAS  PubMed  PubMed Central  Google Scholar 

  • Castro M, Deane SM, Ruiz L, Rawlings DE, Guiliani N (2015) Diguanylate cyclase null mutant reveals that C-Di-GMP pathway regulates the motility and adherence of the extremophile bacterium Acidithiobacillus caldus. PLoS ONE 10(2):e0116399

    PubMed  PubMed Central  Google Scholar 

  • Christen B, Christen M, Paul R, Schmid F, Folcher M, Jenoe P, Meuwly M, Jenal U (2006) Allosteric control of cyclic di-GMP signaling. J Biol Chem 281(42):32015–32024

    CAS  PubMed  Google Scholar 

  • Dessi-Fulgheri F (2013) Antarctic ecosystems: an extreme environment in a changing world. Front Biogeogr 5(1):2215–2232

    Google Scholar 

  • Doll K, Jongsthaphongpun KL, Stumpp NS, Winkel A, Stiesch M (2016) Quantifying implant-associated biofilms: Comparison of microscopic, microbiologic and biochemical methods. J Microbiol Methods 130:61–68

    CAS  PubMed  Google Scholar 

  • Donlan RM (2002) Biofilms: microbial life on surfaces. Emerg Infect Dis 8(9):881–890

    PubMed  PubMed Central  Google Scholar 

  • Fazli M, Rybtke M, Steiner E, Weidel E, Berthelsen J, Groizeleau J, Bin W, Zhi BZ, Yaming Z, Kaever V, Givskov M, Hartmann RW, Eberl L, Tolker-Nielsen T (2017) Regulation of Burkholderia cenocepacia biofilm formation by RpoN and the c-di-GMP effector BerB. Microbiologyopen 6(1483):e00480

    PubMed Central  Google Scholar 

  • Gjermansen M, Nilsson M, Yang L, Tolker-Nielsen T (2010) Characterization of starvation-induced dispersion in Pseudomonas putida biofilms: genetic elements and molecular mechanisms. Mol Microbiol 75(4):815–826

    CAS  PubMed  Google Scholar 

  • Głowacki R, Strek P, Zagórska-Swiezy K, Składzień J, Oleś K, Hydzik-Sobocińska K, Miodoński A (2008) Biofilm from patients with chronic rhinosinusitis morphological SEM studies. Otolaryngol Pol 62(3):305–310

    PubMed  Google Scholar 

  • Gompelman M, van Asten SAV, Peters EJG (2016) Update on the role of infection and biofilms in wound healing: pathophysiology and treatment. Plast Reconstr Surg 138(3):61S-70S

    CAS  PubMed  Google Scholar 

  • Gupta K, Liao J, Petrova OE, Cherny KE, Sauer K (2014) Elevated levels of the second messenger c-di-GMP contribute to antimicrobial resistance of Pseudomonas aeruginosa. Mol Microbiol 92(3):488–506

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ha DG, O’Toole GA (2015) C-di-GMP and its effects on biofilm formation and dispersion: a pseudomonas aeruginosa review. Microbiol Spectr. https://doi.org/10.1128/microbiolspec.MB-0003-2014

    Article  PubMed  Google Scholar 

  • Hachulla EV, Gressin L, Guillevin PD, Groote J, Cabane P, Carpentier C, Francès A (2004) Bacterial biofilms: from the natural environment to infectious diseases. Nat Rev Microbiol 2(2):95–108

    Google Scholar 

  • Hall-Stoodley L, Costerton JW, Stoodley P (2004) Bacterial biofilms:from the natural environment to infectious diseases. Nat Rew Microbiol 2:95–108

    CAS  Google Scholar 

  • He YY, Wang YB, Zheng Z, Liu FM, An ML, He XD, Qu CF, Li LL, Miao JL (2017) Cloning and stress-induced expression analysis of calmodulin in the antarctic alga Chlamydomonas sp. ICE-l Curr Microbiol 74(8):921–929

    CAS  PubMed  Google Scholar 

  • He YY, Qu CF, Zhang LP, Miao JL (2021) DNA photolyase from Antarctic marine bacterium Rhodococcus sp. NJ-530 can repair DNA damage caused by ultraviolet. 3 Biotech. https://doi.org/10.1007/s13205-021-02660-8

    Article  PubMed  PubMed Central  Google Scholar 

  • Hengge R (2016) Trigger phosphodiesterases as a novel class of c-di-GMP effector proteins. Philosoph Trans Royal Soc B Biol Sci 371(1707):20150498

    Google Scholar 

  • Jakobsen TH, Tolker-Nielsen T, Givskov M (2017) Bacterial biofilm control by perturbation of bacterial signaling processes. Int J Mol Sci 18(9):1970

    PubMed Central  Google Scholar 

  • Jenal U, Reinders A, Lori C (2017) Cyclic di-GMP: second messenger extraordinaire. Nat Rev Microbiol 15(5):271–284

