Skip to main content

Advertisement

Log in

Antifouling Activities of Antagonistic Marine Bacterium Pseudomonas putida Associated with an Octopus

  • Research Article
  • Published:
Proceedings of the National Academy of Sciences, India Section B: Biological Sciences Aims and scope Submit manuscript

Abstract

Bacterial symbionts associated with an octopus were isolated and their intra and extracellular extracts were tested for the antagonistic activities against biofilm-forming bacteria. Among the three antagonistic bacterial symbionts, both intra and extracellular extracts of the bacterium, Pseudomonas putida exhibited strong antibacterial activity against biofilm bacteria. Results also showed that both intra and extracellular extracts of P. putida significantly reduced the biofilm formation on test surfaces. The antifouling coating developed with bacterial extracts of P. putida significantly reduced the recruitment of biofouling organisms over a period of 50 days in the coastal waters. The bioactive fractions were partially purified using chromatographic methods such as thin-layer chromatography and high performance liquid chromatography. Based on the findings, it is concluded that potential antifouling compounds could be isolated from the antagonistic bacteria isolated from the octopus.

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
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  1. Verschuere L, Rombaut G, Sorgeloos P, Verstraete W (2000) Probiotic bacteria as biological agents in aquaculture. Microbiol Mole Biol Rev 64(4):655–671

    Article  CAS  Google Scholar 

  2. Slattery M, Rajbhandari I, Wesson K (2001) Competition-mediated antibiotic induction in the marine bacterium Streptomyces tenjimariensis. Microb Ecol 41:90–96

    CAS  PubMed  Google Scholar 

  3. Patterson GL, Bolis CM (1997) Fungal cell-wall polysaccharides elicit an antifungal secondary metabolite (phytoalexin) in the cyanobacterium Scytonema ocellatum. J Phycol 33:54–60

    Article  CAS  Google Scholar 

  4. Lemos ML, Toranzo AE, Barja LJ (1986) Antibiotic activity of epiphytic bacteria isolated from intertidal seaweeds. Microb Ecol 11:149–163

    Article  Google Scholar 

  5. Zhang J, Shen Y, Liu J, Wei D (2005) Antimetastatic effect of prodigiosin through inhibition of tumor invasion. Biochem Pharmacol 69(3):407–414

    Article  CAS  PubMed  Google Scholar 

  6. Burkholder PR, Reutzler K (1969) Antimicrobial activity of some marine sponges. Nature 222:983–984

    Article  CAS  PubMed  Google Scholar 

  7. Newbold RW, Paul R, Jensen PR, Fenical W, Pawlik JR (1999) Antimicrobial activity of Caribbean sponge extracts. Aquat Microb Ecol 19:279–284

    Article  Google Scholar 

  8. Boyed KG, Adams DR, Burgess JG (1999) Antimicrobial and repellent activities of marine bacteria associated with algal surfaces. Biofouling 14:227–236

    Article  Google Scholar 

  9. Burgess JG, Miyashita H, Sudo H, Matsunaga T (1991) Antibiotic bacterium by the marine photosynthetic bacterium Chromatiun purpuratum NKPB 031404, localization of activity to the chromotophores. FEMS Microbiol Lett 84:301–306

    Article  CAS  Google Scholar 

  10. Holmstrom C, James S, Neilan BA, White DC, Kjelleberge S (1996) Pseudoalte-romonas tunicate sp. Nov., a bacterium that produces antifouling agents. Int J Syst Bacteriol 48:1205–1212

    Article  Google Scholar 

  11. James G, Holmstrom C, Kjelleberg S (1996) Purification and characterization of a novel antibacterial protein from the marine bacterium D2. Appl Environ Microbiol 62:2783–2788

    CAS  PubMed Central  PubMed  Google Scholar 

  12. Burgess JG, Boyd KG, Armstrong E, Jiang Z, Yan L, Berggren M, May U, Pisacane T, Granmo A, Adams DR (2003) The development of a marine natural product based antifouling paint. Biofouling 19:197–205

    Article  CAS  PubMed  Google Scholar 

  13. Brammavidhya S, Usharani G (2013) Bioactive potential of sponge associated Bacillus cereus SBS02 isolated from Hyattela cribriformis. Intl J Res Environ Sci Technol 3(2):61–64

