Antifouling Activity of Meroterpenes Isolated from the Ascidian Aplidium aff. densum

Springer Science and Business Media LLC - Tập 23 - Trang 51-61 - 2020
Annabel Levert1,2, Valentin Foulon3, Marilyne Fauchon3, Nathalie Tapissier-Bontemps1,4, Bernard Banaigs1,4, Claire Hellio3
1Université de Perpignan, USR CNRS-EPHE-UPVD 3278, CRIOBE, Perpignan Cedex, France
2AkiNaO SAS, Perpignan, France
3Laboratoire des Sciences de l’Environnement Marin (LEMAR) CNRS, IRD, Ifremer, Univ Brest, Plouzané, France
4Laboratoire d’Excellence CORAIL, Perpignan, France

Tóm tắt

The settlement and growth of fouling organisms on man-made surfaces can be prevented by the application of antifouling paints containing active compounds (biocides, heavy metals), most of which are toxic to non-target organisms. As part of our research program in chemical ecology and blue biotechnology, we are conducting studies to investigate the natural defence mechanisms of marine organisms that are free from epibionts, with the aim of isolating molecules involved in surface defence that could be good candidates as antifouling agents. Ascidians were selected for our investigation because previous studies have shown that they contain abundant and diverse secondary metabolites, which play a defensive role and have been applied to drug discovery. It is therefore relevant to study the role of such secondary metabolites in surface protection. In this study, 5 meroterpenoids (cordiachromene A, didehydroconicol, epiconicol, methoxyconidiol, conidione) from Aplidium aff. densum (ascidian) were investigated as potential antifoulants towards the inhibition of bacterial growth and settlement inhibition of barnacles. Cardiochromene A (IC50 barnacle settlement = 6.04 μg/mL; MIC Gram positive = 125 μg/mL; MIC Gram negative = 32 μg/mL) and epiconicol (IC50 barnacle settlement = 8.05 μg/mL; MIC Bacillus = 63 μg/mL; MIC other strains = 32 μg/mL) were the most promising compounds among those tested in this study.

Tài liệu tham khảo

Alemán-Vega M, Sánchez-Lozano I, Hernández-Guerrero CJ, Hellio C, Quintana ET (2020) Exploring antifouling activity of biosurfactants producing marine bacteria isolated from Gulf of California. Int J Mol Sci 21:6068 Almeida J, Correia-da-Silva M, Sousa E, Antunes J, Pinto M, Vasconcelos V, Cunha I (2017) Antifouling potential of nature-inspired sulfated compounds. Sci Rep 7:42424 Amara I, Miled W, Ben SR, Ladhari N (2018) Antifouling processes and toxicity effects of antifouling paints on marine environment. A review. Environ Toxicol Pharmacol 57:115–130 Appleton DR, Chuen CS, Berridge MV, Webb VL, Copp BR (2009) Rossinones A and B, biologically active meroterpenoids from the antarctic ascidian, Aplidium species. J Org Chem 74:9195–9198 Benslimane AF, Pouchus YF, Le Boterff J et al (1988) Substances cytotoxiques et antibactériennes de l’ascidie Aplidium antillense. J Nat Prod 51:582–583 Bertanha CS, Januário AH, Alvarenga TA, Pimenta L, Silva M, Cunha W, Pauletti P (2014) Quinone and hydroquinone metabolites from the ascidians of the genus Aplidium. Mar Drugs 12:3608–3633 Birringer M, Siems K, Maxones A, Frank J, Lorkowski S (2018) Natural 6-hydroxy-chromanols and-chromenols: structural diversity, biosynthetic pathways and health implications. RSC Adv 8:4803–4841 Blossom N, Szafranski F, Lotz A (2018) Use of copper-based antifouling paint: a US regulatory update. Am Coatings Assoc Ind Mark Anal 9th Ed. https://chemquest.com/wp-content/uploads/2018/03/March-2018-CoatingsTech_Antifouling-article_FINAL.pdf. Accessed 29 Apr 2020 Blunt JW, Copp