Advertisement

Antibacterial and antioxidant aryl-enclosed macrocyclic polyketide from intertidal macroalgae associated heterotrophic bacterium Shewanella algae

  • Vinaya Kizhakkepatt Kizhakkekalam
  • Kajal ChakrabortyEmail author
  • Minju Joy
Original Research
  • 19 Downloads

Abstract

Previously unreported aryl-enclosed 12-membered macrocyclic polyketide characterised as 2′-[(8-ethyl-8-methyl-2,5-dioxo-1-oxacyclododecanyl)methoxy]-methyl benzoate, was identified from the organic extract of Shewanella algae, a heterotrophic gamma proteobacterium, isolated from an intertidal marine macroalgae Hypnea valentiae. The titled macrocyclic polyketide displayed potential antibacterial activity (minimum inhibitory concentration 3.75 µg/mL) compared to that exhibited by chloramphenicol (6.25 µg/mL). Potent antioxidant activity of the studied compound was characterised by its greater scavenging effects on 2,2-diphenyl-1-picrylhydrazyl radical and 2,2′-azino-bis-3-ethylbenzothiozoline-6-sulfonic acid (IC50 0.59 and 0.53 mg/mL, respectively) compared with standard, α-tocopherol (IC50 > 0.65 mg/mL). In silico molecular docking studies of the polyketide with the penicillin binding protein active sites encoded in methicillin resistant Staphylococcus aureus core genome displayed lesser binding energy of −10.31 kcal/mol, which could be correlated with its in vitro antibacterial activities. Structure-activity correlation studies demonstrated the direct relationship of electronic and optimum hydrophobic properties of the macrocyclic polyketide with its bioactivities. Therefore, the presently studied aryl-enclosed macrocyclic compound could be utilised as potent antioxidant and antibacterial pharmacophore in the medicinal formulations.

Keywords

Shewanella algae Heterotrophic gamma proteobacterium Hypnea valentiae Macrocyclic polyketide Antibacterial activity Structure-activity correlation studies 

Notes

Acknowledgements

This work was supported by funding under Kerala State Council for Science, Technology and Environment (Grant No. 040/FSHP-LSS/2014/KSCSTE). The authors are thankful to Indian Council of Agricultural Research, New Delhi for providing facilities to carry out the work. The authors thank the Director, Central Marine Fisheries Research Institute and Dean, Faculty of Marine Sciences, Lakeside Campus, Cochin University of Science and Technology for support. Thanks are due to the Head, Marine Biotechnology Division, Central Marine Fisheries Research Institute for facilitating the research activities.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