    CAS  PubMed  Google Scholar 

  • Jones CJ, Wozniak DJ (2017) Congo Red Stain Identifies Matrix Overproduction and Is an Indirect Measurement for c-di-GMP in Many Species of Bacteria. Methods Mol Biol 1657:147–156

    CAS  PubMed  Google Scholar 

  • Kaplan JB (2010) Biofilm dispersal: mechanisms, clinical implications, and potential therapeutic uses. J Dent Res 89:205–218

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kasim WA, Gaafar RM, Abou-Ali RM, Omar MN, Hewait HM (2016) Effect of biofilm forming plant growth promoting rhizobacteria on salinity tolerance in barley. Ann Agric Sci. https://doi.org/10.1016/j.aoas.2016.07.003

    Article  Google Scholar 

  • Lee K, Yoon SS (2017) Pseudomonas aeruginosa biofilm, a programmed bacterial life for fitness. J Microbiol Biotechnol 27(6):1053–1064

    CAS  PubMed  Google Scholar 

  • Li C, Ma L, Mou SL, Wang YB, Zheng Z, Liu FM, Qi XQ, An ML, Chen H, Miao JL (2015) Cyclobutane pyrimidine dimers photolyase from extremophilic microalga: remarkable UVB resistance and efficient DNA damage repair. Mutat Res 773:37–42

    CAS  PubMed  Google Scholar 

  • Li LL, An ML, Qu CF, Zheng Z, Wang YB, Liu FM, He YY, He XD, Miao JL (2017) Molecular cloning and expression analysis of major intrinsic protein gene in Chlamydomonas sp. ICE-L from Antarctica. Extremophiles 21(4):817–827

    CAS  PubMed  Google Scholar 

  • Liu YJ, Xie J, Zhao LJ, Qian YF, Zhao Y, Liu X (2015) Biofilm formation characteristics of pseudomonas lundensis isolated from meat. J Food Sci 80(12):2904–2910

    Google Scholar 

  • Livak KJ, Schmittgen TD (2002) Analysis of relative gene expression using different real-time quantitative PCR. Methods 25(4):402–408

    Google Scholar 

  • Ma Q, Yang Z, Pu M, Peti W, Wood TK (2010) Engineering a novel c-di-GMP-binding protein for biofilm dispersal. Environ Microbiol 13(3):631–642

    PubMed  PubMed Central  Google Scholar 

  • Marshall SH, Gómez FA, Ramírez R, Nilo L, Henríquez V (2012) Biofilm generation by Piscirickettsia salmonis under growth stress conditions: a putative in vivo survival/persistence strategy in marine environments. Res Microbiol 163(8):557–566

    CAS  PubMed  Google Scholar 

  • Mei X, Xing D, Yang Y, Liu Q, Zhou H, Guo C, Ren N (2017) Adaptation of microbial community of the anode biofilm in microbial fuel cells to temperature. Bioelectrochemistry 117:29–33

    CAS  PubMed  Google Scholar 

  • Mou SL, Zhang X, Ye NH, Dong M, Liang C, Liang Q, Miao JL, Xu D, Zheng Z (2012) Cloning and expression analysis of two different LhcSR genes involved in stress adaptation in an Antarctic microalga, Chlamydomona sp. ICE-L. Extremophiles 16(2):193–203

    CAS  PubMed  Google Scholar 

  • Nagar V, Godambe LP, Bandekar JR, Shashidhar R (2017) Biofilm formation by Aeromonas strains under food-related environmental stress conditions. J Food Process Preserv. https://doi.org/10.1111/jfpp.13182

    Article  Google Scholar 

  • Opoku-Temeng C, Sintim HO (2017) Targeting c-di-GMP Signaling, Biofilm Formation, and Bacterial Motility with Small Molecules. Methods Mol Biol 1657:419–430

    CAS  PubMed  Google Scholar 

  • Qian W, Ma L, Gu L, Zhang L (2017) Preface for special issue on biofilm and c-di-GMP–Microbial society, c-di-GMP regulation, and new research techniques. Sheng Wu Gong Cheng Xue Bao 33(9):1351–1356

    PubMed  Google Scholar 

  • Rice SA, Koh KS, Queck SY, Labbate M, Lam KW, Kjelleberg S (2005) Biofilm formation and sloughing in Serratia marcescens are controlled by quorum sensing and nutrient cues. J Bacteriol 187(10):3477–3485

    CAS  PubMed  PubMed Central  Google Scholar 

  • Römling U, Galperin MY, Gomelsky M (2013) Cyclic di-GMP: the first 25 years of a universal bacterial second messenger. Microbiol Mol Biol Rev 77(1):1–52

    PubMed  PubMed Central  Google Scholar 

  • Schirmer T, Jenal U (2009) Structural and mechanistic determinants of c-di-GMP signalling. Nat Rev Microbiol 7(10):724–735

