The chemical defense ecology of marine unicellular plankton: constraints, mechanisms, and impacts

“The oceans are microbially dominated ecosystems (Sherr and Sherr, 1991), and although marine plankton constitute less than 0.5% of global biomass, they contribute nearly 50% of global net primary production (Field et al., 1998).”

“Given body lengths of less than 200 ␮m, most microbes thus operate in a viscosity-dominated realm (Re Ͻ Ͻ 1) where fluid motions are completely reversible in time (Purcell, 1977).”

“This reign led to the evolution of vast genetic diversity (Barns and Nierzwicki-Bauer , 1997; Pace, 1997); for example, prokaryotic (bacterial and archaeal) metabolic pathways affect all major biogeochemical cycles and led to the oxidation of the Earth's surface (Falkowski and Raven, 1997; Fenchel…”

“But although the behavioral and chemosensory abilities of unicellular microbes have been known for nearly a century (Jennings, 1906; Schaeffer, 1910) and the general physical, chemical, and molecular regulation of microbial signaling and behavior have been recognized for decades (Carlile, 1975; Berg and Purcell, 1977;…”

“Grazers encounter prey at a rate of E ϭ ␲/3 S p N p (3v g 2 ϩ v p 2 )/v g where N p is the prey density and v the speeds (Gerritsen and Strickler, 1977); the frequency of encounters thus increases with relative speed (prey speeds are often small compared to grazers).”

“DMSP is produced by many marine algae and is especially prominent in haptophytes and dinoflagellates (Keller et al., 1989b).”

“3a), a zone termed the phycosphere (Sieburth, 1968; Bell and Mitchell, 1972), which may serve to advertise the presence of the prey.”

“…from the macroscopic world to understanding interactions among microbes, through concepts such as coevolution of predator and prey (Bernays, 1998; Lima, 1998), functional defense groups or defense guilds (Atsatt and O'Dowd, 1976), and complex multitrophic interactions (De Moraes et al., 1998).”

“…chemical effects on zooplankton predators Cyanobacteria spp. Copepods, daphnids, cladocerans, rotifers AV, AT, FI, GR DeMott and Moxter, 1991; DeMott et al., 1991; Kirk and Gilbert, 1992; Haney et al., 1995 Bacillariophyceae Phaeodactylum, Thalassiosira Copepods FI Shaw et al., 1995…”

“Beyond, turbulence at the millimeter scale also dissipates microzone gradients, although the impact is still controversial (Mitchell et al., 1985; Alldredge and Cohen, 1987).”

“The DMSP cleavage reaction was hypothesized to be compartmented (Wolfe et al., 1997).”

“The rich variety of oligosaccharide structures that can be formed with a limited set of oligomers and glycosidic linkages probably contributes to their utility for protein recognition (Sharon and Lis, 1993; Lowe, 1994).”

“Finally, DMS produced from DMSP sequestered at higher trophic levels may act as a chemoattractant for vertebrates such as procellariiform seabirds (Nevitt et al., 1995; Nevitt, 1998, 2000), helping them to locate food patches.”

“…studied in vertebrate systems, nearly all probably originated in unicellular microbes (Carlile , 1975; Kurjan and Taylor, 1993; Csaba and Müller, 1996) and have been studied in detail for a few protozoan models (Paramecium, Tetrahymena, Dictyostelium [Loomis , 1982; Gall, 1986; Devreotes, 1989]).”

“(Much consideration has focused on detection of these microzones by bacteria, whose physical and physiological constraints and mechanisms may be very different from those of larger protozoa [Bowenet al.,1993; Mitchellet al.,1996; Blackburn et al., 1998]).”

“Although polar compounds have relatively low membrane permeabilities, Bjørnson (1988) has suggested that small cells with large surface-to-volume ratios may unavoidably " leak " metabolites at potentially high rates.”

“Metazoan grazers may regurgitate toxic prey (Huntley et al., 1986), but expelled cells appear to be damaged and suffer lower growth rates.”

“Particle capture is determined by particle size, the shear fields produced by feeding currents, and capture structures (Fenchel, 1980; Jonsson, 1986; Monger and Landry, 1991).”

