Abstract
The capacity of two homoserine lactones to stimulate the marine bacteria Pseudoalteromonas ulvae (TC14 strain) for its capacity to form a biofilm when exposed to a potent antibiofilm compound AS162 is reported. Effective concentrations (EC50) of AS162 at 24 h, 48 h, and 72 h were, respectively, of 4.3, 4.4, and 6.0 µM. When tested in combination with HSLs, results showed that quorum-sensing signal molecules 3-oxo-C6 and 3-oxo-C8 homoserine lactones do not act directly on the biofilm formation, but are able to interfere positively with AS162 to promote biofilm growth with EC50 ranging from 30 to 50 µM. The same results were obtained with two other marine bacterial strains: Pseudoalteromonas lipolytica TC8 and Paracoccus sp. 4M6. These findings suggest that HSLs can significantly affect the biocidal sensitivity of marine bacteria to antifouling agents.
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References
Andjouh S, Blache Y (2015) Click-based synthesis of bromotyrosine alkaloid analogs as potential anti-biofilm leads for SAR studies. Bioorg Med Chem Lett 25(24):5762–5766
Andjouh S, Blache Y (2016) Screening of bromotyramine analogues as antifouling compounds against marine bacteria. Biofouling 32(8):871–881
Andjouh S, Blache Y (2019) Parallel synthesis of a bis-triazoles library as psammaplin A analogues: a new wave of antibiofilm compounds? Bioorg Med Chem Lett. https://doi.org/10.1016/j.bmcl.2018.12.047
Andjouh S, Perrin FX, Blache Y (2017) in “bis-triazoles compounds with anti-biofilm and anti-corrosion properties”. WO 2017/102883 A1, International Application Number PCT/EP2016/081068. US 2018 / 0370953 A1. https://patents.google.com/patent/US20180370953A1/en
Ayé AM, Bonnin-Jusserand M, Brian-Jaisson F, Ortalo-Magné A, Culioli G, Nevry RK, Blache NY, Molmeret M (2015) Modulation of violacein production and phenotypes associated with biofilm by exogenous quorum sensing N-acylhomoserine lactones in the marine bacterium Pseudoalteromonas ulvae TC14. Microbiology 161(10):2039–2051
Bhadury P, Wright P (2004) Exploitation of marine algae: biogenic compounds for potential antifouling applications. Planta 219:561–578
Brian-Jaisson F, Ortalo-Magné A, Guentas-Dombrowsky L, Armougom F, Blache Y, Molmeret M (2014) Identification of bacterial strains isolated from the mediterranean sea exhibiting different abilities of biofilm formation. Microb Ecol 68:94–110
Camps M, Briand J-F, Guentas-Dombrowsky L, Culioli G, Bazire A, Blache Y (2011) Antifouling activity of commercial biocides vs. Natural and natural-derived products assessed by marine bacteria adhesion bioassay. Mar Poll Bull 62:1032–1040
Ciriminna R, Bright F, Pagliaro M (2015) Ecofriendly antifouling marine coatings. ACS Sustain Chem Eng 3:559–565
De Nys R, Steinberg PD (2002) Linking marine biology and biotechnology. Curr Opin Biotechnol 13:244–248
Fitridge I, DempsterT Guenther J, de Nys R (2012) The impact and control of biofouling in marine aquaculture: a review. Biofouling 28:649–669
Fusetani N (2004) Biofouling and antifouling. Nat Prod Rep 21:94–104
Fusetani N (2011) Antifouling marine natural products. Nat Prod Rep 28:400–410
Gerwick WH, Moore Bradley S (2012) Lessons from the past and charting the future of marine natural products drug discovery and chemical biology. Chem Biol 19:85–98
Grasland B, Mitalane J, Briandet R, Quémener E, Meylheuc T, Linossier I, Vallée-Réhel K, Haras D (2003) Bacterial biofilm in seawater: cell surface properties of early-attached marine bacteria. Biofouling 19:307–331
Hamann MT, Scheuer PJ, Kelly-Borges M (1993) Biogenetically diverse, bioactive constituents of a sponge, order verongida: bromotyramines and sesquiterpene-shikimate derived metabolites. J Org Chem 58:6565–6569
Hellio C, Tsoukatou M, Maréchal J-P, Aldred N, Beaupoil C, Clare AS, Vagias C, Roussis V (2005) Inhibitory effects of mediterranean sponge extracts and metabolites on larval settlement of the barnacle balanus amphitrite. Mar Biotechnol 7:297–305
