Seaweed defence against bacteria: a poly-brominated 2-heptanone from the red alga Bonnemaisonia hamifera inhibits bacterial colonisation

Abstract

It has previously been shown that the red alga Bonnemaisonia hamifera is less fouled by bacteria relative to co-occurring seaweeds and that surface extracts of B. hamifera inhibit bacterial growth at natural concentrations. In the present study, we isolated the antibacterial metabolite by bioassay-guided fractionation of extracts of B. hamifera using standard chromatographic methods. Nuclear magnetic resonance (NMR) spectroscopy and mass spectrometry were used for molecular identification. The antibacterial activity in the extracts was caused by a previously described polyhalogenated 2-heptanone: 1,1, 3, 3-tetrabromo-2-heptanone. To further investigate the role of this compound as an ecologically relevant antifoulant against bacterial colonisation, we quantified it on the surface of B. hamifera specimens collected in the field. Levels of 1,1, 3, 3-tetrabromo-2-heptanone on the surface of the algae were on average 3.6 µg cm -2 . Natural surface concentrations of this secondary metabolite were used to test for growth-inhibiting effects against 18 bacterial strains isolated from red algae co-occurring with B. hamifera. The test indicated a phylogenetic specificity of the metabolite, and gram-positive bacteria and flavobacteria proved to be particularly sensitive. In a further test, natural surface concentrations of 1,1, 3, 3-tetrabromo-2-heptanone were applied to artificial panels and incubated in the sea. After 4 and 7 d, the number of settled bacteria was significantly lower on all treated panels compared to controls. Thus, this study shows that 1,1, 3, 3-tetrabromo-2-heptanone has an ecologically relevant role as an antifoulant against bacterial colonisation on the surface of B. hamifera. This study is also one of only a few to quantify natural surface concentrations of a seaweed secondary metabolite.

Desorption electrospray ionization mass spectrometry reveals surface-mediated antifungal chemical defense of a tropical seaweed

“…Together, bromophycolides and callophycoic acids represent the largest group of algal antifungal chemical defenses reported to date, adding to only a handful of previously identified antimicrobial chemical defenses from macroalgae (9,11,(17)(18)(19). DESI-MS imaging revealed antifungal bromophycolides both within algal tissues and among distinct patches covering only Ϸ5% of algal surfaces (Fig.…”

“…In the marine realm, numerous taxa have been suggested to use surface-associated defenses against competitors, foulers, and pathogens (5)(6)(7)(8)(9)(10). However, such defenses were often proposed based on inhibitory effects detected in experiments, using whole organism extracts (5,7), and it is unclear whether target species actually encountered these chemicals in nature.…”

“…Among marine macroalgae, only a handful of studies have evaluated roles of specific secondary metabolites in defense against deleterious microbes (17)(18)(19). Only the 22-membered lactone lobophorolide from the brown alga Lobophora variegata (11), a polybrominated 2-heptanone from the red alga Bonnemaisonia hamifera (9), and furanones from the red alga Delisea pulchra (20) have been proposed as surfaceassociated antimicrobial defenses of marine algae.…”

“…However, such defenses were often proposed based on inhibitory effects detected in experiments, using whole organism extracts (5,7), and it is unclear whether target species actually encountered these chemicals in nature. In more ecologically realistic studies, roles of surface-associated molecules were proposed based on experiments employing surface extracts or pure compounds tested at their approximate surface concentration (6,(9)(10)(11)(12)(13). Unfortunately, current extraction-based methodologies are limited to certain classes of molecules.…”

Taxonomy of Marine Macroalgae Used as Sources of Bioactive Compounds

“…These algae are known to produce several secondary metabolites with valuable biological activities, in particular volatile halogenated compounds with strong antibacterial properties (e.g., Genovese et al 2009 ) . Some recent ecological studies have provided evidence that these compounds are the main mechanism that these algae use to maintain bacteriafree surfaces (Paul et al 2006 ;Nylund et al 2008 ) . Several other bioactivities have also been described from crude extracts derived from Asparagopsis armata (e.g., antiviral and antibacterial: Bansemir et al .…”