    Google Scholar 

  14. Graca AP, Viana F, Bondoso J, Correia MI, Gomes L, Humanes M, Reis A, Xavier JR, Gaspar H, Lage OM (2015) The antimicrobial activity of heterotrophic bacteria isolated from the marine sponge Erylus deficiens (Astrophorida, Geodiidae). Front Microbiol 6:389

    PubMed Central  PubMed  Google Scholar 

  15. Hodson SL, Burke CM, Bissett AP (2000) Biofouling of fish-cage netting: the efficacy of a silicone coating and the effect of netting colour. Aquaculture 184:277–290

    Article  Google Scholar 

  16. Callow ME, Callow JE (2002) Marine biofouling: a sticky problem. Biologist 49:10–14

    PubMed  Google Scholar 

  17. Chambers LD, Stokes KR, Walsh FC, Wood RJK (2006) Modern approaches to marine antifouling coatings. Surf Coat Tech 201:3642–3652

    Article  CAS  Google Scholar 

  18. Evans SM (2001) Anti-fouling materials. Newcastle University, Tyne and Wear, London, pp 170–176

    Google Scholar 

  19. Gibbs PE, Bryan GW, Pascoe PL, Burt GR (1990) Reproductive abnormalities in female Ocenebra erinacea (Gastropoda) resulting from tributiletin induced imposex. J Mar Biol 70:639–656

    Article  Google Scholar 

  20. Stewart C, De Mora SJ (1990) A review of the degradation of tri(nbutyl) tin in the marine environment. Environ Technol 11:565–570

    Article  CAS  Google Scholar 

  21. Konstantinou IK, Albanis TA (2004) Worldwide occurrence and effects of antifouling paint booster biocides in the aquatic environment: a review. Environ Int 30:235–248

    Article  CAS  PubMed  Google Scholar 

  22. Limna Mol VP, Raveendran TV, Parameswaran PS, Kunnath RJ, Sathyan N (2010) Antifouling sesquiterpene from the India soft coral, Sinularia kavarattiensis and Alderslade prita. Indian J Mar Sci 39(2):270–273

    Google Scholar 

  23. Ananda TP, Bhata AW, Shouche YS, Siddharth URY, Sarmaa SP (2006) Antimicrobial activity of marine bacteria associated with sponges from the waters off the coast of South East India. Microbiol Res 161:252–262

    Article  Google Scholar 

  24. Shankar CVS, Satheesh S, Viju N, Punitha SMJ (2015) Antibacterial and biofilm inhibitory activities of bacteria associated with polychaetes. J Coast Life Med 3(6):495–502

    Google Scholar 

  25. Turner S, Pryer KM, Miao VP, Palmer JD (1999) Investigating deep phylogenetic relationships among cyanobacteria and plastids by small subunit rRNA sequence analysis. J Eukaryot Microbiol 46:327–338

    Article  CAS  PubMed  Google Scholar 

  26. Margassery LM, Kennedy J, Gara FO, Dobson AD, Morrissey JP (2012) Diversity and antibacterial activity of bacteria isolated from the coastal marine sponges Amphilectus fucorum and Eurypon major. Lett Appl Microbiol 55:2–8

    Article  CAS  PubMed  Google Scholar 

  27. Jain A, Nlshad KK, Narayan KK, Bhosle B (2007) Effects of DNP on the cell surface properties of marine bacteria and its implication for adhesion to surfaces. Biofouling 23:171–177

    Article  CAS  PubMed  Google Scholar 

  28. Viju N, Satheesh S, Punitha SMJ (2016) Antibiofilm and antifouling activities of extracellular polymeric substances isolated from the bacteria associated with marine gastropod Turbo sp. Hydrobiol Oceanol Stud 45(1) (in Press)

  29. Satheesh S, Soniamby AR, Sunjaiy Shankar CV, Punitha SMJ (2012) Antifouling activities of marine bacteria associated with sponge (Sigmadocia sp.). J Ocean Univ China 11:354–360

