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Novel Natural Parabens Produced by a Microbulbifer Bacterium in Its Calcareous Sponge Host Leuconia Nivea

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Novel Natural Parabens Produced by a Microbulbifer Bacterium in Its Calcareous Sponge Host Leuconia Nivea Environmental Microbiology (2009) doi:10.1111/j.1462-2920.2009.01880.x Novel natural parabens produced by a Microbulbifer bacterium in its calcareous sponge host Leuconia nivea Elodie Quévrain,1 Isabelle Domart-Coulon,2 parabens in a sponge host, which may have an eco- Mathieu Pernice2 and logical role as chemical mediators. Marie-Lise Bourguet-Kondracki1* 1Laboratoire de Chimie et Biochimie des Substances Introduction Naturelles UMR 5154 CNRS, Muséum National d’Histoire Naturelle, 57 rue cuvier (C. P 54), Paris, Although the Porifera phylum continues to be an excellent France. source of bioactive and original natural products (Blunt 2Laboratoire de Biologie des Organismes Marins et des et al., 2008), sponge-associated microorganisms have Ecosystèmes UMR 5178 MNHN-CNRS-UPMC, Muséum emerged as promising candidates for the production of National d’Histoire Naturelle, 57 rue cuvier (C. P 51), natural compounds (Moore, 1999; Piel, 2006; Blunt et al., Paris, France. 2007). Recently, many studies revealed that metabolites previously ascribed to sponges were in fact synthesized by microorganisms (Proksch et al., 2002; Hildebrand Summary et al., 2004; Piel, 2004; Salomon et al., 2004), while A broad variety of natural parabens, including four others demonstrated structural similarities between novel structures and known ethyl and butyl parabens, natural products isolated from sponges and bacterial were obtained from culture of a Microbulbifer sp. bac- metabolites (Crews and Bescansa, 1986; Zabriskie et al., terial strain isolated from the temperate calcareous 1986; Jansen et al., 1996; Erickson et al., 1997; Kunze marine sponge Leuconia nivea (Grant 1826). Their et al., 1998). These data explain the considerable atten- structures were elucidated from spectral analysis, tion paid by scientists over the last decade (Bewley and including mass spectrometry and 1D and 2D nuclear Faulkner, 1998; Hentschel et al., 2006; Taylor et al., 2007) magnetic resonance. Their antimicrobial activity to the diverse microorganisms associated with marine evaluated against Staphylococcus aureus was char- sponges. Electron microscopy has shown that in some acterized by much higher in vitro activity of these demosponges these microorganisms constitute up to natural paraben compounds 3–9 than commercial syn- 60% of the biomass (Vacelet and Donadey, 1977; Wilkin- thetic methyl and propyl parabens, usually used as son, 1978). In contrast to siliceous sponges, very few antimicrobial preservatives. Compounds 4 and 9 chemical and microbiological studies have so far been revealed a bacteriostatic effect and compounds 6 and carried out on calcareous sponges. Those which do exist 7 appeared as bactericidal compounds. Major paraben are restricted to the Calcinea subclass, with to our know- compound 6 was also active against Gram positive ledge no studies of the Calcaronea subclass (Schreiber Bacillus sp. and Planococcus sp. sponge isolates and et al., 2006; Muscholl-Silberhorn et al., 2008). was detected in whole sponge extracts during all In a programme devoted to studying the role of sponge- seasons, showing its persistent in situ production associated bacteria and especially the chemical media- within the sponge. Moreover, Microbulbifer sp. bacte- tors of the interactions between microbial associates in ria were visualized in the sponge body wall using their sponge host, the cultivable heterotrophic bacterial fluorescence in situ hybridization with a probe specific biota was isolated from the temperate calcareous sponge to L4-n2 phylotypes. Co-detection in the sponge host Leuconia nivea collected off Concarneau (Northeast of both paraben metabolites and Microbulbifer sp. Atlantic, France). The sponge L. nivea (Grant 1826), L4-n2 indicates, for the first time, production of natural which belongs to the Baeriidae family in the Calcaronea subclass, was chosen because its chloromethylenic (CH2Cl2) crude extract revealed a significant and annually persistent antimicrobial activity against Staphylococcus Received 29 August, 2008; accepted 16 December, 2008. *For cor- respondence. E-mail [email protected]; Tel. (+33)140793135; aureus. This activity was localized in the bacterial fraction Fax (+33)140795606. of the sponge obtained by differential sedimentation © 2009 The Authors Journal compilation © 2009 Society for Applied Microbiology and Blackwell Publishing Ltd 2 E. Quévrain, I. Domart-Coulon, M. Pernice and M.