Fisheries Science

, Volume 85, Issue 3, pp 533–543 | Cite as

Antagonistic activity of marine Streptomyces sp. S073 on pathogenic Vibrio parahaemolyticus

  • Mingxia Yang
  • Jun Zhang
  • Qiting Liang
  • Guanxin Pan
  • Jiachang Zhao
  • Miao Cui
  • Xinqing Zhao
  • Qizhong Zhang
  • Delin XuEmail author
Original Article Aquaculture


Marine Streptomyces sp. isolate S073 was shown to have strong antagonistic activity towards the pathogenic Vibrio parahaemolyticus using the agar diffusion method. The antagonistic substance(s) secreted into the supernatant was thermostable and non-proteinaceous in nature. S073 was found to produce carboxylate-type siderophores during most of its life cycle using a chrome azurol S assay. The antagonistic activity of S073 was mostly attributed to its higher ability to compete for iron compared with that of V. parahaemolyticus, as deduced from siderophore quantification. Iron supplementation studies indicated that additional mechanisms besides iron competition were simultaneously involved in governing the observed inhibition. Co-culture analysis indicated that S073, although disadvantaged in growth rate, was still competitive in inhibiting vibrios. The promising potential of S073 development as a biocontrol agent in aquaculture was discussed.


Vibrio parahaemolyticus Marine Streptomyces Antagonistic activity Siderophore Aquaculture Streptomyces Vibrios 



This work was supported by the National Natural Science Foundation of China (No. 31300046), the Natural Science Foundation of Guangdong Province (Nos. S2013010013705, 2015A030313319, 2018A030313578), Guangdong Marine and Fishery Bureau Science and Technology Project (No. A201601B05), and the Science and Technology Program of Guangzhou China (No. 201604020029)

Compliance with ethical standards

Conflict of interest

All authors declare that they have no conflict of interest.

Supplementary material

12562_2019_1309_MOESM1_ESM.docx (101 kb)
Supplementary material 1 (DOCX 100 kb)