    Article  CAS  Google Scholar 

  30. Karwacki MT, Kadouri DE, Bendaoud M, Izano EA, Sampathkumar V, Inzana TJ, Kaplan JB (2013) Antibiofilm activity of Actinobacillus pleuropneumoniae serotype 5 capsular polysaccharide. PLoS One 8(5):e63844

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  31. Viju N, Anitha A, Sharmin Vini S, Sunjaiy Shankar CV, Satheesh S, Punitha SMJ (2014) Antibiofilm activities of extracellular polymeric substances produced by bacterial symbionts of seaweeds. Indian J Geom Mar Sci 43(11):2136–2146

    Google Scholar 

  32. Jayanth K, Jeyasekaran G, Jeya Shakila R (2002) Isolation of marine bacteria antagonistic to human pathogens. Indian J Marin Sci 31(1):39–44

    CAS  Google Scholar 

  33. Burgess JG, Jordan EM, Bregu M, Mearns-Spragg A, Boyd KG (1999) Microbial antagonism: a neglected avenue of natural products research. J Biotechnol 70:27–32

    Article  CAS  PubMed  Google Scholar 

  34. Chelossi E, Milanese M, Milano A, Pronzato R, Riccardi G (2004) Characterization and antimicrobial activity of epibiotic bacteria from Petrosia ficiformis (Porifera, Demospongiae). J Exp Mar Biol Ecol 309:21–33

    Article  CAS  Google Scholar 

  35. Gnanambal KME, Chellaram C, Patterson J (2005) Isolation of antagonistic marine bacteria from the surface of the gonorian corals at Tuticorin, South east cost of India. Indian J Mar Sci 34(3):316–319

    Google Scholar 

  36. Chellaram C, Anand TP, Kesavan D, Chandrika M, Gladis C, Priya G (2012) Antagonistic effect of hard coral associated bacteria from Tuticorin Coastal waters. Int J Pharm Pharm Sci 4(1):580–583

    Google Scholar 

  37. Emmanuel S, Jebasingh J, Murugan A (2011) Antagonistic activity of the barnacle (Balanus Amphitrite) associated bacteria against human bacterial pathogens. World Appl Sci J 12(2):202–207

    Google Scholar 

  38. Krishnakumar S, Bai VDM (2014) Antagonistic characterization of marine microalgae surface associated bacterium Staphylococcus albus SBU1 against selected human pathogens. Int J PharmTech Res 6(7):2008–2014

    Google Scholar 

  39. Jensen PR, Fenical W (1994) Strategies for the discovery of secondary extracts from marine bacteria: ecological perspectives. Annu Rev Microbiol 48:559–584

    Article  CAS  PubMed  Google Scholar 

  40. Skariyachan S, Rao AG, Patil MR, Saikia B, Bharadwaj KN, Rao GS (2013) Antimicrobial potential of metabolites extracted from bacterial symbionts associated with marine sponges in coastal area of Gulf of Mannar Biosphere, India. Lett Appl Microbiol 58(3):231–241

    Article  PubMed  Google Scholar 

  41. Delfan AS, Etemadifar Z, Bouzari M, Emtiazi G (2012) Screening of noval bacteriophage infection in Pseudomonas putida isolated from potato disease. Jundishapur J Microbiol 5(4):550–554

    Article  Google Scholar 

  42. Dupont S, Carré-Mlouka A, Descarrega F, Ereskovsky A, Longeon A, Mouray E, Florent I, Bourguet-Kondracki ML (2013) Diversity and biological activities of the bacterial community associated with the marine sponge Phorbas tenacior (Porifera, Demospongiae). Lett Appl Microbiol 58(1):42–52

    Article  PubMed  Google Scholar 

  43. Isnansetyo A, Cui L, Hiramatsu K, Kamei Y (2003) Antibacterial activity of 2,4 diacetylphloroglucinol produced by Pseudomonas sp. AMNS isolated from a marine algae, against vancomycin resistant Staphylococcus aureus. Int J Antimicrob AG 22(5):545–547

    Article  CAS  Google Scholar 

  44. Wratten SJ, Wolfe MS, Anderson RF, Faulkner DJ (1977) Antibiotic extracts from a marine Pseudomonas. Antimicrob Agents Chemother 11:411–414