BR, Keyzers RA et al (2018) Marine natural products. Nat Prod Rep 35:8–53 Bovio E, Fauchon M, Toueix Y, Mehiri M, Varese GC, Hellio C (2019) The sponge-associated fungus Eurotium chevalieri MUT 2316 and its bioactive molecules: potential applications in the field of antifouling. Mar Biotechnol 21:743–752 Bryan PJ, McClintock JB, Slattery M, Rittschof DP (2003) A comparative study of the non-acidic chemically mediated antifoulant properties of three sympatric species of ascidians associated with seagrass habitats. Biofouling 19:235–245 Carbone M, Núñez-Pons L, Paone M, Castelluccio F, Avila C, Gavagnin M (2012) Rossinone-related meroterpenes from the Antarctic ascidian Aplidium fuegiense. Tetrahedron. 68:3541–3544 Carroll AR, Copp BR, Davis RA, Keyzers RA, Prinsep MR (2020) Marine natural products. Nat Prod Rep 37:175–223 Carson RT, Damon M, Johnson LT, Gonzales JA (2009) Conceptual issues in designing a policy to phase out metal-based antifouling paint on recreational boats in San Diego Bay. J Environ Manag 90:2460–2468 Chan STS, Pearce AN, Januario AH, Page MJ, Kaiser M, McLaughlin RJ, Harper JL, Webb VL, Barker D, Copp BR (2011) Anti-inflammatory and antimalarial meroterpenoids from the New Zealand ascidian Aplidium scabellum. J Org Chem 76:9151–9156 Christie AO, Dalley R (1987) Barnacle fouling and its prevention. In: Southward AJ (ed) Barnacle Biology, Crustacean issues 5:419–433 Clare AS (1996) Marine natural product antifoulants: status and potential. Biofouling 9:211–229 Culioli G, Ortalo-Magné A, Valls R et al (2008) Antifouling activity of meroditerpenoids from the marine brown alga Halidrys siliquosa. J Nat Prod 71:1121–1126 Dafforn KA, Lewis JA, Johnston EL (2011) Antifouling strategies: history and regulation, ecological impacts and mitigation. Mar Pollut Bull 62:453–465 Darya M, Sajjadi MM, Yousefzadi M, Sourinejad I, Zarei M (2020) Antifouling and antibacterial activities of bioactive extracts from different organs of the sea cucumber Holothuria leucospilota. Helgol Mar Res 74:4 Davis AR (1991) Alkaloids and ascidian chemical defense: evidence for the ecological role of natural products from Eudistoma olivaceum. Mar Biol 111:375–379 Davis AR, Wright AE (1989) Interspecific differences in fouling of two congeneric ascidians (Eudistoma olivaceum and E. capsulatum): is surface acidity an effective defense? Mar Biol 102:491–497 Davis AR, Wright AE (1990) Inhibition of larval settlement by natural products from the ascidian, Eudistoma olivaceum (Van Name). J Chem Ecol 16:1349–1357 Davis AR, Targett NM, McConnell OJ, Young CM (1989) Epibiosis of marine algae and benthic invertebrates: natural products chemistry and other mechanisms inhibiting settlement and overgrowth. In: Scheuer PJ (ed) Bioorganic marine chemistry, vol 3. Springer, Berlin, Heidelberg de Carvalho CCCR (2018) Marine biofilms: a successful microbial strategy with economic implications. Front Mar Sci 5:126 De Nys R, Steinberg PD (2002) Linking marine biology and biotechnology. Curr Opin Biotechnol 13:244–248 Demirel YK, Turan O, Incecik A (2017) Predicting the effect of biofouling on ship resistance using CFD. Appl Ocean Res 62:100–118 El Hattab M, Genta-Jouve G, Bouzidi N et al (2015) Cystophloroketals A-E, unusual phloroglucinol-meroterpenoid hybrids from the brown alga Cystoseira tamariscifolia. J Nat Prod 78:1663–1670 Flach CF, Pal C, Svensson CJ, Kristiansson E, Östman M, Bengtsson-Palme J, Tysklind M, Larsson DGJ (2017) Does antifouling paint select for antibiotic resistance? Sci Total Environ 590-591:461–468 Garrido L, Zubía E, Ortega