“Recent evidence on bacterivore grazers suggests that predation can cause major shifts in food abundance and taxa (Hahn and Höfle, 1998; Jürgens et al., 1999).”

“non-self” discrimination and have been hypothesized to be precursors of vertebrate immune systems (Burnet, 1971; Popescu and Misevic, 1997).”

“Aggregates of cells relay waves of cAMP to control reproductive development (Nanjundiah, 1973; Devreotes, 1982).”

“…in a few minutes following ingestion, times typical for food vacuole formation, and thus produce concentrated acrylate inside protist food vacuoles at levels (ca. 70 mM) that have been shown to be toxic or have antimicrobial activity (Sieburth, 1960, 1961; Thijsse, 1964; Bringmann and Kühn, 1980).”

“However, little has been done to apply models of organismal behavior and ecology from the macroscopic world to understanding interactions among microbes, through concepts such as coevolution of predator and prey (Bernays, 1998; Lima, 1998), functional defense groups or defense guilds (Atsatt and O’Dowd, 1976), and com…”

“But although the behavioral and chemosensory abilities of unicellular microbes have been known for nearly a century (Jennings, 1906; Schaeffer, 1910) and the general physical, chemical, and molecular regulation of microbial signaling and behavior have been recognized for decades (Carlile, 1975; Berg and Purcell, 1977;…”

“…in a few minutes following ingestion, times typical for food vacuole formation, and thus produce concentrated acrylate inside protist food vacuoles at levels (ca. 70 mM) that have been shown to be toxic or have antimicrobial activity (Sieburth, 1960, 1961; Thijsse, 1964; Bringmann and Kühn, 1980).”

“In all strains, although DMSP lyase is a constitutive enzyme, cleavage— deduced from DMS production— does not appear to occur in healthy growing cells (Wolfe and Steinke, 1996; Fig.”

“Although typically studied in vertebrate systems, nearly all probably originated in unicellular microbes (Carlile , 1975; Kurjan and Taylor, 1993; Csaba and Müller, 1996) and have been studied in detail for a few protozoan models (Paramecium, Tetrahymena, Dictyostelium [Loomis , 1982; Gall, 1986; Devreotes, 1989]).”

“Finally, DMS produced from DMSP sequestered at higher trophic levels may act as a chemoattractant for vertebrates such as procellariiform seabirds (Nevitt et al., 1995; Nevitt, 1998, 2000), helping them to locate food patches.”

“Only recently has a first report even demonstrated the production of a compartmented mixing reaction in a phospholipid bilayer system similar in size to a eukaryotic nanoplankter cell (Chiu et al., 1999).”

“Constitutive toxins, already discussed, may incapacitate grazers (Hansen, 1989; Hansen et al., 1992).”

“…copepods AV Admiraal et al., 1986; Estep et al., 1990; Hansen et al., 1990 Chrysochromulina Ciliates, copepods AT, GR Carlsson et al., 1990; Nielsen et al., 1990; Turiff et al., 1995 Dinophyceae Alexandrium Ciliates, copepods AT, GR, AV Hansen, 1989; Bagøien et al., 1996; Teegarden and…”

“Examples of such systems in macroalgae (Paul and van Alstyne, 1992) and vascular plants include some of the best-known plant defense systems, including hydrolysis of glucosinolates (Newman et al., 1992) and cyanogenesis (Jones et al., 1978).”

“They are also critical trophic links between their prey and larger metazoan grazers (Fessenden and Cowles, 1994), forming the base of the marine food web (Pomeroy, 1992).”

“In vascular plants, vacuoles often serve as compartments to concentrate toxins (Wagner, 1978; Wink, 1997).”

“Many marine protozoan grazers are known to selectively ingest or reject particular prey [Table 3, (Stoecker et al., 1986; Taniguchi and Takeda, 1988; Verity, 1991; Stoecker et al., 1995; Strom and Loukos , 1998)], and prey preferences differ among predators (Rapport et al., 1972; Hansen et al.,…”

“Such cues are not necessarily limited to highly toxic cells or compounds (Stoecker et al., 1981; Rassoulzadegan and Fenaux, 1984; DeMott, 1986; Cowles et al., 1988; Sanders, 1988; Van Donk et al., 1997).”

