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Applied Microbiology and Biotechnology

, Volume 99, Issue 4, pp 1571–1586 | Cite as

Antimicrobial compounds from seaweeds-associated bacteria and fungi

  • Ravindra Pal SinghEmail author
  • Puja Kumari
  • C. R. K. ReddyEmail author
Mini-Review

Abstract

In recent decade, seaweeds-associated microbial communities have been significantly evaluated for functional and chemical analyses. Such analyses let to conclude that seaweeds-associated microbial communities are highly diverse and rich sources of bioactive compounds of exceptional molecular structure. Extracting bioactive compounds from seaweed-associated microbial communities have been recently increased due to their broad-spectrum antimicrobial activities including antibacterial, antifungal, antiviral, anti-settlement, antiprotozoan, antiparasitic, and antitumor. These allelochemicals not only provide protection to host from other surrounding pelagic microorganisms, but also ensure their association with the host. Antimicrobial compounds from marine sources are promising and priority targets of biotechnological and pharmaceutical applications. This review describes the bioactive metabolites reported from seaweed-associated bacterial and fungal communities and illustrates their bioactivities. Biotechnological application of metagenomic approach for identifying novel bioactive metabolites is also dealt, in view of their future development as a strong tool to discover novel drug targets from seaweed-associated microbial communities.

Keywords

Biotechnological application Seaweed Antibacterial Antifungal Antifouling Bioactive compounds Metagenomics 

Notes

Acknowledgments

CSIR is gratefully acknowledged for awarding the Senior Research Fellowship (SRF) to R.P. Singh and P. Kumari. CSIR-CSMCRI also thanked for facilities and encouragement provided while preparing this manuscript.

References

  1. Abdel-Lateff A, Fisch KM, Wright AD, König GM (2003) A new antioxidant isobenzofuranone derivative from the algicolous marine fungus Epicoccum sp. Planta Med 69:831–834PubMedGoogle Scholar
  2. Armstrong E, Yan L, Boyd KG, Wright PC, Burgess JG (2001) The symbiotic role of marine microbes on living surfaces. Hydrobiologia 461:37–40Google Scholar
  3. Beattie P, Tan K, Bourne RM, Leach D, Rich PR, Ward FB (1994) Cloning and sequencing of four structural genes for the Na(+)-translocating NADH-ubiquinone oxidoreductase of Vibrio alginolyticus. FEBS Lett 356:333–338PubMedGoogle Scholar
  4. Bondoso J, Balague V, Gasol JM, Lage OM (2013) Community composition of the Planctomycetes associated with different macroalgae. FEMS Microbiol Ecol 88:445–456Google Scholar
  5. Brady SF, Clardy J (2000) Long-chain N-acyl amino acid antibiotics isolated from heterologously expressed environmental DNA. J Am Chem Soc 122:12903–12904Google Scholar
  6. Braña AF, Fiedler HP, Nava H, González V, Sarmiento-Vizcaíno A, Molina A, Acuña JL, García LA, Blanco G (2014) Two Streptomyces species producing antibiotic, antitumor, and anti-inflammatory compounds are widespread among intertidal macroalgae and deep-sea coral reef invertebrates from the central cantabrian sea. Microb Ecol. doi: 10.1007/s00248-014-0508-0 Google Scholar
  7. Bruhn JB, Gram L, Belas R (2007) Production of antibacterial compounds and biofilm formation by Roseobacter species are influenced by culture conditions. Appl Environ Microbiol 73:442–450PubMedCentralPubMedGoogle Scholar
  8. Bugni TS, Ireland CM (2004) Marine-derived fungi: a chemically and biologically diverse group of microorganisms. Nat Prod Rep 21:143–163PubMedGoogle Scholar
  9. Burgess JG, Jordan EM, Bregu M, Mearns-Spragg A, Boyd KG (1999) Microbial antagonism: a neglected avenue of natural products research. J Biotechnol 70:27–32PubMedGoogle Scholar
  10. 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 19:197–205PubMedGoogle Scholar
  11. Burke C, Thomas T, Egan S, Kjelleberg S (2007) The use of functional genomics for the identification of a gene cluster encoding for the biosynthesis of an antifungal tambjamine in the marine bacterium Pseudoalteromonas tunicata. Environ Microbiol 9:814–818PubMedGoogle Scholar
  12. Burke C, Steinberg P, Rusch D, Kjelleberg S, Thomas T (2011) Bacterial community assembly based on functional genes rather than species. Proc Natl Acad Sci U S A 108:14288–14293PubMedCentralPubMedGoogle Scholar
  13. Butzin NC, Owen HA, Collins MLP (2010) A new system for heterologous expression of membrane proteins: Rhodospirillum rubrum. Protein Expr Purif 70:88–94PubMedGoogle Scholar
  14. 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. doi: 10.1021/jf504845m PubMedGoogle Scholar
  15. Cho JY, Kim MS (2012) Induction of antifouling diterpene production by Streptomyces cinnabarinus PK209 in co-culture with marine-derived Alteromonas sp. KNS-16. Biosci Biotechnol Biochem 76:1849–1854Google Scholar