44_2019_2468_MOESM1_ESM.doc (15.9 mb)
Supplementary Information

References

  1. Barbieri E, Barry K, Child A, Wainwright N (1997) Antimicrobial activity in the microbial community of the accessory nidamental gland and egg cases of Loligo pealei (Cephalopoda: Loliginidae). Biol Bull 193:275–276CrossRefGoogle Scholar
  2. Ben Ali AI, El Bour M, Ktari L, Bolhuis H, Ahmed M, Boudabbous A, Stal LJ (2012) Jania rubens associated bacteria: molecular identification and antimicrobial activity. J Appl Phycol 24:525–534CrossRefGoogle Scholar
  3. Blunt JW, Copp BR, Keyzers RA, Munro MHG, Prinsep MR (2013) Marine natural products. Nat Prod Rep 30:237–323CrossRefGoogle Scholar
  4. Cao F, Yang Q, Shao C-L, Kong C-J, Zheng J-J, Liu Y-F, Wang C-Y (2015) Bioactive 7-oxabicyclic [6.3.0] lactam and 12-membered macrolides from a gorgonian-derived Cladosporium sp. fungus. Mar Drugs 13:4171–4178PubMedCentralCrossRefGoogle Scholar
  5. Chakraborty K, Thilakan B, Kizhakkekalm VK (2017a) Antibacterial aryl-crowned polyketide from Bacillus subtilis associated with seaweed Anthophycus longifolius. J Appl Microbiol 124:108–125CrossRefGoogle Scholar
  6. Chakraborty K, Thilakan B, Raola VK (2014) Polyketide family of novel antibacterial 7-O-methyl-5′-hydroxy-3′-heptenoate-macrolactin from seaweed-associated Bacillus subtilis MTCC 10403. J Agric Food Chem 62:12194–12208CrossRefGoogle Scholar
  7. Chakraborty K, Thilakan B, Raola VK (2017c) Antimicrobial polyketide furanoterpenoids from seaweed-associated heterotrophic bacterium Bacillus subtilis MTCC 10403. Phytochemistry 142:112–125CrossRefGoogle Scholar
  8. Chakraborty K, Thilakan B, Raola VK, Joy M (2017b) Antibacterial polyketides from Bacillus amyloliquefaciens associated with edible red seaweed Laurenciae papillosa. Food Chem 218:427–434CrossRefGoogle Scholar
  9. Chew YL, Lim YY, Omar M, Khoo KS (2008) Antioxidant activity of three edible seaweeds from two areas in South East Asia. LWT-Food Sci Technol 41:1067–1072CrossRefGoogle Scholar
  10. Donadio S, Monciardini P, Sosio M (2007) Polyketide synthases and nonribosomal peptide synthetases: the emerging view from bacterial genomics. Nat Prod Rep 24:1073–1109CrossRefGoogle Scholar
  11. Driggers EM, Hale SP, Lee J, Terrett NK (2008) The exploration of macrocycles for drug discovery an underexploited structural class. Nat Rev Drug Discov 7(7):608–624CrossRefGoogle Scholar
  12. Du YL, Alkhalaf LM, Ryan KS (2015) In vitro reconstitution of indolmycin biosynthesis reveals the molecular basis of oxazolinone assembly. Proc Natl Acad Sci USA 112:2717–2722CrossRefGoogle Scholar
  13. Epel D (2002) Frontiers in squid reproduction: prospecting for new antibiotics. California Sea Grant College Program Research Profiles Report CSG-MP-02- 001, University of California, San DiegoGoogle Scholar
  14. Hau HH, Gralnick JA (2007) Ecology and biotechnology of the genus Shewanella. Annu Rev Microbiol 61:237–258CrossRefGoogle Scholar
  15. Horta A, Pinteus S, Alves C, Fino N, Silva J, Fernandez S, Rodrigues A, Pedrosa R (2014) Antioxidant and antimicrobial potential of the Bifurcaria bifurcata epiphytic bacteria. Mar Drugs 12:1676–1689PubMedCentralCrossRefGoogle Scholar
  16. Hu L, Zhu H, Li L, Huang J, Sun W, Liu J, Li H, Luo Z, Wang J, Xue Y, Zhang Y, Zhang Y (2016) (±)-Japonones A and B, two pairs of new enantiomers with anti-KSHV activities from Hypericum japonicum. Sci Rep 6:27588Google Scholar
  17. Ivanova EP, Sawabe T, Zhukova NV, Gorshkova NM, Nedashkovskaya OI, Hayashi K, Frolova GM, Sergeev AF, Pavel KG, Mikhailov VV, Nicolau DV (2003) Occurrence and diversity of mesophilic Shewanella strains isolated from the North-West Pacific Ocean. Syst Appl Microbiol 26:293–301CrossRefGoogle Scholar
  18. Kanagasabhapathy M, Sasaki H, Nagata S (2008) Phylogenetic identification of epibiotic bacteria possessing antimicrobial activities isolated from red algal species of Japan. World J Microbiol Biotechnol 24:2315–2321CrossRefGoogle Scholar
  19. Karpiński TM (2019) Marine macrolides with antibacterial and/or antifungal activity. Mar Drugs 17:241PubMedCentralCrossRefGoogle Scholar
  20. Kennedy J, Baker P, Piper C, Cotter PD, Walsh M, Mooij MJ, Bourke MB, Rea MC, O’Connor PM, Ross RP, Hill C, O’Gara F, Marchesi JR, Dobson AD (2009) Isolation and analysis of bacteria with antimicrobial activities from the marine sponge Haliclona simulans collected from Irish waters. Mar Biotechnol 11:384–396CrossRefGoogle Scholar
  21. Kizhakkekalam VK, Chakraborty K (2019) Pharmacological properties of marine macroalgae-associated heterotrophic bacteria. Arch Microbiol 201:505–518CrossRefGoogle Scholar