  1. Al_husnan LA, Alkahtani MDF (2016) Molecular Identification of Streptomyces producing antibiotics and their antimicrobial activities. Ann Agric Sci 61:251–255CrossRefGoogle Scholar
  2. Assefa A, Abunna F (2018) Maintenance of fish health in aquaculture: review of epidemiological approaches for prevention and control of infectious disease of fish. Vet Med Int 2018:5432497CrossRefGoogle Scholar
  3. Augustine D, Jacob JC, Philip R (2016) Exclusion of Vibrio spp. by an antagonistic marine actinomycete Streptomyces rubrolavendulae M56. Aquacult Res 47:2951–2960CrossRefGoogle Scholar
  4. Baakza A, Vala AK, Dave BP (2004) A comparative study of siderophore production by fungi from marine and terrestrial habitats. J Exp Mar Biol Ecol 311:1–9CrossRefGoogle Scholar
  5. Baker-Austin C, Oliver JD, Alam M (2018) Vibrio spp. infections. Nat Rev Disease Primers 4:8CrossRefGoogle Scholar
  6. Bermudez-Brito M, Plaza-Diaz J, Munoz-Quezada S (2012) Probiotic mechanisms of action. Ann Nutr Metab 61:160–174CrossRefGoogle Scholar
  7. Bernal MG, Campa-Cordova AI, Saucedo PE (2015) Isolation and in vitro selection of actinomycetes strains as potential probiotics for aquaculture. Vet World 8:170–176CrossRefGoogle Scholar
  8. Bondad-Reantaso MG, Subasinghe RP, Arthur JR (2005) Disease and health management in Asian aquaculture. Vet Parasitol 132:249–272CrossRefGoogle Scholar
  9. Challis GL, Hopwood DA (2003) Synergy and contingency as driving forces for the evolution of multiple secondary metabolite production by Streptomyces species. Proc Natl Acad Sci USA 100(Suppl 2):14555–14561CrossRefGoogle Scholar
  10. Das S, Ward LR, Burke C (2008) Prospects of using marine actinobacteria as probiotics in aquaculture. Appl Microbiol Biotechnol 81:419–429CrossRefGoogle Scholar
  11. Defoirdt T, Boon N, Sorgeloos P (2007) Alternatives to antibiotics to control bacterial infections: luminescent vibriosis in aquaculture as an example. Trends Biotechnol 25:472–479CrossRefGoogle Scholar
  12. Defoirdt T, Sorgeloos P, Bossier P (2011) Alternatives to antibiotics for the control of bacterial disease in aquaculture. Curr Opin Microbiol 14:251–258CrossRefGoogle Scholar
  13. Elmahdi S, DaSilva LV, Parveen S (2016) Antibiotic resistance of Vibrio parahaemolyticus and Vibrio vulnificus in various countries: a review. Food Microbiol 57:128–134CrossRefGoogle Scholar
  14. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791CrossRefGoogle Scholar
  15. Garcia Bernal M, Trabal Fernandez N, Saucedo Lastra PE (2017) Streptomyces effect on the bacterial microbiota associated to Crassostrea sikamea oyster. J Appl Microbiol 122:601–614CrossRefGoogle Scholar
  16. Goarant C, Merien F, Berthe F (1999) Arbitrarily primed PCR to type Vibrio spp. pathogenic for shrimp. Appl Environ Microbiol 65:1145–1151Google Scholar
  17. Greenlees KJ, Machado J, Bell T (1998) Food borne microbial pathogens of cultured aquatic species. Vet Clin North Am Food Anim Pract 14:101–112CrossRefGoogle Scholar
  18. Hai NV (2015) The use of probiotics in aquaculture. J Appl Microbiol 119:917–935CrossRefGoogle Scholar
  19. Huang Y, Zhang L, Tiu L (2015) Characterization of antibiotic resistance in commensal bacteria from an aquaculture ecosystem. Front Microbiol 6:914Google Scholar
  20. Ina-Salwany MY, Al-Saari N, Mohamad A (2018) Vibriosis in fish: a review on disease development and prevention. J Aquat Anim Health 31:3–22CrossRefGoogle Scholar
  21. Karunasagar I, Pai R, Malathi GR (1994) Mass mortality of Penaeus monodon larvae due to antibiotic resistant Vibrio harveyi infection. Aquaculture 128:203–209CrossRefGoogle Scholar
  22. Kieser T, Bibb MJ, Chater K (2000) Practical Streptomyces genetics. The John Innes Foundation, NorwichGoogle Scholar
  23. Kishimoto S, Nishimura S, Hattori A (2014) Chlorocatechelins A and B from Streptomyces sp.: new siderophores containing chlorinated catecholate groups and an acylguanidine structure. Org Lett 16:6108–6111CrossRefGoogle Scholar
  24. Lafferty KD, Harvell CD, Conrad JM (2015) Infectious diseases affect marine fisheries and aquaculture economics. Ann Rev Marine Sci 7:471–496CrossRefGoogle Scholar
  25. Lane DJ (1991) 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. Wiley, Chichester, pp 115–175Google Scholar
  26. Latha S, Vinothini G, John Dickson Calvin D (2016) In vitro probiotic profile based selection of indigenous actinobacterial probiont Streptomyces sp. JD9 for enhanced broiler production. J Biosci Bioeng 121:124–131CrossRefGoogle Scholar
  27. Margalith P, Beretta G (1960) Rifomycin. XI. taxonomic study on Streptomyces mediterranei nov. sp. Mycopathologia et mycologia applicata 13:321–330CrossRefGoogle Scholar
  28. Marshall BM, Levy SB (2011) Food animals and antimicrobials: impacts on human health. Clin Microbiol Rev 24:718–733CrossRefGoogle Scholar
  29. McCafferty DG, Cudic P, Yu MK (1999) Synergy and duality in peptide antibiotic mechanisms. Curr Opin Chem Biol 3:672–680CrossRefGoogle Scholar
  30. Mohapatra S, Chakraborty T, Kumar V (2013) Aquaculture and stress management: a review of probiotic intervention. J Anim Physiol Anim Nutr (Berl) 97:405–430CrossRefGoogle Scholar