  16. Chow J, Kovacic F, Dall Antonia Y, Krauss U, Fersini F, Schmeisser C, Lauinger B, Bongen P, Pietruszka J, Schmidt M, Menyes I, Bornscheuer UT, Eckstein M, Thum O, Liese A, Mueller-Dieckmann J, Jaeger KE, Streit WR (2012) The metagenome-derived enzymes LipS and LipT increase the diversity of known lipases. PLoS One 7:e47665PubMedCentralPubMedGoogle Scholar
  17. Clardy J, Fischbach MA, Walsh CT (2006) New antibiotics from bacterial natural products. Nat Biotechnol 24:1541–1550PubMedGoogle Scholar
  18. Cui CM, Li XM, Li HF, Gao SS, Wang BG (2009) Benzodiazepine alkaloids from marine-derived endophytic fungus Aspergillus ochraceus. Helv Chim Acta 92:1366–1370Google Scholar
  19. Cui CM, Li XM, Meng L, Li CS, Huang CG, Wang BG (2010) 7-Nor-ergosterolide; a pentalactone- containing norsteroid and related steroids from the marine- derived endophytic Aspergillus ochraceus EN-31. J Nat Prod 73:1780–1784PubMedGoogle Scholar
  20. Dai J, Krohn K, Flörke U, Pescitelli G, Kerti G, Papp T, Kövér KE, Bényei AC, Draeger S, Schulz B, Kurtán T (2011) Curvularin-type metabolites from the fungus Curvularia sp. isolated from a marine alga. Eur J Org Chem 36:6928–6937Google Scholar
  21. Debnath M, Paul AK, Bisen PS (2007) Natural bioactive compounds and biotechnological potential of marine bacteria. Curr Pharm Biotechnol 8:253–260PubMedGoogle Scholar
  22. Dobretsov SV, Qian PY (2002) Effect of bacteria associated with the green alga Ulva reticulata on marine micro- and macrofouling. Biofouling 18:217–228Google Scholar
  23. Egan S, James S, Holmstrom C, Kjelleberg S (2001) Inhibition of algal spore germination by the marine bacterium Pseudoalteromonas tunicata. FEMS Microbiol Ecol 35:67–73PubMedGoogle Scholar
  24. Egan S, James S, Holmstrom C, Kjelleberg S (2002) Correlation between pigmentation and antifouling compounds produced by Pseudoalteromonas tunicata. Environ Microbiol 4:433–442PubMedGoogle Scholar
  25. Egan S, Thomas T, Kjelleberg S (2008) Unlocking the diversity and biotechnological potential of marine surface associated microbial communities. Curr Opin Microbiol 11:219–225PubMedGoogle Scholar
  26. Ekkers DM, Cretoiu MS, Kielak AM, Elsas JD (2012) The great screen anomaly—a new frontier in product discovery through functional metagenomics. Appl Microbiol Biotechnol 93:1005–1020PubMedCentralPubMedGoogle Scholar
  27. Elsebai MF, Kehraus S, Lindequist U, Sasse F, Shaaban S, Gütschow M, Josten M, Sahl HG, König GM (2010) Antimicrobial phenalenone derivatives from the marine-derived fungus Coniothyrium cereal. Org Biomol Chem 9:802–808PubMedGoogle Scholar
  28. Engel S, Jensen PR, Fenical W (2002) Chemical ecology of marine microbial defense. J Chem Ecol 28:1971–1985PubMedGoogle Scholar
  29. Fenical W (1993) Chemical studies of marine bacteria: developing a new resource. Chem Rev 93:1673–1683Google Scholar
  30. Fenical W, Jensen PR (1991) Marine Biotechnology. Plenum Press, New YorkGoogle Scholar
  31. Ferreira CV, Bos CL, Versteeg HH, Justo GZ, Duran N, Peppelenbosch MP (2004) Molecular mechanism of violacein-mediated human leukemia cell death. Blood 104:1459–1464PubMedGoogle Scholar
  32. Flewelling AJ, Johnson JA, Gray CA (2013) Isolation and bioassay screening of fungal endophytes from North Atlantic marine macroalgae. Bot Mar 56:287–297Google Scholar
  33. Foerstner KU, Doerks T, Creevey CJ, Doerks A, Bork PA (2008) Computational screen for type I polyketide synthases in metagenomics shotgun data. PLoS One 3:e3515PubMedCentralPubMedGoogle Scholar
  34. Franks A, Haywood P, Holmstrom C, Egan S, Kjelleberg S, Kumar N (2005) Isolation and structure elucidation of a novel yellow pigment from the marine bacterium Pseudoalteromonas tunicata. Molecules 10:1286–1291PubMedGoogle Scholar
  35. Franks A, Egan S, Holmström C, James S, Lappin-Scott H, Kjelleberg S (2006) Inhibition of fungal colonization by Pseudoalteromonas tunicata provides a competitive advantage during surface colonization. Appl Environ Microbiol 72:6079–6087PubMedCentralPubMedGoogle Scholar
  36. Fudou R, Iizuka T, Yamanaka S (2001) Haliangicin, a novel antifungal metabolite produced by a marine Myxobacterium 1. Fermentation and biological characteristics. J Antibiot 54:149–152PubMedGoogle Scholar
  37. Furbino LE, Godinho VM, Santiago IF, Pellizari FM, Alves TMA, Zani CL, Junior PAS, Romanha AJ, Carvalho AJO, Gil LHVG, Rosa CA, Minnis AM, Rosa LH (2014) Diversity patterns; ecology and biological activities of fungal communities associated with the endemic macroalgae across the Antarctic peninsula. Microb Ecol 67:775–787PubMedGoogle Scholar
  38. Gamal-Eldeen AM, Abdel-Lateff A, Okino T (2009) Modulation of carcinogen metabolizing enzymes by chromanone A; a new chromone derivative from algicolous marine fungus Penicillium sp. Environ Toxicol Phar 28:317–322Google Scholar