    CAS  PubMed  Google Scholar 

  • Shikuma NJ, Yildiz FH (2009) Identification and characterization of OscR, a transcriptional regulator involved in osmolarity adaptation in Vibrio cholerae. J Bacteriol 191(13):4082–4096

    CAS  PubMed  PubMed Central  Google Scholar 

  • Simm R, Morr M, Kader A, Nimtz M, Römling U (2004) GGDEF and EAL domains inversely regulate cyclic di-GMP levels and transition from sessility to motility. Mol Microbiol 53(4):1123–1134

    CAS  PubMed  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30(12):2725–2729

    CAS  PubMed  PubMed Central  Google Scholar 

  • Townsley L, Yildiz FH (2015) Temperature affects c-di-GMP signalling and biofilm formation in Vibrio cholerae. Environ Microbiol 17(11):4290–4305

    CAS  PubMed  PubMed Central  Google Scholar 

  • Townsley YFA (2015) The role of temperature in the environmental survival and transmission of Vibrio cholerae. https://escholarship.org/uc/item/104933v8

  • Ueda A, Wood TK (2009) Connecting quorum sensing, c-di-GMP, pel polysaccharide, and biofilm formation in Pseudomonas aeruginosa through tyrosine phosphatase TpbA (PA3885). PLoS Pathog 5(6):e1000483

    PubMed  PubMed Central  Google Scholar 

  • Vásquez-Ponce F, Higuera-Llantén S, Pavlov MS, Ramírez-Orellana R, Marshall SH, Olivares-Pacheco J (2017) Alginate overproduction and biofilm formation by psychrotolerant Pseudomonas mandelii depends on temperature in Antarctic marine sediments. Electron J Biotechnol 28(C):27–34

    Google Scholar 

  • Xu Z, Liang Y, Lin S, Chen D, Li B, Li L, Deng Y (2016) Crystal violet and XTT assays on staphylococcus aureus biofilm quantification. Curr Microbiol 73(4):474–482

    CAS  PubMed  Google Scholar 

  • Yang CY, Chin KH, Chuah ML, Liang ZX, Wang AH, Chou SH (2011) The structure and inhibition of a GGDEF diguanylate cyclase complexed with (c-di-GMP)(2) at the active site. Acta Crystallogr D Biol Crystallogr 67(12):997–1008

    CAS  PubMed  Google Scholar 

  • Zogaj X, Wyatt GC, Klose KE (2012) Cyclic di-GMP stimulates biofilm formation and inhibits virulence of Francisella novicida. Infect Immun 80(12):4239–4247

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Funding

This research was funded by the National Key Research and Development Program of China, grant no: 2018YFD0900705, Jinlai Miao, Basic Scientific Fund for National Public Research Institutes of China, grant no: 2020Q02, Changfeng Qu, Natural Science Foundation of China, grant no: 32000074, Changfeng Qu, grant no: 42176130, Jinlai Miao, Natural Science Foundation of Shandong, grant no: ZR2019BD023, Changfeng Qu, grant no: ZR2021MD044, Jinlai Miao,Tai Mountain Industry Leading Talent of Shan Dong, grant no: 2019TSCYCX-06, Jinlai Miao, Science and Technology Planning Project of Guangxi, grant no: AA21196002, Jinlai Miao

Author information

Authors and Affiliations

  1. College of Chemistry and Molecular Engineering, Qingdao University of Science and Technology, Qingdao, 266042, China

    Xixi Wang, Yashan Deng, Dan Li & Fushan Chen

  2. Key Laboratory of Marine Eco-Environmental Science and Technology, First Institute of Oceanography, Ministry of Natural Resource, No. 6 of Xianxialing Road, Qingdao, 266061, China

    Xixi Wang, Yingying He, Yashan Deng, Zhicong Zuo, Dan Li, Changfeng Qu & Jinlai Miao

  3. Laboratory for Marine Drugs and Bioproducts of Qingdao National Laboratory for Marine Science and Technology, Qingdao, 266237, China

    Changfeng Qu & Jinlai Miao

Authors
  1. Xixi Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yingying He
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yashan Deng
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Zhicong Zuo
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Dan Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Fushan Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Changfeng Qu
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Jinlai Miao
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Changfeng Qu or Jinlai Miao.

Ethics declarations

Conflicts of interest

No conflict of interest is associated with this work.

Ethical standards

This article does not contain any studies with human participants or animals performed by any of the authors.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 93 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, X., He, Y., Deng, Y. et al. A diguanylate cyclase regulates biofilm formation in Rhodococcus sp. NJ-530 from Antarctica. 3 Biotech 12, 27 (2022). https://doi.org/10.1007/s13205-021-03093-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s13205-021-03093-z

Keywords

Search

Navigation