The relevance of marine chemical ecology to plankton and ecosystem function: an emerging field

Abstract

Marine chemical ecology comprises the study of the production and interaction of bioactive molecules affecting organism behavior and function. Here we focus on bioactive compounds and interactions associated with phytoplankton, particularly bloom-forming diatoms, prymnesiophytes and dinoflagellates. Planktonic bioactive metabolites are structurally and functionally diverse and some may have multiple simultaneous functions including roles in chemical defense (antipredator, allelopathic and antibacterial compounds), and/or cell-to-cell signaling (e.g., polyunsaturated aldehydes (PUAs) of diatoms). Among inducible chemical defenses in response to grazing, there is high species-specific variability in the effects on grazers, ranging from severe physical incapacitation and/or death to no apparent physiological response, depending on predator susceptibility and detoxification capability. Most bioactive compounds are present in very low concentrations, in both the producing organism and the surrounding aqueous medium. Furthermore, bioactivity may be subject to synergistic interactions with other natural and anthropogenic environmental toxicants. Most, if not all phycotoxins are classic secondary metabolites, but many other bioactive metabolites are simple molecules derived from primary metabolism (e.g., PUAs in diatoms, dimethylsulfoniopropionate (DMSP) in prymnesiophytes). Producing cells do not seem to suffer physiological impact due to their synthesis. Functional genome sequence data and gene expression analysis will provide insights into regulatory and metabolic pathways in producer organisms, as well as identification of mechanisms of action in target organisms. Understanding chemical ecological responses to environmental triggers and chemically-mediated species interactions will help define crucial chemical and molecular processes that help maintain biodiversity and ecosystem functionality.

Keywords: allelopathy; biotoxins; signal molecule; teratogen; toxic algae.

Figure 1

Pathways of chemical interactions between a species and its environment demonstrated for the dinoflagellate Alexandrium tamarense and methods that are necessary to address this topic. Interactions include: intra- and interspecific competition potentially involving allelopathy particularly within a bloom situation, resistance and resilience to infection, and capacity to deter grazing. All chemical interaction pathways must be considered within the framework of changing abiotic conditions.

Figure 2

Multiple effects of diatom polyunsaturated aldehydes (PUAs): Upper left, anti-predatory (teratogenic) effect on copepods. Abnormal Calanus helgolandicus copepod nauplius hatched from a mother fed with the PUA-producing diatom Skeletonema marinoi. Yellow parts indicate TUNEL-positive apoptotic tissues (from [16]). Upper right, allelopathic (anti-growth) effect on phytoplankton species other than diatoms in culture. Clockwise from upper left: Dunaliella tertiolecta, Tetraselmis suecica, Isochrysis galbana and Amphidinium carterae, after 48 h exposure to PUA, light transmitted (left) and epifluorescence microscopy after DNA staining with SYTOX Green, (from [17]). Lower left, effect on community composition of picoplankton. Flow cytograms represent a natural seawater sample from the Adriatic Sea; left panels are controls, right panels are picophytoplankton (top) and heterotrophic bacteria (bottom), after 24 h inoculation with a mixture of octadienal and heptadienal. Lower right, signaling effect. Sublethal doses of PUA confer resistance to further doses of PUAs. Pre-treated cultures of Phaeodactylum tricornutum, are able to recover after release from PUA exposure compared to non-pretreated cultures (left flask, from [18]).