  39. Gandhi NM, Nazareth J, Divekar PV, Kohl H, Desouza NJ (1973) Magnesidin, a novel magnesium-containing antibiotic. J Antibiot 26:799–801Google Scholar
  40. Gao SS, Li XM, Du FY, Li CS, Proksch P, Wang BG (2011a) Secondary metabolites from a marine-derived endophytic fungus Penicillium chrysogenum QEN- 24S. Mar Drugs 9:59–70PubMedCentralGoogle Scholar
  41. Gao SS, Li XM, Du FY, Li CS, Proksch P, Wang BG (2011b) Penicisteroids A and B; antifungal and cytotoxic polyoxygenated steroids from the marine alga-derived endophytic fungus Penicillium chrysogenum QEN- 24S. Bioorg Med Chem Lett 21:2894–2897PubMedGoogle Scholar
  42. Gao SS, Li XM, Du FY, Li CS, Proksch P, Wang BG (2011c) Conidiogenones H and I; two new diterpenes of cyclopiane class from a marine-derived endophytic fungus Penicillium chrysogenum QEN-24S. Chem Biodivers 8:1748–1753PubMedGoogle Scholar
  43. Gauthier MJ (1976) Morphological, physiological, and biochemical characteristics of some violet-pigmented bacteria isolated from seawater. Can J Microbiol 22:138–149PubMedGoogle Scholar
  44. Gauthier MJ (1979) Alteromonas rubra sp. nov a new marine antibiotic-producing bacterium. Int J Syst Bacteriol 26:459–466Google Scholar
  45. Gauthier MJ, Breittmayer VA (1979) A new antibiotic-producing bacterium from seawater: Alteromonas aurantia sp.nov. Int J Syst Bacteriol 29:366–372Google Scholar
  46. Gerard J, Lloyd R, Barsby T, Haden P, Kelly MT, Andersen RJ (1997) Antimycobacterial cyclic depsipeptides produced by two pseudomonads isolated from marine habitats. J Nat Prod 60:223–229PubMedGoogle Scholar
  47. Gillespie DE, Brady SF, Bettermann AD, Cianciotto NP, Liles MR, Rondon MR, Clardy J, Goodman RM, Handelsman J (2002) Isolation of antibiotics turbomycin A and B from a metagenomic library of soil microbial DNA. Appl Environ Microbiol 68:4301–4306PubMedCentralPubMedGoogle Scholar
  48. Godinho VM, Furbino LE, Santiago IF, Pellizzari FM, Yokoya NS, Pupo D, Alves TM, Junior PA, Romanha AJ, Zani CL, Cantrell CL, Rosa CA, Rosa LH (2013) Diversity and bioprospecting of fungal communities associated with endemic and cold-adapted macroalgae in Antarctica. ISME J 7:1434–1451PubMedCentralPubMedGoogle Scholar
  49. Goecke F, Labes A, Wiese J, Imhoff JF (2010) Chemical interactions between marine macroalgae and bacteria. Mar Ecol Prog Ser 409:267–300Google Scholar
  50. Goecke F, Thiel V, Wiese J, Labes A, Imhoff JF (2013) Algae as an important environment for bacteria—Phylogenetic relationships among new bacterial species isolated from algae. Phycologia 52:14–24Google Scholar
  51. Goto T, Takahashi S, Kishi Y, Hirata Y (1965) Tetrodotoxin. Tetrahedron 21:2059–2088PubMedGoogle Scholar
  52. Gulder TAM, Moore BS (2009) Chasing the treasures of the sea—Bacterial marine natural products. Curr Opin Microbiol 12:252–260PubMedCentralPubMedGoogle Scholar
  53. Handelsman J (2004) Metagenomics: Application of genomics to uncultured microorganisms. Microbiol Mol Biol Rev 68:669–685Google Scholar
  54. Harder T (2009) Marine epibiosis: Concepts, ecological consequences and host defence. In: Costerton JW (ed) Marine and Industrial Biofouling. Springer, Berlin, pp 219–231Google Scholar
  55. Hayashi M, Hirai K, Unemoto T (1994) Cloning of the Na(+)-translocating NADH-quinone reductase gene from the marine bacterium Vibrio alginolyticus and the expression of the beta-subunit in Escherichia coli. FEBS Lett 356:330–332PubMedGoogle Scholar
  56. Hayashi M, Hirai K, Unemoto T (1995) Sequencing and the alignment of structural genes in the nqr operon encoding the Na+-translocating NADH-quinone reductase from Vibrio alginolyticus. FEBS Lett 363:75–77Google Scholar
  57. Hayashi M, Shibata N, Nakayama Y, Yoshikawa K, Unemoto T (2002) Korormicin insensitivity in Vibrio alginolyticus is correlated with a single point mutation of Gly-140 in the NqrB subunit of the Na(+)-translocating NADH-quinone reductase. Arch Biochem Biophys 401:173–177PubMedGoogle Scholar
  58. Hollants J, Leliaert F, Verbruggen H, Willems A, De-Clerck O (2013) Permanent residents or temporary lodgers: characterizing intracellular bacterial communities in the siphonous green alga Bryopsis Proc R Soc Lond B 20122659Google Scholar
  59. Holmstrom C, Kjelleberg S (1999) Marine Pseudoalteromonas species are associated with higher organisms and produce active extracellular agents. FEMS Microbiol Ecol 30:285–293Google Scholar
  60. Holmström C, Egan S, Franks A, McCloy S, Kjelleberg S (2002) Antifouling activities expressed by marine surface associated Pseudoalteromonas species. FEMS Microbiol Ecol 41:47–58PubMedGoogle Scholar
  61. Imamura N, Nishijima M, Takadera T, Adachi K (1997) New anticancer antibiotics pelagiomicins, produced by a new marine bacterium Pelagiobacter variabilis. J Antibiot 50:8–12PubMedGoogle Scholar
