Chemical ecology of the marine plankton.

Covering: January 2015 through December 2017 This review focuses on recent studies on the chemical ecology of planktonic marine ecosystems, with the objective of presenting a comprehensive overview of new findings in the field in the time period covered. In order to highlight the role of chemically mediated interactions in the marine plankton this review has been organized by ecological concepts starting with intraspecific communication, followed by interspecific interactions (including facilitation and mutualism, host-parasite, allelopathy, and predator-prey), and finally the effects of plankton secondary metabolites on community and ecosystem-wide interactions.

Karenia brevis allelopathy compromises the lipidome, membrane integrity, and photosynthesis of competitors.

The formation, propagation, and maintenance of harmful algal blooms are of interest due to their negative effects on marine life and human health. Some bloom-forming algae utilize allelopathy, the release of compounds that inhibit competitors, to exclude other species dependent on a common pool of limiting resources. Allelopathy is hypothesized to affect bloom dynamics and is well established in the red tide dinoflagellate Karenia brevis. K. brevis typically suppresses competitor growth rather than being acutely toxic to other algae. When we investigated the effects of allelopathy on two competitors, Asterionellopsis glacialis and Thalassiosira pseudonana, using nuclear magnetic resonance (NMR) spectroscopy and mass spectrometry (MS)-based metabolomics, we found that the lipidomes of both species were significantly altered. However, A. glacialis maintained a more robust metabolism in response to K. brevis allelopathy whereas T. pseudonana exhibited significant alterations in lipid synthesis, cell membrane integrity, and photosynthesis. Membrane-associated lipids were significantly suppressed for T. pseudonana exposed to allelopathy such that membranes of living cells became permeable. K. brevis allelopathy appears to target lipid biosynthesis affecting multiple physiological pathways suggesting that exuded compounds have the ability to significantly alter competitor physiology, giving K. brevis an edge over sensitive species.

Variable allelopathy among phytoplankton reflected in red tide metabolome.

Harmful algae are known to utilize allelopathy, the release of compounds that inhibit competitors, as a form of interference competition. Competitor responses to allelopathy are species-specific and allelopathic potency of producing algae is variable. In the current study, the biological variability in allelopathic potency was mapped to the underlying chemical variation in the exuded metabolomes of five genetic strains of the red tide dinoflagellate Karenia brevis using 1H nuclear magnetic resonance (NMR) spectroscopy. The impacts of K. brevis allelopathy on growth of a model competitor, Asterionellopsis glacialis, ranged from strongly inhibitory to negligible to strongly stimulatory. Unique metabolomes of K. brevis were visualized as chemical fingerprints, suggesting three distinct metabolic modalities - allelopathic, non-allelopathic, and stimulatory - with each modality distinguished from the others by different concentrations of several metabolites. Allelopathic K. brevis was characterized by enhanced concentrations of fatty acid-derived lipids and aromatic or other polyunsaturated compounds, relative to less allelopathic K. brevis. These findings point to a previously untapped source of information in the study of allelopathy: the chemical variability of phytoplankton, which has been underutilized in the study of bloom dynamics and plankton chemical ecology.

Enhancement of antibiotic activity against multidrug-resistant bacteria by the efflux pump inhibitor 3,4-dibromopyrrole-2,5-dione isolated from a Pseudoalteromonas sp.

Members of the resistance nodulation cell division (RND) of efflux pumps play essential roles in multidrug resistance (MDR) in Gram-negative bacteria. Here, we describe the search for new small molecules from marine microbial extracts to block efflux and thus restore antibiotic susceptibility in MDR bacterial strains. We report the isolation of 3,4-dibromopyrrole-2,5-dione (1), an inhibitor of RND transporters, from Enterobacteriaceae and Pseudomonas aeruginosa, from the marine bacterium Pseudoalteromonas piscicida. 3,4-Dibromopyrrole-2,5-dione decreased the minimum inhibitory concentrations (MICs) of two fluoroquinolones, an aminoglycoside, a macrolide, a beta-lactam, tetracycline, and chloramphenicol between 2- and 16-fold in strains overexpressing three archetype RND transporters (AcrAB-TolC, MexAB-OprM, and MexXY-OprM). 3,4-Dibromopyrrole-2,5-dione also increased the intracellular accumulation of Hoechst 33342 in wild-type but not in transporter-deficient strains and prevented H33342 efflux (IC50 = 0.79 µg/mL or 3 µM), a hallmark of efflux pump inhibitor (EPI) functionality. A metabolomic survey of 36 Pseudoalteromonas isolates mapped the presence of primarily brominated metabolites only within the P. piscicida phylogenetic clade, where a majority of antibiotic activity was also observed, suggesting a link between halogenation and enhanced secondary metabolite biosynthetic potential. In sum, 3,4-dibromopyrrole-2,5-dione is a potent EPI and deserves further attention as an adjuvant to enhance the effectiveness of existing antibiotics.

Metabolomics and proteomics reveal impacts of chemically mediated competition on marine plankton.

Competition is a major force structuring marine planktonic communities. The release of compounds that inhibit competitors, a process known as allelopathy, may play a role in the maintenance of large blooms of the red-tide dinoflagellate Karenia brevis, which produces potent neurotoxins that negatively impact coastal marine ecosystems. K. brevis is variably allelopathic to multiple competitors, typically causing sublethal suppression of growth. We used metabolomic and proteomic analyses to investigate the role of chemically mediated ecological interactions between K. brevis and two diatom competitors, Asterionellopsis glacialis and Thalassiosira pseudonana. The impact of K. brevis allelopathy on competitor physiology was reflected in the metabolomes and expressed proteomes of both diatoms, although the diatom that co-occurs with K. brevis blooms (A. glacialis) exhibited more robust metabolism in response to K. brevis. The observed partial resistance of A. glacialis to allelopathy may be a result of its frequent exposure to K. brevis blooms in the Gulf of Mexico. For the more sensitive diatom, T. pseudonana, which may not have had opportunity to evolve resistance to K. brevis, allelopathy disrupted energy metabolism and impeded cellular protection mechanisms including altered cell membrane components, inhibited osmoregulation, and increased oxidative stress. Allelopathic compounds appear to target multiple physiological pathways in sensitive competitors, demonstrating that chemical cues in the plankton have the potential to alter large-scale ecosystem processes including primary production and nutrient cycling.

Chemical ecology of the marine plankton.

This review summarizes recent work in the chemical ecology of pelagic marine ecosystems. In order to provide a comprehensive overview of advances in the field over the period covered, we have organized this review by ecological interaction type beginning with intraspecific interactions, then interspecific interactions (including mutualism, parasitism, competition, and predation), and finally community- and ecosystem-wide interactions.