MJ, Salvá J (2002) New Meroterpenoids from the ascidian Aplidium conicum. J Nat Prod 65:1328–1331 Hastings J, Owen G, Dekker A, Ennis M, Kale N, Muthukrishnan V, Turner S, Swainston N, Mendes P, Steinbeck C (2016) ChEBI in 2016: improved services and an expanding collection of metabolites. Nucleic Acids Res 44:D1214–D1219 Hellio C, Berge JP, Beaupoil C et al (2002) Screening of marine algal extracts for anti-settlement activities against microalgae and macroalgae. Biofouling 18:205–215 Holmström C, Kjelleberg S (1994) The effect of external biological factors on settlement of marine invertebrate and new antifouling technology. Biofouling 8:147–160 Jadidi P, Zeinoddini M (2020) Influence of hard marine fouling on energy harvesting from vortex-induced vibrations of a single-cylinder. Renew Energy 152:516–528 Jones B, Bolam T (2007) Copper speciation survey from UK marinas, harbours and estuaries. Mar Pollut Bull 54:1127–1138 King JR, Edgar S, Qiao K, Stephanopoulos G (2016) Accessing Nature’s diversity through metabolic engineering and synthetic biology. F1000Research 5:397 Kjelleberg S, Steinberg P (1994) Marine biofouling: problems and solution-executive summary. In: Biofouling: problems and solutions. Proceedings of the international workshop, UNSW, Sydney, Australia. pp 32–38 Koplovitz G (2011) An examination of secondary metabolites and inorganic acids as chemical defences against predation and fouling in antarctic and sub-tropical ascidians. The University of Alabama at Birmingham, ProQuest Dissertations Publishing. 3469618 Koryakova MD, Korn OM (1993) Use of barnacle larvae to test the toxicity of some antifouling coatings. Biol morya/Marine Biol Vladivostok 3:106–113 Kymenvaara S, Tegnér Anker H, Baaner L et al (2017) Regulating antifouling paints for leisure boats-a patchwork of rules across three Baltic Sea countries. Nord Environ Law J 1:7–32 Lau SCK, Qian P (2000) Inhibitory effect of phenolic compounds and marine bacteria on larval settlement of the barnacle Balanus amphitrite amphitrite Darwin. Biofouling 16:47–58 Le Manach C, Paquet T, Wicht K et al (2018) Antimalarial lead-optimization studies on a 2, 6-imidazopyridine series within a constrained chemical space to circumvent atypical dose–response curves against multidrug resistant parasite strains. J Med Chem 61:9371–9385 Li Y, Ning C (2019) Latest research progress of marine microbiological corrosion and biofouling, and new approaches of marine anti-corrosion and anti-fouling. Bioact Mater 4:189–195 Little BJ, Lee JS, Ray RI (2008) The influence of marine biofilms on corrosion: a concise review. Electrochim Acta 54:2–7 López-Legentil S, Turon X, Erwin PM (2016) Feeding cessation alters host morphology and bacterial communities in the ascidian Pseudodistoma crucigaster. Front Zool 13:2 Lotz A (2016) Marine coatings: making sense of US, state, and local mandates of copper-based antifouling regulations. JCT CoatingTech 13:50–54 Marechal JP, Hellio C (2009) Challenges for the development of new non-toxic antifouling solutions. Int J Mol Sci 10:4623–4637 Mayzel B, Haber M, Ilan M (2014) Chemical defense against fouling in the solitary ascidian Phallusia nigra. Biol Bull 227:232–241 Menna M, Aiello A, D’Aniello F et al (2013) Conithiaquinones A and B, tetracyclic cytotoxic meroterpenes from the mediterranean ascidian Aplidium conicum. Eur J Org Chem 2013:3241–3246 Moodie LWK, Trepos R, Cervin G, Larsen L, Larsen DS, Pavia H, Hellio C, Cahill P, Svenson J (2017) Probing the structure–activity relationship of the natural antifouling agent polygodial