“It is highly nontoxic and is an excellent compatible osmolyte (Dickson and Kirst, 1987).”

“…release by mast cells following inflammation (Gomperts et al., 1994), neutrophil phagocytosis (Suzaki et al., 1997), sperm acrosomal and egg activation reactions during fertilization (Jaffe, 1985; Tilney, 1985), and neurotransmitter release at nerve synapses (von Gersdorff and Matthews, 1994).”

“Carr (1988) pointed out that many biochemical intermediates , such as amino acids, nucleic acids, and fatty acids, and their derivatives, are often in the high millimolar range inside cells.”

“All eukaryotic cells have highly compartmented organelles and many produce highly toxic metabolites (Hall and Strichartz, 1990; Plumley, 1997).”

“Particle capture is determined by particle size, the shear fields produced by feeding currents, and capture structures (Fenchel, 1980; Jonsson, 1986; Monger and Landry, 1991).”

“DLs have a mildly acidic pH optimum (Steinke et al., 1998) and retain significant activity even at pH 4 – 6, the probable range during formation of food vacuoles.”

“…and coevolution are only crudely known, and even the species concept is poorly defined for microbes that divide both sexually and asexually (Manhart and McCourt, 1992; Wood and Leatham, 1992; Colwell et al., 1995) and where horizontal gene transfer appears rapid and rampant (Dahlberg et al., 1998).”

“Protozoa also produce hormone molecules (LeRoith et al., 1982) that may interact with cell receptors (Marino and Wood, 1993).”

“Beyond, turbulence at the millimeter scale also dissipates microzone gradients, although the impact is still controversial (Mitchell et al., 1985; Alldredge and Cohen, 1987).”

“For example, tetrodotoxin , the nerve-impulse inhibitor produced by the pufferfish Fugu, also functions as a mating pheromone (Matsumura, 1995).”

“Viral lysis of the DL-containing haptophyte Phaeocystis pouchetii also initiates DMS production (Malin et al., 1998).”

“It may also serve for transmethylation reactions (Ishida and Kadota, 1968) or act as a cryoprotectant (Karsten et al., 1996).”

“…et al., 1990; Nielsen et al., 1990; Turiff et al., 1995 Dinophyceae Alexandrium Ciliates, copepods AT, GR, AV Hansen, 1989; Bagøien et al., 1996; Teegarden and Cembella, 1996 Gymnodinium Copepods AT, GR, AV Fiedler, 1982; Bagøien et al., 1996 Dinophysis Copepods AV Carlsson et al., 1995…”

“…and coevolution are only crudely known, and even the species concept is poorly defined for microbes that divide both sexually and asexually (Manhart and McCourt, 1992; Wood and Leatham, 1992; Colwell et al., 1995) and where horizontal gene transfer appears rapid and rampant (Dahlberg et al., 1998).”

“DMSP is also a close chemical analog of quaternary or tertiary amines known to act as alarm cues in metazoans, including anthopleurine (Howe and Sheikh, 1975) and homarine (McClintock et al.”

“Constitutive toxins, already discussed, may incapacitate grazers (Hansen, 1989; Hansen et al., 1992).”

“For example, genetic variation is just beginning to be known within phytoplankton classes or species (Costas et al., 1995; Medlin et al., 1996; Larsen and Medlin, 1997; Scholin, 1998), much less within natural populations (Brand, 1989) or blooms (Gallagher, 1998)—and even less is known of marine protozoa (Lim et al.”

“DMSP and analogs have been found localized in the cytoplasm or vacuoles of other microorganisms (Schlenk et al., 1970) and vascular plants (Hall et al., 1978; Leigh et al., 1981; Matoh et al., 1987), and algal DLs are membranebound enzymes (de Souza et al., 1996).”

“Long-range chemical signals may act as repellents, preventing the initiation of feeding by causing the predator to orient away from a potential prey; closer-range signals may act as deterrents, repelling predators that have attempted to feed (Lindstedt, 1971).”

“, 1998) but probably contributes to their success (Buskey and Hyatt, 1995; Buskey et al., 1997).”