-L. Bourguet-Kondracki Table 1. Antimicrobial activity of the sponge Leuconia nivea throughout 2005–2007, extraction yield and presence of compound 6 in the CH2Cl2 crude extracts. Wet weight Dry weight CH2Cl2 mass CH2Cl2 extract’s yield Activity against Compound 6 Season Collection date (g) (g) extract (mg) (% of dry weight) S. aureus ATCC 6538a detection (LC/MS) Spring 30 March 2006 21.9 5.2 13.5 0.26 + (7.5 mm) ND 27 April 2006 517.0 13.7 26.9 0.20 + (7.5 mm) + Summer 24 June 2005 4.5 1.1 18.0 1.67 + (11 mm) ND 24 July 2005 27.0 6.5 55.9 0.86 + (7 mm) + Fall 09 September 2006 ND ND 12.3 ND + (8 mm) + 27 September 2007 5.3 1.3 11.0 0.87 + (10 mm) + 17 October 2005 24.8 5.9 22.7 0.38 + (9 mm) + Winter 31 January 2006 45.6 10.9 13.3 0.12 + (8 mm) + 19 February 2007 12.1 2.9 3.3 0.11 + (8 mm) ND a. Inhibition’s diameter of the CH2Cl2 extract measured by the disc diffusion assay method for 1 mg per disc. ND, not determined. following the method of Richelle-Maurer and colleagues to three different seasons (data not shown). These results (2001). The cultivable heterotrophic bacterial biota asso- prompted us to investigate the microbial community asso- ciated with L. nivea was screened to isolate bioactive ciated with this marine calcareous sponge. strains, with antimicrobial activity spectra that matched whole sponge extracts. This provided a novel model to investigate the contribution of bacterial metabolites to the Description of the strain L4-n2 chemical profile and antimicrobial activity of their sponge Among the cultivable heterotrophic bacterial biota asso- host. ciated with L. nivea, one of the most active strains, named The antimicrobial activity of heterotrophic bacteria iso- L4-n2, was isolated in January 2006 on Marine Agar lated from L. nivea was examined. CH2Cl2 crude extract supplemented with nalidixic acid and grown in pure culture investigations of the most active strains, Microbulbifer in marine agar or marine broth. Bacteria of the strain L4-n2 sp., led to the isolation of a broad variety of natural para- were Gram negative, rod-shaped, and approximately bens. In addition to the known ethyl 1 and butyl 2 para- 0.3–0.5 mm wide by 2–4 mm long. They were aerobic and bens, seven natural parabens including four novel formed smooth, convex and mucoid colonies on marine structures 5, 6, 7 and 9 were identified. We also con- agar, producing a non-diffusible brown pigment. They were firmed the in situ production and annual persistence of resistant to ampicillin, penicillin and oxacillin and sensitive the major bacterial compound 6 in the L. nivea sponge to kanamycin (30 UI) and ceftazidime (30 mg). through liquid chromatography mass spectrometry (LC/ MS) analysis. This study provides the first chemical report of a family Phylogenetic affiliation of L4-n2 of bioactive compounds from a bacterium associated to a calcareous sponge belonging to the Baeriidae family, and Strain L4-n2 was identified by sequencing the partial 16S proves its in situ production within the sponge host. rRNA gene. Sequences were compared with those in the database by using FASTA (Pearson and Lipman, 1988). The FASTA search affiliated L4-n2 isolated from L. nivea Results with the RSBr-1 type strain of marine bacterium Micro- bulbifer arenaceous previously isolated from red sand- Antimicrobial activity of the sponge L. nivea stone off the coast of Scotland (Tanaka et al., 2003) with We established that CH2Cl2 extracts of the sublittoral 99.8% 16S rDNA sequence identity. A 16S rRNA-based sponge L. nivea collected off Concarneau inhibited the phylogenetic tree constructed using the maximum likeli- growth of the clinical strain S. aureus (ATCC 6538) in the hood algorithm (Felsenstein, 1981) affiliated L4-n2 with agar diffusion assay. Collection at three month intervals the genus Microbulbifer in the Alteromonadales order of from 2005 to 2007 showed that this activity was retained the Gammaproteobacteria subdivision. Within the Microb- throughout the year (Table 1). Furthermore, the anti- ulbifer genus, the L4-n2 isolate formed a highly supported S. aureus activity was reproducibly localized in the bacte- clade with the marine sandstone derived species rial fraction of the sponge, obtained by differential M. arenaceous and with the halophile environmental sedimentation of mechanically dissociated sponge sus- Microbulbifer sp. strain YIM C306, with a bootstrap confi- pension in three independent experiments corresponding dence level of 99.8% (Fig. 1). © 2009 The Authors Journal compilation © 2009 Society for Applied Microbiology and Blackwell Publishing Ltd, Environmental Microbiology Parabens from sponge associated bacteria 3 Bacillus algicola SC3 (DQ001308) Moritella marina NCIMB 1144T (X82142) 99 Alteromonas macleodii DSM 6062 (Y18228) 77 Pseudoalteromonas flavipulchra NCIMB 2033 (AF297958) Microbulbifer maritimus TF-17 (AY377986) (intertidal) L4-n2 (FM200853) (intertidal) 100 Microbulbifer sp. YIM C306 (EU135714) 98 Microbulbifer arenaceous RSBr-1T (AJ510266) (intertidal) Microbulbifer sp. KBB-1 (DQ412068) (deep sea) 100 Microbulbifer agarilyticus JAMB A3 (AB158515) 50 Bacterium QM46 (DQ822531)
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