  62. Ismail-Ben Ali A, El Bour M, Ktari L, Bolhuis H, Ahmed M, Boudabous A, Stal LJ (2012) Jania rubens-associated bacteria: Molecular identification and antimicrobial activity. J Appl Phycol 24:525–534Google Scholar
  63. Isnansetyo A, Horikawa M, Kamei Y (2001) In vitro antimethicillin- resistant Staphylococcus aureus activity of 2,4- diacetylphloroglucinol produced by Pseudomonas sp. AMSN isolated from a marine alga. J Antimicrob Chemother 47:719–730Google Scholar
  64. Izumikawa M, Hashimoto J, Takagi M, Shin-ya K (2010) Isolation of two new terpeptin analogs—JBIR-81 and JBIR-82 from a seaweed-derived fungus, Aspergillus sp. SpD081030G1f1. J Antibiot 63:389–391PubMedGoogle Scholar
  65. Jamal MT, Morris PC, Hansen R, Jamieson DJ, Burgess JG, Austin B (2006) Recovery and characterization of a 30.7- kDa protein from Bacillus licheniformis associated with inhibitory activity against methicillin-resistant Staphylococcus aureus, vancomycin-resistant Enterococci, and Listeria monocytogenes. Mar Biotechnol 8:587–592PubMedGoogle Scholar
  66. JanakiDevi V, YokeshBabuM, Umarani R, Kumarguru A (2013) Antagonistic activity of seaweed associated bacteria against human pathogens. Int J Cur Micobiol App Sci 2:140–147Google Scholar
  67. Jaruchoktaweechai C, Suwanboriux K, Tanasupawatt S, Kittakoop P, Menasveta P (2000) New macrolactins from a marine Bacillus sp. ScO26. J Nat Prod 63:984–986Google Scholar
  68. Jiang Z, Mearns-Spragg A, Adams DR, Wright PC, Burgess JG (2001) Two diketopiperazines and one halogenated phenol from cultures of the marine bacterium, Pseudoalteromonas luteoviolacea. Nat Prod Lett 14:435–440Google Scholar
  69. Kamei Y, Isnansetyo A (2003) Lysis of methicillin-resistant Staphylococcus aureus by 2, 4-diacetylphloroglucinol produced by Pseudomonas sp. AMSN isolated from a marine alga. Int J Antimicrob Agents 21:71–74Google Scholar
  70. Kanagasabhapathy M, Sazaki H, Haldar S, Yamasaki S, Ngata S (2006) Antibacterial activities of marine epibiotic bacteria isolated from brown algae. Ann Microb 56:167–173Google Scholar
  71. 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 24:2315–2321Google Scholar
  72. Kanagasabhapathy M, Yamazaki G, Ishida A, Sasaki H, Nagata S (2009) Presence of quorum-sensing inhibitor-like compounds from bacteria isolated from the brown alga Colpomenia sinuosa. Lett Appl Microbiol 49:573–579Google Scholar
  73. Kanoh K, Kohno S, Asari T, Harada T, Katada J, Muramatsu M, Kawashima H, Sekiya H, Uno I (1997) (−)-phenylahistin: a new mammalian cell cycle inhibitor produced by Aspergillus ustus. Bioorg Med Chem Lett 7:2847–2852Google Scholar
  74. Kanoh K, Kohno S, Katada J, Hayash Y, Muramatsu M, Uno I (1999) Antitumor activity of phenylahistin in vitro and in vivo. Bios Biotechol Biochem 63:1130–1133Google Scholar
  75. Kim H, Kim W, Ryoo I, Kim C, Suk J, Han K, Hwang S, Yoo I (1997) Neuronal cell protection activity of macrolactin A produced by Actinomadura sp. J Microbiol Biotechnol 7:429–434Google Scholar
  76. Kimelman A, Levy A, Sberro H, Kidron S, Leavitt A, Amitai G, Yoder-Himes DR, Wurtzel O, Zhu Y, Rubin EM, Sorek R (2012) A vast collection of microbial genes that are toxic to bacteria. Genome Res 22:802–809PubMedCentralPubMedGoogle Scholar
  77. Kodach LL, Bos CL, Durán N, Peppelenbosch MP, Ferreira CV, Hardwick JC (2006) Violacein synergistically increases 5-fluorouracil cytotoxicity, induces apoptosis and inhibits Akt-mediated signal transduction in human colorectal cancer cells. Carcinogenesis 27:508–516PubMedGoogle Scholar
  78. Krohn-Molt I, Wemheuer B, Alawi M, Poehlein A, Güllert S, Schmeisser C, Pommerening-Röser A, Grundhoff A, Daniel R, Hanelt D, Streit WR (2013) Metagenome survey of a multispecies and alga-associated biofilm revealed key elements of bacterial-algal interactions in photobioreactors. Appl Environ Microbiol 79:6196–6206PubMedCentralPubMedGoogle Scholar
  79. Kumar V, Rao D, Thomas T, Kjelleberg S, Egan S (2011) Antidiatom and antibacterial activity of epiphytic bacteria isolated from Ulva lactuca in tropical waters. World J Microbiol Biotechnol 27:1543–1549Google Scholar
  80. Lachnit T, Blümel M, Imhoff JF, Wahl M (2009) Specific epibacterial communities on macroalgae: Phylogeny matters more than habitat. Aquat Biol 5:181–186Google Scholar
  81. Lachnit T, Meske D, Wahl M, Harder T, Schmitz R (2011) Epibacterial community patterns on marine macroalgae are host-specific but temporally variable. Environ Microbiol 13:655–665PubMedGoogle Scholar
  82. Lafi FF, Garson MJ, Fuerst JA (2005) Culturable bacterial symbionts isolated from two distinct sponge species (Pseudoceratina clavata and Rhabdastrella globostellata) from the Great Barrier Reef display similar phylogenetic diversity. Microb Ecol 50:213–220PubMedGoogle Scholar