“…et al., 1986; Estep et al., 1990; Hansen et al., 1990 Chrysochromulina Ciliates, copepods AT, GR Carlsson et al., 1990; Nielsen et al., 1990; Turiff et al., 1995 Dinophyceae Alexandrium Ciliates, copepods AT, GR, AV Hansen, 1989; Bagøien et al., 1996; Teegarden and Cembella, 1996…”

“, 1998) but probably contributes to their success (Buskey and Hyatt, 1995; Buskey et al., 1997).”

“Just as microbial sensory systems most likely evolved into those of multicellular organisms (Carlile, 1975; Anderson , 1989; Carr, 1989), conserved microbial behaviors and organismal interactions may be the basis of those we know so well from " higher " animals and plants.”

“…in a few minutes following ingestion, times typical for food vacuole formation, and thus produce concentrated acrylate inside protist food vacuoles at levels (ca. 70 mM) that have been shown to be toxic or have antimicrobial activity (Sieburth, 1960, 1961; Thijsse, 1964; Bringmann and Kühn, 1980).”

“Although acute responses that result from ingestion of a small number of highly toxic prey (death, reduced growth or reproductive rates) have been noted in some laboratory studies (Sykes and Huntley, 1987; Hansen, 1995), it is not clear how these operate in natural populations .”

“…selectively ingest or reject particular prey [Table 3, (Stoecker et al., 1986; Taniguchi and Takeda, 1988; Verity, 1991; Stoecker et al., 1995; Strom and Loukos , 1998)], and prey preferences differ among predators (Rapport et al., 1972; Hansen et al., 1996; Buskey, 1997; Strom and Loukos, 1998).”

“Recent evidence on bacterivore grazers suggests that predation can cause major shifts in food abundance and taxa (Hahn and Höfle, 1998; Jürgens et al., 1999).”

“Just as microbial sensory systems most likely evolved into those of multicellular organisms (Carlile, 1975; Anderson , 1989; Carr, 1989), conserved microbial behaviors and organismal interactions may be the basis of those we know so well from " higher " animals and plants.”

“Ciliate extrusomes probably play multiple roles: Paramecium trichocysts aid in both food capture and escape from predation (Wesenberg and Antipa, 1970; Harumoto and Miyake, 1991).”

“…Alexandrium Ciliates, copepods AT, GR, AV Hansen, 1989; Bagøien et al., 1996; Teegarden and Cembella, 1996 Gymnodinium Copepods AT, GR, AV Fiedler, 1982; Bagøien et al., 1996 Dinophysis Copepods AV Carlsson et al., 1995 Chrysophyceae Olisthodiscus Tintinnids, rotifers AT, FI, GR Verity…”

“The reaction functions for defense against metazoan grazers, acting as a " burglar alarm " to attract predators of the grazers (Esaias and Curl Jr., 1972; White, 1979; Buskey and Swift, 1985; Mensinger and Case, 1992; Abrahams and Townsend, 1993).”

“(Much consideration has focused on detection of these microzones by bacteria, whose physical and physiological constraints and mechanisms may be very different from those of larger protozoa [Bowen et al., 1993; Mitchell et al., 1996; Blackburn et al., 1998]).”

“Formic acid, a close analog of acrylic acid, is a well-known alarm and defense signal in the formacine ants from which it was first isolated (Löfqvist, 1976).”

“Whether protozoan grazers can use gradients to locate individual prey cells is less certain (Jackson, 1987).”

“…from reacting by attachment to a luciferin-binding protein; mechanical distortion of the cell plasma membrane generates an electrical action potential that traverses the cell in less than a microsecond (Nicolas et al., 1975), creating an influx of protons that releases luciferin for oxidation.”

“All eukaryotic cells have highly compartmented organelles and many produce highly toxic metabolites (Hall and Strichartz, 1990; Plumley, 1997).”

“…toxins may function as grazing deterrents (Turner and Tester, 1997; Turner et al., 1998) or allelopathic compounds (Dakshini and Dakshini, 1994; Subba Rao et al., 1995; Windust et al., 1996; Sugg and VanDolah, 1999), evidence is contradictory, and their ecological functions are poorly understood.”