  22. Lang G, Mitova MI, Ellis G, van der Sar S, Phipps RK, Blunt JW, Cummings NJ, Cole AL, Munro MH (2006) Bioactivity profiling using HPLC/microtiter-plate analysis: application to a New Zealand marine alga-derived fungus, Gliocladium sp. J Nat Prod 69:621–624CrossRefGoogle Scholar
  23. Leonardo M, Moser D, Barbieri E, Brantner C, MacGregor BJ, Paster BJ, Stackebrandt E, Nealson KH (1999) Shewanella pealeana sp. nov., a member of the microbial community associated with the accessory nidamental gland of the squid Loligo pealei. Int J Syst Bacteriol 49:1341–1351CrossRefGoogle Scholar
  24. Lipinski C, Hopkins A (2004) Navigating chemical space for biology and medicine. Nature 432:855–861CrossRefGoogle Scholar
  25. MacDonell M, Colwell R (1985) Phylogeny of the Vibrionaceae, and recommendation for two new genera, Listonella and Shewanella. Syst Appl Microbiol 6:171–82CrossRefGoogle Scholar
  26. Marsault E, Peterson ML (2011) Macrocycles are great cycles: applications, opportunities, and challenges of synthetic macrocycles in drug discovery. J Med Chem 54(7):1961–2004CrossRefGoogle Scholar
  27. Nagao T, Adachi K, Sakai M, Nishijima M, Sano H (2001) Novel macrolactins as antibiotic lactones from a marine bacterium. J Antibiot 54:333–339CrossRefGoogle Scholar
  28. National Committee for Clinical Laboratory Standards (2003) Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically. Approved Standard M7-A6. National Committee for Clinical Laboratory Standards, Wayne, PAGoogle Scholar
  29. Penesyan A, Marshall-Jones Z, Holmstrom C, Kjelleberg S, Egan S (2009) Antimicrobial activity observed among cultured marine epiphytic bacteria reflects their potential as a source of new drugs. FEMS Microbiol Ecol 69(1):113–124CrossRefGoogle Scholar
  30. Ridley CE (2008) Hybridization and the evolution of invasiveness in the California wild radish (Raphanus sativus), botany and plant sciences. University of California Riverside, Riverside, CAGoogle Scholar
  31. Scherlach K, Hertweck C (2009) Triggering cryptic natural product biosynthesis in microorganisms. Org Biomol Chem 7:1753–1760CrossRefGoogle Scholar
  32. Shelest E, Heimerl N, Fichtner M, Sasso S (2015) Multimodular type I polyketide synthases in algae evolve by module duplications and displacement of AT domains in trans. BMC Genomics 16:1015PubMedCentralCrossRefGoogle Scholar
  33. Shigemori H, Kasai Y, Komatsu K, Tsuda M, Mikami Y, Kobayashi J (2004) Sporiolides A and B, new cytotoxic twelve-membered macrolides from a marine-derived fungus Cladosporium species. Mar Drugs 2:164–169PubMedCentralCrossRefGoogle Scholar
  34. Takahashi C, Takada T, Yamada T, Minoura K, Uchida K, Matsumura E, Numata A (1994) Halichomycin, a new class of potent cytotoxic macrolide produced by an actinomycete from a marine fish. Tetrahedron Lett 35:5013–5014CrossRefGoogle Scholar
  35. Thilakan B, Chakraborty K, Chakraborty RD (2017) Antimicrobial properties of cultivable bacteria associated with seaweeds in Gulf of Mannar of South East Coast of India. Can J Microbiol 62:668–681CrossRefGoogle Scholar
  36. Thornburg CC, Zabriskie TM, McPhail KL (2010) Deep-sea hydrothermal vents: potential hot spots for natural products discovery? J Nat Prod 73(3):489–499CrossRefGoogle Scholar
  37. Timmermans ML, Paudel YP, Ross AC (2017) Investigating the biosynthesis of natural products from marine proteobacteria: a survey of molecules and strategies. Mar Drugs 15:235Google Scholar
  38. Weber T, Welzel K, Pelzer S, Vente A, Wohlleben W (2003) Exploiting the genetic potential of polyketide producing Streptomycetes. J Biotechnol 106:221–232CrossRefGoogle Scholar
  39. Wiese J, Thiel V, Nagel K, Staufenberger T, Imhoff JF (2009) Diversity of antibiotic active bacteria associated with the brown alga Laminaria saccharina from the Baltic Sea. Mar Biotechnol 11:287–300CrossRefGoogle Scholar
  40. Wojdylo A, Oszmianski J, Czemerys R (2007) Antioxidant activity and phenolic compounds in 32 selected herbs. Food Chem 105:940–949CrossRefGoogle Scholar
  41. Xie LW, Ouyang YC, Zou K, Wang GH, Chen MJ, Sun HM, Dai SK, Li X (2009) Isolation and difference in anti Staphylococcus aureus bioactivity of curvularin derivates from fungus Eupenicillum sp. Appl Biochem Biotechnol 159:284–293CrossRefGoogle Scholar
  42. Xu J, Jiang C-S, Zhang Z-L, Ma W-Q, Guo Y-W (2014) Recent progress regarding the bioactivities, biosynthesis and synthesis of naturally occurring resorcinolic macrolides. Acta Pharmacol Sin 35:316–330PubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Central Marine Fisheries Research InstituteCochinIndia
  2. 2.Faculty of Marine Sciences, Lakeside CampusCochin University of Science and TechnologyCochinIndia

Personalised recommendations