Krug PJ (2006) Defense of benthic invertebrates against surface colonization by larvae: a chemical arms race. Antifouling compounds. Springer, Berlin, Heidelberg, pp 1–53
Linares D, Bottzeck O, Pereira O, Praud-Tabariès A, Blache Y (2011) Designing 2-aminoimidazole alkaloids analogs with anti-biofilm activities: structure–activities relationships of polysubstituted triazoles. Bioorg Med Chem Lett 21:6751
Liu N, Xu Y, Hossain S, Huang N, Coursolle D, Gralnick JA, Boon EM (2012) Nitric oxide regulation of cyclic di-GMP synthesis and hydrolysis in Shewanella woodyi. Biochem. (Mosc) 51:2087–2099
Mangwani N, Kumari S, Das S (2016) Effect of synthetic N-acylhomoserine lactones on cell–cell interactions in marine Pseudomonas and biofilm mediated degradation of polycyclic aromatic hydrocarbons. Chem Eng J 302:172–186
Maréchal J-P, Hellio C (2009) Challenges for the development of new non-toxic antifouling solutions. Int JMol Sci 10:4623–4637
Müller WG, Brümmer F, Batel R, Müller I, Schröder H (2003) Molecular biodiversity. Case study: Porifera (sponges). Naturwissenschaften 90:103–120
Muras A, López-Pérez M, Mayer C, Parga A, Amaro-Blanco J Ana, Otero A (2018) High prevalence of quorum-sensing and quorum-quenching activity among cultivable bacteria and metagenomic sequences in the mediterranean sea. Genes 9:100
Othmani A, Bouzidi N, Viano Y, Alliche Z, Seridi H, Blache Y, El Hattab M, Briand J-F, Culioli G (2014) Anti-microfouling properties of compounds isolated from several mediterranean dictyota spp. J Appl Phycol 26:1573–1584
Passos da Silva D, Schofield MC, Parsek MR, Tseng BS (2017) An update on the sociomicrobiology of quorum sensing in gram-negative biofilm development. Pathogens (Basel Switz.) 6:51
Qian PY, Lau SCK, Dahms HU, Dobretsov S, Harder T (2007) Marine biofilms as mediators of colonization by marine macroorganisms: implications for antifouling and aquaculture. Mar Biotechnol 9:399–410
Sipkema D, Franssen MR, Osinga R, Tramper J, Wijffels R (2005) Marine sponges as pharmacy. Mar Biotechnol 7:142–162
Steinberg P, Schneider R, Kjelleberg S (1997) Chemical defenses of seaweeds against microbial colonization. Biodegradation 8:211–220
Stowe SD, Richards JJ, Tucker AT, Thompson R, Melander C, Cavanagh J (2011) Anti-biofilm compounds derived from marine sponges. Mar Drugs 9:2010–2035
Sun J, Wu L, An B, de Voogd J, Cheng N, Lin W (2018) Bromopyrrole alkaloids with the inhibitory effects against the biofilm formation of gram-negative bacteria. Mar drugs 16:9
Tsukamoto S, Kato H, Hirota H, Fusetani N (1996a) Ceratinamides a and b: new antifouling dibromotyrosine derivatives from the marine sponge pseudoceratina purpurea. Tetrahedron 52:8181–8186
Tsukamoto S, Kato H, Hirota H, Fusetani N (1996b) Ceratinamine: an unprecedented antifouling cyanoformamide from the marine sponge Pseudoceratina purpurea. J Org Chem 61:2936–2937
Tsukamoto S, Kato H, Hirota H, Fusetani N (1996c) Pseudoceratidine: a new antifouling spermidine derivative from the marine sponge Pseudoceratina purpurea. Tetrahedron Lett 37:1439–1440
Waters CM, Bassler BL (2005) Quorum sensing: cell-to-cell communication in bacteria. Annu Rev Cell Dev Biol 21:319–346
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
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This research did not receive any specific grant from funding agencies (public, or private). The Paracoccus sp. strain 4M6 was provided by the LBCM (Université de Bretagne Sud).
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Gozoua, E., Koffi-Nevry, R. & Blache, Y. Biofilm formation in marine bacteria and biocidal sensitivity: interplay between a potent antibiofilm compound (AS162) and quorum-sensing autoinducers. 3 Biotech 9, 338 (2019). https://doi.org/10.1007/s13205-019-1866-6
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DOI: https://doi.org/10.1007/s13205-019-1866-6