“Measurements of in situ DL activity and of grazing rates on algal populations (Stefels et al., 1995) will be necessary to assess the deterrent role of this reaction in bloom formation and maintenance.”

“Compartmentation may reduce autotoxicity; saxitoxins in Gonyaulax and okadaic acid in Prorocentrum localize to chloroplasts (Anderson and Cheng, 1988; Zhou and Fritz, 1994).”

“Particle capture is determined by particle size, the shear fields produced by feeding currents, and capture structures (Fenchel, 1980; Jonsson, 1986; Monger and Landry, 1991).”

“, 1995; Strom and Loukos, 1998)], and prey preferences differ among predators (Rapport et al., 1972; Hansen et al., 1996; Buskey, 1997; Strom and Loukos, 1998).”

“…Cyanobacteria spp. Copepods, daphnids, cladocerans, rotifers AV, AT, FI, GR DeMott and Moxter, 1991; DeMott et al., 1991; Kirk and Gilbert, 1992; Haney et al., 1995 Bacillariophyceae Phaeodactylum, Thalassiosira Copepods FI Shaw et al., 1995 Prymnesiophyceae Emiliania Dinoflagellates, ciliates…”

“Many marine protozoan grazers are known to selectively ingest or reject particular prey [Table 3, (Stoecker et al., 1986; Taniguchi and Takeda, 1988; Verity, 1991; Stoecker et al., 1995; Strom and Loukos , 1998)], and prey preferences differ among predators (Rapport et al., 1972; Hansen et al.,…”

“…toxins may function as grazing deterrents (Turner and Tester, 1997; Turner et al., 1998) or allelopathic compounds (Dakshini and Dakshini, 1994; Subba Rao et al., 1995; Windust et al., 1996; Sugg and VanDolah, 1999), evidence is contradictory, and their ecological functions are poorly understood.”

“, 1997) or have mitogenic activity (Vallesi et al., 1995).”

“The oceans are microbially dominated ecosystems (Sherr and Sherr, 1991), and although marine plankton constitute less than 0.”

“non-self” discrimination and have been hypothesized to be precursors of vertebrate immune systems (Burnet, 1971; Popescu and Misevic, 1997).”

“Community-level patterns such as succession, niche occupation, and coevolution are only crudely known, and even the species concept is poorly defined for microbes that divide both sexually and asexually (Manhart and McCourt, 1992; Wood and Leatham, 1992; Colwell et al., 1995) and where horizontal gene transfer appears…”

“, 1996; Larsen and Medlin, 1997; Scholin, 1998), much less within natural populations (Brand, 1989) or blooms (Gallagher, 1998)—and even less is known of marine protozoa (Lim et al., 1996).”

“Ciliate extrusomes probably play multiple roles: Paramecium trichocysts aid in both food capture and escape from predation (Wesenberg and Antipa, 1970; Harumoto and Miyake, 1991).”

“Recent calculations suggest that microbial chemosensory adaptations to diffusive environments may be even more sophisticated than previously thought (Dusenbery, 1998).”

“The reaction functions for defense against metazoan grazers, acting as a " burglar alarm " to attract predators of the grazers (Esaias and Curl Jr., 1972; White, 1979; Buskey and Swift, 1985; Mensinger and Case, 1992; Abrahams and Townsend, 1993).”

“The reaction functions for defense against metazoan grazers, acting as a " burglar alarm " to attract predators of the grazers (Esaias and Curl Jr., 1972; White, 1979; Buskey and Swift, 1985; Mensinger and Case, 1992; Abrahams and Townsend, 1993).”

“…Steinke, 1996; Wolfe et al., 1997; Strom and Wolfe, unpublished data Phaeocystis Ciliates, copepods AV Admiraal et al., 1986; Estep et al., 1990; Hansen et al., 1990 Chrysochromulina Ciliates, copepods AT, GR Carlsson et al., 1990; Nielsen et al., 1990; Turiff et al., 1995 Dinophyceae…”

“…pouchetii, a bloom-forming haptophyte closely related to Emiliania, has a colonial life stage that forms large (1-mm) colonies concentrated in spherical shells of polysaccharide mucus (van Rijssel et al., 1997) that are critical to its widespread ecological success (Lancelot and Rosseau, 1994).”