  31. Panda SH, Goli JK, Das S (2017) Production, optimization and probiotic characterization of potential lactic acid bacteria producing siderophores. AIMS Microbiol 3:88–107CrossRefGoogle Scholar
  32. Payne SM (1994) Detection, isolation, and characterization of siderophores. Methods Enzymol 235:329–344CrossRefGoogle Scholar
  33. Pereira AM, Silva LJ, Meisel LM (2015) Fluoroquinolones and tetracycline antibiotics in a portuguese aquaculture system and aquatic surroundings: occurrence and environmental impact. J Toxicol Environ Health A 78:959–975CrossRefGoogle Scholar
  34. Pfeffer C, Oliver JD (2003) A comparison of thiosulphate-citrate-bile salts-sucrose (TCBS) agar and thiosulphate–chloride–iodide (TCI) agar for the isolation of Vibrio species from estuarine environments. Lett Appl Microbiol 36:150–151CrossRefGoogle Scholar
  35. Porse BT, Garrett RA (1999) Sites of interaction of streptogramin A and B antibiotics in the peptidyl transferase loop of 23 S rRNA and the synergism of their inhibitory mechanisms. J Mol Biol 286:375–387CrossRefGoogle Scholar
  36. Saha R, Saha N, Donofrio RS (2013) Microbial siderophores: a mini review. J Basic Microbiol 53:303–317CrossRefGoogle Scholar
  37. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425Google Scholar
  38. Schwyn B, Neilands JB (1987) Universal chemical assay for the detection and determination of siderophores. Anal Biochem 160:47–56CrossRefGoogle Scholar
  39. Selvakumar D, Arun K, Suguna S (2010) Bioactive potential of Streptomyces against fish and shellfish pathogens. Iran J Microbiol 2:157–164Google Scholar
  40. Sivaperumal P, Kamala K, Rajaram R (2015) Bioactive DOPA melanin isolated and characterised from a marine actinobacterium Streptomyces sp. MVCS6 from Versova coast. Nat Prod Res 29:2117–2121CrossRefGoogle Scholar
  41. Subramani R, Aalbersberg W (2012) Marine actinomycetes: an ongoing source of novel bioactive metabolites. Microbiol Res 167:571–580CrossRefGoogle Scholar
  42. Takehana Y, Umekita M, Hatano M (2017) Fradiamine A, a new siderophore from the deep-sea actinomycete Streptomyces fradiae MM456M-mF7. J Antibiot (Tokyo) 70:611–615CrossRefGoogle Scholar
  43. Tan LT, Chan KG, Lee LH (2016) Streptomyces bacteria as potential probiotics in aquaculture. Front Microbiol 7:79Google Scholar
  44. Thirumurugan D, Vijayakumar R (2015) Characterization and structure elucidation of antibacterial compound of Streptomyces sp. ECR77 isolated from east coast of India. Curr Microbiol 70:745–755CrossRefGoogle Scholar
  45. Thompson JD, Gibson TJ, Plewniak F (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucl Acids Res 25:4876–4882CrossRefGoogle Scholar
  46. Tinh NT, Dierckens K, Sorgeloos P (2008) A review of the functionality of probiotics in the larviculture food chain. Mar Biotechnol (NY) 10:1–12CrossRefGoogle Scholar
  47. Tomova A, Ivanova L, Buschmann AH (2015) Antimicrobial resistance genes in marine bacteria and human uropathogenic Escherichia coli from a region of intensive aquaculture. Environ Microbiol Rep 7:803–809CrossRefGoogle Scholar
  48. Tuo Y, Yu H, Ai L (2013) Aggregation and adhesion properties of 22 Lactobacillus strains. J Dairy Sci 96:4252–4257CrossRefGoogle Scholar
  49. Yang N, Sun C (2016) The inhibition and resistance mechanisms of actinonin, isolated from marine Streptomyces sp. NHF165, against Vibrio anguillarum. Front Microbiol 7:1467Google Scholar
  50. Yeole RD, Dave BP, Dube HC (2001) Siderophore production by fluorescent pseudomonads colonizing roots of certain crop plants. Indian J Exp Biol 39:464–468Google Scholar
  51. Yoon SH, Ha SM, Kwon S, Lim J, Kim Y, Seo H, Chun J (2017) Introducing EzBioCloud: a taxonomically united database of 16S rRNA gene sequences and whole-genome assemblies. Int J Syst Evol Microbiol 67:1613–1617CrossRefGoogle Scholar
  52. You JL, Cao LX, Liu GF (2005) Isolation and characterization of actinomycetes antagonistic to pathogenic Vibrio spp. from nearshore marine sediments. World J Microbiol Biotechnol 21:679–682CrossRefGoogle Scholar
  53. You J, Xue X, Cao L (2007) Inhibition of Vibrio biofilm formation by a marine actinomycete strain A66. Appl Microbiol Biotechnol 76:1137–1144CrossRefGoogle Scholar

Copyright information

© Japanese Society of Fisheries Science 2019

Authors and Affiliations

  • Mingxia Yang
    • 1
  • Jun Zhang
    • 1
  • Qiting Liang
    • 1
  • Guanxin Pan
    • 1
  • Jiachang Zhao
    • 1
  • Miao Cui
    • 1
  • Xinqing Zhao
    • 2
  • Qizhong Zhang
    • 1
  • Delin Xu
    • 1
    Email author
  1. 1.Department of Ecology, Institute of Hydrobiology, School of Life Science and Technology, Key Laboratory of Eutrophication and Red Tide Prevention of Guangdong Higher Education Institutes, Engineering Research Center of Tropical and Subtropical Aquatic Ecological Engineering, Ministry of EducationJinan UniversityGuangzhouPeople’s Republic of China
  2. 2.State Key Laboratory of Microbial Metabolism and School of Life Science and BiotechnologyShanghai Jiao Tong UniversityShanghaiChina

Personalised recommendations