  83. Lane AL, Kubanek J (2008) Secondary metabolite defenses against pathogens and biofoulers. In: Amsler CH (ed) Algal chemical ecology. Springer, Berlin, pp 229–243Google Scholar
  84. Lee CH, Ruben PC (2008) Interaction between voltage-gated sodium channels and the neurotoxin, tetrodotoxin. Channels (Austin) 2:407–412Google Scholar
  85. Lee YM, Kim MJ, Li H, Zhang P, Bao B, Lee KJ, Jung JH (2013) Marine-derived Aspergillus species as a source of bioactive secondary metabolites. Mar Biotechnol 15:499–519PubMedGoogle Scholar
  86. Lemos ML, Toranzo AE, Barja JL (1985) Antibiotic activity of epiphytic bacteria isolated from Inter-tidal seaweeds. Microbiol Ecol 11:149–163Google Scholar
  87. Li S, Norioka S, Sakiyama F (1998) Bacteriolytic activity and specificity of Achromobacter beta-lytic protease. J Biochem 124:332–339PubMedGoogle Scholar
  88. Li Y, Li X, Son BW (2005) Antibacterial and radical scavenging epoxycyclohexenones and aromatic polyols from a marine isolate of the fungus Aspergillus. Nat Prod Sci 11:136–138Google Scholar
  89. Longford SR, Tujula NA, Crocetti G, Holmes AJ, Holmström C, Kjelleberg S, Steinberg PD, Taylor MW (2007) Comparisons of diversity of bacterial communities associated with three sessile marine eukaryotes. Aquat Microb Ecol 48:217–229Google Scholar
  90. Loque CP, Medeiros AO, Pellizzari FM, Oliveira EC, Rosa CA, Rosa LH (2010) Fungal community associated with marine macroalgae from Antarctica. Polar Biol 33:641–648Google Scholar
  91. Lu XL, QZh X, Shen YH, Liu XY, Jiao BH, Zhang WD, Ni KY (2008) Macrolactin S, a novel macrolactin antibiotic from marine Bacillus sp. Nat Prod Res 22:342–347PubMedGoogle Scholar
  92. Ma Y, Liu P, Yu S, Li D, Cao S (2009) Inhibition of common fouling organisms in mariculture by epiphytic bacteria from the surfaces of seaweeds and invertebrates. Acta Ecol Sin 29:222–226Google Scholar
  93. Marshall K, Joint I, Callow ME, Callow JA (2006) Effect of marine bacterial isolates on the growth and morphology of axenic plantlets of the green alga Ulva linza. Microb Ecol 52:302–310PubMedGoogle Scholar
  94. Mathan S, Subramanian V, Nagamony S, Ganapathy K (2013) Isolation of endophytic fungi from marine algae and its bioactivity. Int J Res Pharm Sci 4:45–49Google Scholar
  95. Matsuo Y, Suzuli M, Kasai H, Shizuri Y, Harayama S (2003) Isolation and phylogenetic characterization of bacteria capable of inducing differentiation in the green alga Monostroma oxyspermum. Environ Microbiol 5:25–35PubMedGoogle Scholar
  96. Matsuo Y, Imagawa H, Nishizawa M, Shizuri Y (2005) Isolation of an algal morphogenesis inducer from a marine bacterium. Science 307:1598PubMedGoogle Scholar
  97. Matz C, Webb JS, Schupp PJ, Phang SY, Penesyan A, Egan S, Steinberg P, Kjelleberg S (2008) Marine biofilm bacteria evade eukaryotic predation by targeted chemical defense. PLoS One 3:e2744PubMedCentralPubMedGoogle Scholar
  98. Miao FP, Li XD, Liu XH, Cichewicz RH, Ji NY (2012) Secondary metabolites from an algicolous Aspergillus versicolor strain. Mar Drugs 10:131–139PubMedCentralPubMedGoogle Scholar
  99. Molinski TF, Dalisay DS, Lievens SL, Saludes JP (2009) Drug development from marine natural products. Nat Rev Drug Discov 8:69–85PubMedGoogle Scholar
  100. Mondol MA, Kim JH, Lee HS, Lee YJ, Shin HJ (2011) Macrolactin W, a new antibacterial macrolide from a marine Bacillus sp. Bioorg Med Chem Lett 21:3832–3835PubMedGoogle Scholar
  101. Murakami A, Miyashita H, Iseki M, Adachi K, Mimuro M (2004) Chlorophyll d in an epiphytic cyanobacterium of red algae. Science 303:1633PubMedGoogle Scholar
  102. Myobatake Y, Takeuchi T, Kuramochi K, Kuriyama I, Ishido T, Hirano K, Sugawara F, Yoshida H, Mizushina Y (2012) Pinophilins A and B, inhibitors of mammalian A-, B-, and Y-family DNA polymerases and human cancer cell proliferation. J Nat Prod 75:135–141PubMedGoogle Scholar
  103. Naganuma M, Nishida M, Kuramochi K, Sugawara F, Yoshida H, Mizushina Y (2008) 1-Deoxyrubralactone, a novel specific inhibitor of families X and Y of eukaryotic DNA polymerases from a fungal strain derived from sea algae. Bioorg Med Chem 16:2939–2944PubMedGoogle Scholar
  104. Nagao T, Adachi K, Sakai M, Nishijima M, Sano H (2001) Novel macrolactins as antibiotic lactones from a marine bacterium. J Antibiot 54:333–339PubMedGoogle Scholar
  105. Nakanishi K, Nishijima M, Nomoto AM, Yamazaki A, Saga N (1999) Requisite morphologic interaction for attachment between Ulva pertusa (Chlorophyta) and symbiotic bacteria. Mar Biotechnol 1:107–111PubMedGoogle Scholar
  106. Nakayama Y, Hayashi M, Yoshikawa K, Mochida K, Unemoto T (1999) Inhibitor studies of a new antibiotic, korormicin, 2-n-heptyl-4-hydroxyquinoline N-oxide and Ag + toward the Na+-translocating NADH-quinone reductase from the marine Vibrio alginolyticus. Biol Pharm Bull 22:1064–1067Google Scholar