“The reaction functions for defense against metazoan grazers, acting as a " burglar alarm " to attract predators of the grazers (Esaias and Curl Jr., 1972; White, 1979; Buskey and Swift, 1985; Mensinger and Case, 1992; Abrahams and Townsend, 1993).”

“Coastal Texas has experienced a " brown tide " of the chrysophyte Aureococcus for over five years, while an E. huxleyi bloom in the Bering Sea has persisted for two years (Vance et al., 1998); both blooms have had dramatic impacts on regional food webs.”

“…to gradients of dissolved cues and specific prey strains was filmed and analyzed by computer-aided motion analysis (Sjoblad and Mitchell, 1979; Zimmer-Faust et al., 1996), and preliminary observations suggest that Amphidinium's motions are greatly inhibited by acrylate (R. Zimmer , pers.…”

“(Much consideration has focused on detection of these microzones by bacteria, whose physical and physiological constraints and mechanisms may be very different from those of larger protozoa [Bowen et al., 1993; Mitchell et al., 1996; Blackburn et al., 1998]).”

“…Ciliates, copepods AT, GR, AV Hansen, 1989; Bagøien et al., 1996; Teegarden and Cembella, 1996 Gymnodinium Copepods AT, GR, AV Fiedler, 1982; Bagøien et al., 1996 Dinophysis Copepods AV Carlsson et al., 1995 Chrysophyceae Olisthodiscus Tintinnids, rotifers AT, FI, GR Verity and Stoecker,…”

“…in a few minutes following ingestion, times typical for food vacuole formation, and thus produce concentrated acrylate inside protist food vacuoles at levels (ca. 70 mM) that have been shown to be toxic or have antimicrobial activity (Sieburth, 1960, 1961; Thijsse, 1964; Bringmann and Kühn, 1980).”

“Peptide signals and surface receptors occur widely in protozoa (LeRoith et al., 1982; Freiburg, 1993; Luporini et al., 1995; Ortenzi and Luporini, 1995), and many protozoa have receptors for vertebrate hormones (reviewed above).”

“Such cues are not necessarily limited to highly toxic cells or compounds (Stoecker et al., 1981; Rassoulzadegan and Fenaux, 1984; DeMott, 1986; Cowles et al., 1988; Sanders, 1988; Van Donk et al., 1997).”

“…release by mast cells following inflammation (Gomperts et al., 1994), neutrophil phagocytosis (Suzaki et al., 1997), sperm acrosomal and egg activation reactions during fertilization (Jaffe, 1985; Tilney, 1985), and neurotransmitter release at nerve synapses (von Gersdorff and Matthews, 1994).”

“Ca 2ϩ and cyclic AMP are important molecules in mediating signal transduction and may also act externally to the cell (O'Day, 1990; Louis et al., 1993).”

“…modes are astonishingly diverse and fluid; it is estimated that a large fraction of photoautotrophic plankton can simultaneously use heterotrophic nutrition (mixotrophy), either by uptake of dissolved organic solutes or by ingestion of organic particles (Boraas et al., 1988; Stoecker, 1992).”

“However, complete lysis may not be necessary: merely sparging water containing Phaeocystis colonies activates DMS production (Wolfe et al., 2000).”

“Phagocytosis can be mediated by prey-excreted or prey-surface molecules (Rabinovitch and De Stefano , 1971; Brown et al., 1975; Vogel et al., 1980; Wright and Silverstein, 1986; Kiersnowska et al., 1988).”

“But although the behavioral and chemosensory abilities of unicellular microbes have been known for nearly a century (Jennings, 1906; Schaeffer, 1910) and the general physical, chemical, and molecular regulation of microbial signaling and behavior have been recognized for decades (Carlile, 1975; Berg and Purcell, 1977;…”

“…1989; Bagøien et al., 1996; Teegarden and Cembella, 1996 Gymnodinium Copepods AT, GR, AV Fiedler, 1982; Bagøien et al., 1996 Dinophysis Copepods AV Carlsson et al., 1995 Chrysophyceae Olisthodiscus Tintinnids, rotifers AT, FI, GR Verity and Stoecker, 1982; Egloff, 1986 * AT ϭ Acute Toxicity, FI…”

“Trimethylamine, a volatile nitrogen analog of DMS produced microbially as a decay byproduct, appears to initiate vertical migration in freshwater daphnids (Boriss et al., 1999) as a defense against predatory fish (Nesbitt et al., 1996).”