against both micro- and macrofoulers by semisynthetic modification. J Nat Prod 80:515–525 Murugan A, Ramasamy MS (2003) Biofouling deterrent activity of the natural product from ascidian, Distaplia nathensis [Chordata]. Indian J Geo-Mar Sci 32:162–164 Núñez-Pons L, Carbone M, Vázquez J, Rodríguez J, Nieto RM, Varela MM, Gavagnin M, Avila C (2012) Natural products from antarctic colonial ascidians of the genera Aplidium and Synoicum: variability and defensive role. Mar Drugs 10:1741–1764 Odate S, Pawlik JR (2007) The role of vanadium in the chemical defense of the solitary tunicate, Phallusia nigra. J Chem Ecol 33:643–654 Palanisamy SK, Rajendran NM, Marino A (2017) Natural products diversity of marine ascidians (tunicates; Ascidiacea) and successful drugs in clinical development. Nat Products Bioprospect 7:1–111 Parry D (1984) Chemical properties of the test of ascidians in relation to predation. Mar Ecol Prog Ser 17:279–282 Piazza V, Roussis V, Garaventa F, Greco G, Smyrniotopoulos V, Vagias C, Faimali M (2011) Terpenes from the red alga Sphaerococcus coronopifolius inhibit the settlement of barnacles. Mar Biotechnol 13:764–772 Piazza V, Dragić I, Sepečić K et al (2014) Antifouling activity of synthetic alkylpyridinium polymers using the barnacle model. Mar Drugs 12:1959–1976 Piola FR, Dafforn KA, Johnston EL (2009) The influence of antifouling practices on marine invasions: a mini-review. Biofouling 25:633–644 Pisut DP, Pawlik JR (2002) Anti-predatory chemical defenses of ascidians: secondary metabolites or inorganic acids? J Exp Mar Biol Ecol 270:203–214 Ponasik JA, Conova S, Kinghorn D, Kinney WA, Rittschof D, Ganem B (1998) Pseudoceratidine, a marine natural product with antifouling activity: synthetic and biological studies. Tetrahedron 54:6977–6986 Qi S-H, Ma X (2017) Antifouling compounds from marine invertebrates. Mar Drugs 15:263 Qian P-YY, Li Z, Xu Y, Li Y, Fusetani N (2015) Mini-review: marine natural products and their synthetic analogs as antifouling compounds: 2009-2014. Biofouling 31:101–122 Ralston E, Swain G (2009) Bioinspiration - the solution for biofouling control? Bioinspir Biomim 4:015007 Rittschof D (2000) Natural product antifoulant: one perspective on the challenges related to coatings development. Biofouling 15:119–127 Rittschof D, Clare AS, Gerhart DJ, Mary SA, Bonaventura J (1992) Barnacle in vitro assays for biologically active substances: toxicity and settlement inhibition assays using mass cultured Balanus amphitrite amphitrite Darwin. Biofouling 6:115–122 Sánchez-Lozano I, Hernández-Guerrero CJ, Muñoz-Ochoa M, Hellio C (2019) Biomimetic approaches for the development of new antifouling solutions: study of incorporation of macroalgae and sponge extracts for the development of new environmentally-friendly coatings. Int J Mol Sci 20:4863 Schiff K, Brown J, Diehl D, Greenstein D (2007) Extent and magnitude of copper contamination in marinas of the San Diego region, California, USA. Mar Pollut Bull 54:322–328 Schultz MP (2007) Effects of coating roughness and biofouling on ship resistance and powering. Biofouling 23:331–341 Schultz MP, Bendick JA, Holm ER, Hertel WM (2011) Economic impact of biofouling on a naval surface ship. Biofouling 27:87–98 Sera Y, Adachi K, Nishida F, Shizuri Y (1999) A new sesquiterpene as an antifouling substance from a Palauan marine sponge, Dysidea herbacea. J Nat Prod 62:395–396 Simon-Levert A, Arrault A, Bontemps-Subielos N, Canal C, Banaigs B (2005) Meroterpenes from the ascidian Aplidium aff. densum. J Nat Prod 68:1412–1415 Simon-Levert A, Aze