  107. Ogawa A, Murakami C, Kamisuki S, Kuriyama I, Yoshida H, Sugawara F, Mizushina Y (2004) Pseudodeflectusin; a novel isochroman derivative from Aspergillus pseudodeflectus a parasite of the seaweed; Sargassum fusiform; as a selective human cancer cytotoxin. Bioorg Med Chem Lett 14:3539–3543PubMedGoogle Scholar
  108. Oliveira ALL, de Felício R, Debonsi HM (2012) Marine natural products: Chemical and biological potential of seaweeds and their endophytic fungi. Brazil J Pharmacogn 22:906–920Google Scholar
  109. Osterhage C, Kaminsky R, König GM, Wright AD (2000) Ascosalipyrrolidinone A, an antimicrobial alkaloid, from the obligate marine fungus Ascochyta salicorniae. J Org Chem 5:6412–6417Google Scholar
  110. Osterhage C, König GM, Höller U, Wright AD (2002) Rare sesquiterpenes from the algicolous fungus Drechslera dematioidea. J Nat Prod 65:306–313PubMedGoogle Scholar
  111. 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 69:113–124PubMedGoogle Scholar
  112. Penesyan A, Kjelleberg S, Egan S (2010) Development of novel drugs from marine surface associated microorganisms. Mar Drugs 8:438–459PubMedCentralPubMedGoogle Scholar
  113. Penesyan A, Tebben J, Lee M, Thomas T, Kjelleberg S, Harder T, Egan S (2011) Identification of the antibacterial compound produced by the marine epiphytic bacterium Pseudovibrio sp. D323 and related sponge-associated bacteria. Mar Drugs 9:1391–1402PubMedCentralPubMedGoogle Scholar
  114. Penesyan A, Ballestriero F, Daim M, Kjelleberg S, Thomas T, Egan S (2013a) Assessing the effectiveness of functional genetic screens for the identification of bioactive metabolites. Mar Drugs 11:40–49PubMedCentralGoogle Scholar
  115. Penesyan A, Breider S, Schumann P, Tindall BJ, Egan S, Brinkhoff T (2013b) Epibacterium ulvae gen. nov sp. nov epibiotic bacteria isolated from the surface of a marine alga. Int J Syst Evol Microbiol 63:1589–1596PubMedGoogle Scholar
  116. Pontius A, Mohamed I, Krick A, Kehraus S, König GM (2008a) Aromatic polyketides from marine algicolous fungi. J Nat Prod 71:272–274PubMedGoogle Scholar
  117. Pontius A, Krick A, Kehraus S, Foegen SE, Müller M, Klimo K, Gerhäuser C, König GM (2008b) Noduliprevenone: a novel heterodimeric chromanone with cancer chemopreventive potential. Chem Eur J 14:9860–9863PubMedGoogle Scholar
  118. Pontius A, Krick A, Mesry R, Kehraus S, Foegen SE, Müller M, Klimo K, Gerhäuser C, König GM (2008c) Monodictyochromes A and B, dimeric xanthone derivatives from the marine algicolous fungus Monodictys putredinis. J Nat Prod 71:1793–1799Google Scholar
  119. Prieto ML, O’Sullivan L, Tan SP, McLoughlin P, Hughes H, O’Connor PM, Cotter PD, Lawlor PG, Gardiner GE (2012) Assessment of the bacteriocinogenic potential of marine bacteria reveals lichenicidin production by seaweed-derived Bacillus spp. Mar Drugs 10:2280–2299PubMedGoogle Scholar
  120. Qiao MF, Ji NY, Liu XH, Li K, Zhu QM, Xue QZ (2010) Indoloditerpenes from an algicolous isolate of Aspergillus oryzae. Bioorg Med Chem Lett 20:5677–5680PubMedGoogle Scholar
  121. Rao D, Webb JS, Holmström C, Case R, Low A, Steinberg P, Kjelleberg S (2007) Low densities of epiphytic bacteria from the marine alga Ulva australis inhibits settlement of fouling organisms. Appl Environ Microbiol 73:7844–7852PubMedCentralPubMedGoogle Scholar
  122. Rastogi G, Sani R (2011) Molecular techniques to assess microbial community structure, function, and dynamics in the environment. In: Ahmad I, Ahmad F, Pichtel J (eds) Microbes and Microbial Technology. Springer, New York, pp 29–57Google Scholar
  123. Ravisankar A, Gnanambal MEK, Sundaram LR (2013) A Newly Isolated Pseudomonas sp. epibiotic on the seaweed, Padina tetrastromatica, off southeastern coast of India, reveals antibacterial action. Appl Biochem Biotechnol 171:1968–1985PubMedGoogle Scholar
  124. Reverchon S, Rouanet C, Expert D, Nasser W (2002) Characterization of indigoidine biosynthetic genes in Erwinia chrysanthemi and role of this blue pigment in pathogenicity. J Bacteriol 184:654–665PubMedCentralPubMedGoogle Scholar
  125. Rungprom W, Siwu ERO, Lambert LK, Dechsakulwatana C, Barden MC, Kokpol U (2008) Cyclic tetrapeptides from marine bacteria associated with the seaweed Diginea sp. and the sponge Halisarca ectofibrosa. Tetrahedron 64:3147–3152Google Scholar
  126. Schallmey M, Ly A, Wang C, Meglei G, Voget S, Streit WR, Driscoll BT, Charles TC (2011) Harvesting of novel polyhydroxyalkanaote (PHA) synthase encoding genes from a soil metagenome library using phenotypic screening. FEMS Microbiol Lett 321:150–156PubMedGoogle Scholar
  127. Schulz B, Draeger S, Del Cruz TE, Rheinheimer J, Siems K, Loesgen S, Bitzer J, Schloerke O, Zeek A, Kock I, Hussain H, Dai J, Krohn K (2008) Screening strategies for obtaining novel; biologically active; fungal secondary metabolites from marine habitats. Bot Mar 51:219–234Google Scholar
