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.
Seaweed cultivation attracts growing interest and sustainability assessments from various perspectives are needed. The paper presents a holistic qualitative assessment of ecosystem services affected by seaweed cultivation on the Swedish west coast. Results suggest that supporting, regulating and provisioning services are mainly positively or non-affected while some of the cultural services are likely negatively affected. The analysis opens for a discussion on the framing of seaweed cultivation - is it a way of supplying ecosystem services and/or a way of generating valuable biomass? Exploring these framings further in local contexts may be valuable for identifying trade-offs and designing appropriate policies and development strategies. Many of the found impacts are likely generalizable in their character across sites and scales of cultivation, but for some services, including most of the supporting services, the character of impacts is likely to be site-specific and not generalizable.
1. Allelopathy is an important non-resource interaction in terrestrial plant communities that may affect invasions by non-indigenous plants. The 'novel weapons hypothesis' (NWH) predicts that non-indigenous plants will become invasive if they have allelopathic compounds that assemblages in the new range are not adapted to. Recently, the non-indigenous, chemically rich macroalga Bonnemaisonia hamifera (Hariot) has become one of the most abundant filamentous red algae in Scandinavian waters. 2. We used B. hamifera to specifically test the aspect of the NWH that concerns invasion success based on novel allelochemicals in the invaded range. Allelopathic interactions were tested through effects on the growth rate of adult native macroalgae in co-cultures with B. hamifera and through the settlement success of native macroalgal propagules and microalgae on surfaces coated with 1,1,3,3-tetrabromo-2-heptanone. We also investigated whether 1,1,3,3-tetrabromo-2-heptanone can be transferred from B. hamifera to its native host algae, as a means of pre-emptive competition. 3. The settlement of native macroalgal propagules and microalgae was strongly inhibited on surfaces coated with 1,1,3,3-tetrabromo-2-heptanone at ecologically relevant concentrations, but there were no effects of adult B. hamifera on growth rates of adults of the six native naturally co-occurring species. The compound was shown to be transferred from B. hamifera to the surface of its native host algae at inhibitory concentrations in both laboratory and field experiments. 4. By inhibiting the settlement of propagules on its thallus and on surrounding surfaces, B. hamifera achieves a competitive advantage over native macroalgae, a finding that parallels previous reports on soil-and litter-mediated allelopathic interactions among vascular plants. Because competition for available substrata in marine benthic systems is intense, the ability to reserve space may be vital for B. hamifera's successful invasion. This is the first example of an allelopathic compound that can be transferred by direct contact from an exotic to a native species, with an active and unaltered function. 5. Synthesis. Our results clearly show that the main secondary metabolite of the invasive red alga B. hamifera has strong allelopathic effects towards native competitors, suggesting that its novel chemical weapon is important for the highly successful invasion of new ranges.
In comparison with terrestrial plants the mechanistic knowledge of chemical defences is poor for marine macroalgae. This restricts our understanding in the chemically mediated interactions that take place between algae and other organisms. Technical advances such as metabolomics, however, enable new approaches towards the characterisation of the chemically mediated interactions of organisms with their environment. We address defence responses in the red alga Gracilaria vermiculophylla using mass spectrometry based metabolomics in combination with bioassays. Being invasive in the north Atlantic this alga is likely to possess chemical defences according to the prediction that well-defended exotics are most likely to become successful invaders in systems dominated by generalist grazers, such as marine macroalgal communities. We investigated the effect of intense herbivore feeding and simulated herbivory by mechanical wounding of the algae. Both processes led to similar changes in the metabolic profile. Feeding experiments with the generalist isopod grazer Idotea baltica showed that mechanical wounding caused a significant increase in grazer resistance. Structure elucidation of the metabolites of which some were up-regulated more than 100 times in the wounded tissue, revealed known and novel eicosanoids as major components. Among these were prostaglandins, hydroxylated fatty acids and arachidonic acid derived conjugated lactones. Bioassays with pure metabolites showed that these eicosanoids are part of the innate defence system of macroalgae, similarly to animal systems. In accordance with an induced defence mechanism application of extracts from wounded tissue caused a significant increase in grazer resistance and the up-regulation of other pathways than in the activated defence. Thus, this study suggests that G. vermiculophylla chemically deters herbivory by two lines of defence, a rapid wound-activated process followed by a slower inducible defence. By unravelling involved pathways using metabolomics this work contributes significantly to the understanding of activated and inducible defences for marine macroalgae.
Diatoms and copepods are main actors in marine food webs. The prey–predator interactions between them affect bloom dynamics, shape marine ecosystems and impact the energy transfer to higher trophic levels. Recently it has been demonstrated that the presence of grazers may affect the diatom prey beyond the direct effect of grazing. Here, we investigated the response of the chain-forming centric diatom Skeletonema marinoi to grazer cues, including changes in morphology, gene expression and metabolic profile. S. marinoi cells were incubated with Calanus finmarchicus or with Centropages typicus and in both cases responded by reducing the chain length, whereas changes in gene expression indicated an activation of stress response, changes in the lipid and nitrogen metabolism, in cell cycle regulation and in frustule formation. Transcripts linked to G protein-coupled receptors and to nitric oxide synthesis were differentially expressed suggesting involvement of these signalling transduction pathways in the response. Downregulation of a lipoxygenase in the transcriptomic data and of its products in the metabolomic data also indicate an involvement of oxylipins. Our data contribute to a better understanding of the gene function in diatoms, providing information on the nature of genes implicated in the interaction with grazers, a crucial process in marine ecosystems.
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