A, Bontemps-Subielos N, Banaigs B, Genevière AM (2007) Antimitotic activity of methoxyconidiol, a meroterpene isolated from an ascidian. Chem Biol Interact 168:106–116 Simon-Levert A, Menniti C, Soulère L, Genevière AM, Barthomeuf C, Banaigs B, Witczak A (2010) Marine natural meroterpenes: synthesis and antiproliferative activity. Mar Drugs 8:347–358 Steinberg PD, Schneider R, Kjelleberg S (1997) Chemical defenses of seaweeds against microbial colonization. Biodegradation 8:211–220 Stoecker D (1978) Resistance of a tunicate to fouling. Biol Bull 155:615–626 Stoecker D (1980a) Chemical defenses of ascidians against predators. Ecology 61:1327–1334 Stoecker D (1980b) Distribution of acid and vanadium in Rhopalaea birkelandi Tokioka. J Exp Mar Biol Ecol 48:277–281 Tello E, Castellanos L, Arevalo-Ferro C, Rodríguez J, Jiménez C, Duque C (2011) Absolute stereochemistry of antifouling cembranoid epimers at C-8 from the Caribbean octocoral Pseudoplexaura flagellosa. Revised structures of plexaurolones. Tetrahedron 67:9112–9121 Teo SLM, Ryland JS (1995) Potential antifouling mechanisms using toxic chemicals in some British ascidians. J Exp Mar Biol Ecol 188:49–62 Thompson TE (1988) Acidic allomones in marine organisms. J Mar Biol Assoc U K 68:499–517 Tianero MD, Kwan JC, Wyche TP et al (2015) Species specificity of symbiosis and secondary metabolism in ascidians. ISME J 9:615–628 Trepos R, Cervin G, Hellio C, Pavia H, Stensen W, Stensvåg K, Svendsen JS, Haug T, Svenson J (2014) Antifouling compounds from the sub-arctic ascidian Synoicum pulmonaria: Synoxazolidinones A and C, pulmonarins A and B, and synthetic analogues. J Nat Prod 77:2105–2113 Tsukamoto S, Kato H, Hirota H, Fusetani N (1997) Antifouling terpenes and steroids against barnacle larvae from marine sponges. Biofouling 11:283–291 Turon X (1992) Periods of non-feeding in Polysyncraton lacazei (Ascidiacea: Didemnidae): a rejuvenative process? Mar Biol 112:647–655 Vallee-Rehel K, Mariette B, Hoarau PA, Guerin P, Langlois V, Langlois JY (1998) A new approach in the development and testing of antifouling paints without organotin derivatives. J Coatings Technol 70:55–63 Wahl M, Banaigs B (1991) Marine epibiosis. III. Possible antifouling defense adaptations in Polysyncraton lacazei (Giard)(Didemnidae, Ascidiacea). J Exp Mar Biol Ecol 145:49–63 Wahl M, Lafargue F (1990) Marine epibiosis. Oecologia 82:275–282 Wahl M, Jensen PR, Fenical W (1994) Chemical control of bacterial epibiosis on ascidians. Mar Ecol Prog Ser 110:45–57 Wang K-L, Wu Z-H, Wang Y, Wang CY, Xu Y (2017) Mini-review: antifouling natural products from marine microorganisms and their synthetic analogs. Mar Drugs 15:266 Watermann BT, Daehne B, Sievers S, Dannenberg R, Overbeke JC, Klijnstra JW, Heemken O (2005) Bioassays and selected chemical analysis of biocide-free antifouling coatings. Chemosphere 60:1530–1541 Wu RSS, Lam PKS, Zhou B (1997) A settlement inhibition assay with cyprid larvae of the barnacle Balanus amphitrite. Chemosphere 35:1867–1874 Xu Y, Li N, Jiao WH, Wang RP, Peng Y, Qi SH, Song SJ, Chen WS, Lin HW (2012) Antifouling and cytotoxic constituents from the South China Sea sponge Acanthella cavernosa. Tetrahedron 68:2876–2883 Yebra DM, Kiil S, Dam-Johansen K (2004) Antifouling technology - past, present and future steps towards efficient and environmentally friendly antifouling coatings. Prog Org Coat 50:75–104 Zega G, Pennati R, Dahlström M, Berntsson K, Sotgia C, de Bernardi F (2007) Settlement of the barnacle Balanus improvisus: the roles of dopamine and serotonin. Ital J Zool 74:351–361