  128. Silva-Aciares F, Riquelme C (2008) Inhibition of attachment of some fouling diatoms and settlement of Ulva lactuca zoospores by film-forming bacterium and their extracellular products isolated from biofouled substrata in Northern Chile. Elect J Biotechnol 11:60–70Google Scholar
  129. Simu K, Hagstrom A (2004) Oligotrophic bacterioplankton with a novel single-cell life strategy. Appl Environ Microbiol 70:2445–2451PubMedCentralPubMedGoogle Scholar
  130. Singh RP, Reddy CRK (2014) Seaweed–microbial interactions: Key functions of seaweed-associated bacteria. FEMS Microbiol Ecol 88:213–230PubMedGoogle Scholar
  131. Singh RP, Bijo AJ, Baghel RS, Reddy CRK, Jha B (2011a) Role of bacterial isolates in enhancing the bud induction in the industrially important red alga Gracilaria dura. FEMS Microbiol Ecol 76:381–392PubMedGoogle Scholar
  132. Singh RP, Mantri VA, Reddy CRK, Jha B (2011b) Isolation of seaweed-associated bacteria and their morphogenesis inducing capability in axenic cultures of the green alga Ulva fasciata. Aquat Biol 12:13–21Google Scholar
  133. Streit WR, Daniel R, Jaeger KE (2004) Prospecting for biocatalysts and drugs in the genomes of non-cultured microorganisms. Curr Opin Biotechnol 15:285–290PubMedGoogle Scholar
  134. Subramaniam S, Ravi V, Sivasubramanian A (2014) Synergistic antimicrobial profiling of violacein with commercial antibiotics against pathogenic microorganisms. Pharm Biol 52:86–90PubMedGoogle Scholar
  135. Suja M, Vasuki S, Sajitha N (2014) Anticancer activities of compounds isolated from marine endophytic fungus Aspergillus terreus. World J Pharm Pharm Sci 3(6):661–672Google Scholar
  136. Suresh M, Iyapparaj P, Anantharaman P (2014) Optimization, characterization and partial purification of bacteriocin produced by Staphylococcus haemolyticus MSM an isolate from seaweed. Biocatal Agric Biotechnol. doi: 10.1016/j.bcab.2014.08.005 Google Scholar
  137. Suryanarayanan TS (2012) Fungal Endosymbionts of Seaweeds. In: Raghu Kumar C (ed) Biology of marine fungi; progress in molecular and subcellular biology. Springer, Berlin, pp 53–69Google Scholar
  138. Suryanarayanan TS, Venkatachalam A, Thirunavukkarasu N, Ravishankar JP, Doble M, Geetha V (2010) Internal mycobiota of marine macroalgae from the Tamilnadu coast: distribution; diversity and biotechnological potential. Bot Mar 53:457–468Google Scholar
  139. Suryanarayanan TS, Thirunavukkarasu N, Govindarajulu MB, Gopalan V (2012) Fungal endophytes: an untapped source of biocatalysts. Fungal Divers 54:19–30Google Scholar
  140. Suvega T, Kumar KA (2014) Antimicrobial activity of bacteria associated with seaweeds against plant pathogens on par with bacteria found in seawater and sediments. British Microbiol Res J 4(841–85):2014Google Scholar
  141. Tait K, Williamson H, Atkinson S, Williams P, Camara M, Joint I (2009) Turnover of quorum sensing signal molecules modulate cross-kingdom signalling. Environ Microbiol 11:1792–1802PubMedGoogle Scholar
  142. Takahashi H, Kumagai T, Kitani K, Mori M, Matoba Y, Sugiyama M (2007) Cloning and characterization of a Streptomyces single module type non-ribosomal peptide synthetase catalyzing a blue pigment synthesis. J Biol Chem 12:9073–9081Google Scholar
  143. Tebben J, Tapiolas DM, Motti CA, Abrego D, Negri AP, Blackall LL, Steinberg PD, Harder T (2011) Induction of larval metamorphosis of the coral Acropora millepora by tetrabromopyrrole isolated from a Pseudoalteromonas bacterium. PLoS One 6:e19082PubMedCentralPubMedGoogle Scholar
  144. Tebben J, Motti C, Tapiolas D, Thomas-Hall P, Harder T (2014) A coralline algal-associated bacterium, Pseudoalteromonas strain J010, yields five new korormicins and a bromopyrrole. Mar Drugs 12:2802–2815PubMedCentralPubMedGoogle Scholar
  145. Thirunavukkarasu N, Suryanarayanan TS, Murali TS, Ravishankar JP, Gummadi SN (2011) L-asparaginase from marine derived fungal endophytes of seaweeds. Mycosphere 2:147–155Google Scholar
  146. Tran H, Ficke A, Asiimwe T, Höfte M, Raaijmakers JM (2007) Role of the cyclic lipopeptide massetolide A in biological control of Phytophthora infestans and in colonization of tomato plants by Pseudomonas fluorescens. New Phytol 175:731–742PubMedGoogle Scholar
  147. Tsuda K, Ikuma S, Kawamura M, Tachikawa R, Sakai K, Tamura C, Amakasu D (1964) Tetrodotoxin. VII. On the structures of tetrodotoxin and its derivatives. Chem Pharm Bull 12:1357–1374PubMedGoogle Scholar
  148. Tujula NA, Crocetti GR, Burke C, Thomas T, Holmstrom C, Kjelleberg S (2010) Variability and abundance of the epiphytic bacterial community associated with a green marine Ulvacean alga. ISME J 4:301–311PubMedGoogle Scholar
  149. Uchiyama T, Miyazaki K (2009) Functional metagenomics for enzyme discovery: Challenges to efficient screening. Curr Opin Biotechnol 20:616–622PubMedGoogle Scholar