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  45. Kodani S, Imoto A, Mitsutani A, Murakami M (2002) Isolation and identification of the anti algal compound, harmane (1-methyl-b-carboline), produced by the algicidal bacterium, Pseudomonas sp. K44–1. J App J Phycol 14:109–114

    Article  CAS  Google Scholar 

  46. Viju N, Satheesh S, Vincent Prakash SG (2013) Antibiofilm activity of coconut (Cocos nucifera Linn.) husk fibre extract. Saudi J Biol Sci 20:85–91

    Article  CAS  PubMed  Google Scholar 

  47. Trentin DS, Gorziza DF, Abraham WR, Antunes ALS, Lerner C, Mothes B, Termignoni C, Macedo AJ (2011) Antibiofilm activity of Cobetia marina filtrate upon Staphylococcus epidermidis catheter-related isolates. Braz J Microbiol 42:1329–1333

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  48. Jiang P, Li J, Han F, Duan G, Lu X, Gu Y, Yu W (2011) Antibiofilm activity of an exopolysaccharide from marine bacterium Vibrio sp. QY101. PLoS One 6(4):e18514

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  49. Costerton JW, Cheng KJ, Geesey GG, Ladd TIM, Nickel JC, Dasgupta M, Marie TJ (1987) Bacterial biofilms in nature and disease. Annu Rev Microbiol 41:435–464

    Article  CAS  PubMed  Google Scholar 

  50. Bazes A, Alla A, Philippe D, Fabienne F, Nelly K, Danièle M, Jean-Pascal B, Nathalie B (2009) Investigation of the antifouling constituents from the brown alga Sargassum muticum (Yendo) Fensholt. J Appl Phycol 21:395–403

    Article  CAS  Google Scholar 

  51. Jellali R, Campistrona I, Pasettoa P, Laguerrea A, Gohiera F, Helliob C, Pilard JF, Mougetc JL (2013) Antifouling activity of novel polyisoprene-based coatings made from photocurable natural rubber derived oligomers. Prog Org Coat 76:1203–1214

    Article  CAS  Google Scholar 

  52. Willemsen PR, Ferrari GM (1993) The use of anti-fouling compounds from sponges in anti-fouling paints. Surf Coat Int 10:423–427

    Google Scholar 

  53. Xu Y, He H, Schulz S, Liu X, Fusetani N, Xiong H, Xiao X, Qian PY (2010) Potent antifouling compounds produced by marine Streptomyces. Bioresour Technol 101:1331–1336

    Article  CAS  PubMed  Google Scholar 

  54. Manilal A, Sujith S, Sabarathnam B, Kiran GS, Selvin J, Shakir C, Lipton AP (2010) Antifouling potentials of seaweeds collected from the Southwest Coast of India. World J Agric Sci 6(6):670–675

    Google Scholar 

  55. Iyapparaj P, Revathi P, Ramasubburayan R, Prakash S, Palavesam A, Immanuel G, Anantharaman P, Sautreau A, Hellio C (2014) Antifouling and toxic properties of the bioactive extracts from the seagrasses Syringodium isoetifolium and Cymodocea serrulata. Ecotoxicol Environ Safe 03:54–60

    Article  Google Scholar 

  56. Piana M, Zadra M, De Brum TF, Boligon AA, Gonçalves AF, Da Cruz RC (2013) Analysis of rutin in the extract and gel of Viola tricolor. J Chromatogr Sci 51:406–411

    Article  CAS  PubMed  Google Scholar 

  57. Karimi E, Jaafar HZE (2011) HPLC and GC-MS determination of bioactive compounds in microwave obtained extracts of three varieties of Labisia pumila Benth. Molecules 16:6791–6805

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The authors are thankful to University Grants Commission for providing financial support through the major project scheme (Ref. F. No: 39-294/2010 SR).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to N. Viju.

Ethics declarations

Conflict of interest

The authors declare that there is no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Viju, N., Satheesh, S. & Punitha, S.M.J. Antifouling Activities of Antagonistic Marine Bacterium Pseudomonas putida Associated with an Octopus. Proc. Natl. Acad. Sci., India, Sect. B Biol. Sci. 87, 1113–1124 (2017). https://doi.org/10.1007/s40011-015-0691-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s40011-015-0691-x

Keywords

Navigation