  150. Unemoto T, Hayashi M, Hayashi M (1977) Na+-dependent activation of NADH oxidase in membrane fractions from halophilic Vibrio alginolyticus and V. costicolus. J Biochem 82:1389–1395Google Scholar
  151. Villarreal-Gómez LJ, Soria-Mercado IE, Guerra-Rivas G, Ayala-Sánchez NE (2010) Antibacterial and anticancer activity of seaweeds and bacteria associated with their surface. Revista de Biología Marina y Oceanografía 45:267–275Google Scholar
  152. Wang GY, Graziani E, Waters B, Pan W, Li X, McDermott J, Meurer G, Saxena G, Andersen RJ, Davies J (2000) Novel natural products from soil DNA libraries in a streptomycete host. Org Lett 2:2401–2404PubMedGoogle Scholar
  153. Wang S, Li X, Teuscher F, Li D, Diesel A, Ebel E, Proksch P, Wang B (2006) Chaetopyranin, a benzaldehyde derivative, and other related metabolites from Chaetomium globosum, an endophytic fungus derived from the marine red alga Polysiphonia urceolata. J Nat Prod 69:1622–1625PubMedGoogle Scholar
  154. Ward DM, Weller R, Bateson MM (1990) 16S rRNA sequences reveal numerous uncultured microorganisms in a natural community. Nature 345:63–65PubMedGoogle Scholar
  155. Waters AL, Hill RT, Place AR, Hamann MT (2010) The expanding role of marine microbes in pharmaceutical development. Curr Opin Biotechnol 21:780–786PubMedCentralPubMedGoogle Scholar
  156. Webster NS, Cobb RE, Negri AP (2008) Temperature thresholds for bacterial symbiosis with a sponge. ISME J 2:830–842PubMedGoogle Scholar
  157. White JF Jr, Torres MS (2010) Is plant endophyte-mediated defensive mutualism the result of oxidative stress protection? Physiol Plant 138:440–446PubMedGoogle Scholar
  158. 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 11:287–300PubMedGoogle Scholar
  159. Woodward RB (1964) The structure of tetrodotoxin. Pure Appl Chem 9:49–74Google Scholar
  160. Yasumoto T, Yasumura D, Yotsu M, Michishita T, Endo A, Kotaki Y (1986) Bacterial production of tetrodotoxin and anhydrotetrodotoxin. Agric Biol Chem 50:793–795Google Scholar
  161. Yokoo A (1950) Chemical studies on pufferfish toxin (3)—Separation of spheroidine. Nippon Kagaku Zasshi 71:590–592Google Scholar
  162. Yoshikawa K, Takadera T, Adachi K, Nishijima M, Sano H (1997) Korormicin, a novel antibiotic specifically active against marine Gram-negative bacteria, produced by a marine bacterium. J Antibiot 50:949–953PubMedGoogle Scholar
  163. Yoshikawa K, Nakayama Y, Hayashi M, Unemoto T, Mochida K (1999) Korormicin, an antibiotic specific for gram-negative marine bacteria, strongly inhibits the respiratory chain-linked Na+-translocating NADH: Quinone reductase from the marine Vibrio alginolyticus. J Antibiot 52:182–185PubMedGoogle Scholar
  164. Yoshikawa K, Adachi K, Nishida F, Mochida K (2003) Planar structure and antibacterial activity of korormicin derivatives isolated from Pseudoalteromonas sp. F-420. J Antibiot 56:866–870PubMedGoogle Scholar
  165. Yung PY, Burke C, Lewis M, Kjelleberg S, Thomas T (2011) Novel antibacterial proteins from the microbial communities associated with the sponge Cymbastela concentrica and the green alga Ulva australis. Appl Environ Microbiol 77:1512–1515PubMedCentralPubMedGoogle Scholar
  166. Zhang Y, Li XM, Wang BG (2007) Nigerasperones A ~ C; new monomeric and dimeric naphto-γ-pyrones from a marine alga-derived endophytic fungus Aspergillus niger EN-13. J Antibiot 60:204–210PubMedGoogle Scholar
  167. Zhang Y, Li XM, Feng Y, Wang BG (2010) Phenethyl-α-pyrone derivatives and cyclodipeptides from a marine algous endophytic fungus Aspergillus niger EN-13. Nat Prod Res 24:1036–1043PubMedGoogle Scholar
  168. Zhu TJ, Du L, Hao PF, Lin ZJ, Gu QQ (2009) Citrinal A, a novel tricyclic derivative of citrinin, from an algicolous fungus Penicillium sp. i-1-1. Chin Chem Lett 20:917–920Google Scholar
  169. Zuccaro A, Mitchell JI (2005) Fungal communities of seaweeds. In: Dighton J, White JF Jr, Oudemans P (eds) The fungal community. CRC Press, New York, pp 533–579Google Scholar
  170. Zuccaro A, Schulz B, Mitchell JI (2003) Molecular detection of ascomycetes associated with Fucus serratus. Mycol Res 107:1451–1466PubMedGoogle Scholar
  171. Zuccaro A, Schoch CL, Spatafora JW, Kohlmeyer J, Draeger S, Mitchell JI (2008) Detection and identification of fungi intimately associated with the brown seaweed Fucus serratus. Appl Environ Microbiol 74:931–941PubMedCentralPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  1. 1.Discipline of Marine Biotechnology and EcologyCSIR—Central Salt and Marine Chemicals Research InstituteBhavnagarIndia
  2. 2.Laboratory of Microbial Technology, Department of Bioscience and Biotechnology, Faculty of AgricultureKyushu UniversityFukuokaJapan
  3. 3.Institute of Plant SciencesAgricultural Research Organization (ARO), Volcani CenterBet DaganIsrael
  4. 4.Academy of Scientific and Innovative Research (AcSIR)New DelhiIndia

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