“Little is known about peptide-mediated signaling among marine planktonic protists, but peptides probably function universally as chemocues in the marine environment (Rittschof, 1990; Decho et al., 1998).”

“In vascular plants, vacuoles often serve as compartments to concentrate toxins (Wagner, 1978; Wink, 1997).”

“For example, genetic variation is just beginning to be known within phytoplankton classes or species (Costas et al., 1995; Medlin et al., 1996; Larsen and Medlin, 1997; Scholin, 1998), much less within natural populations (Brand, 1989) or blooms (Gallagher, 1998)—and even less is known of marine…”

“Although the feeding mechanisms of suspension (filter) feeders strongly determine the size spectrum of particles that they can capture, many also appear to discriminate between similarly sized particles with different chemical characteristics (Stoecker, 1988; Verity, 1991).”

“For example, genetic variation is just beginning to be known within phytoplankton classes or species (Costas et al., 1995; Medlin et al., 1996; Larsen and Medlin, 1997; Scholin, 1998), much less within natural populations (Brand, 1989) or blooms (Gallagher, 1998)—and even less is known of marine protozoa (Lim et al.”

“Signals received at the cell surface are conveyed intracellularly by several major mechanisms, including ion-channel-linked receptors, G protein-linked receptors and enzyme-linked receptors (Van Houten, 1994).”

“Ciliated cells are covered in an array of shorter cilia (5 hair); metachronous depolarization waves passing over the ciliate cell cause coordinated ciliary movement for motion (Hennessey, 1989; Clark et al., 1993).”

“There is increasing evidence that prey selection is based on chemical cues determined during prey capture, handling, or ingestion, leading to rejection following prey capture (e.g., Taniguchi and Takeda, 1988; Stoecker et al., 1995), but these cues are little understood at present.”

“Trimethylamine, a volatile nitrogen analog of DMS produced microbially as a decay byproduct, appears to initiate vertical migration in freshwater daphnids (Boriss et al., 1999) as a defense against predatory fish (Nesbitt et al., 1996).”

“The extent to which genetic diversity occurs among clonal plankton is just beginning to be known (Oppen et al., 1996).”

“, 1995; Strom and Loukos, 1998)], and prey preferences differ among predators (Rapport et al., 1972; Hansen et al., 1996; Buskey, 1997; Strom and Loukos, 1998).”

“2 DMSP lyase mode of action: LA ϭ lysis-activated; EX ϭ extracellu- lar. cell-surface DL (Stefels and van Boekel, 1993) and may pump DMSP across the cell membrane and cleave it externally , where the acrylate produced becomes highly concentrated at the colony surface (Noordkamp et al., 1998).”

“Even the static microscale distributions of microbial populations are only beginning to be visualized (Müller-Niklas et al., 1996; Krembs et al., 1998); their chemical interactions are a still greater challenge.”

“Nematocysts and toxicysts are used to secure and immobilize prey (Wesenberg and Antipa, 1970), but the role of trichocysts has long been a puzzle (Mast, 1906; Haacke-Bell et al., 1990).”

“One is mechanically stimulated bioluminescence , produced by many marine dinoflagellates (e.g., Pyrocystis, Pyrodinium, Gonyaulax, or Noctiluca [Johnson et al., 1985; Anderson et al., 1988]).”

“…et al., 1996 Dinophysis Copepods AV Carlsson et al., 1995 Chrysophyceae Olisthodiscus Tintinnids, rotifers AT, FI, GR Verity and Stoecker, 1982; Egloff, 1986 * AT ϭ Acute Toxicity, FI ϭ Feeding Inhibition, AV ϭ Avoidance, GR ϭ Growth Reduction. refuge for prey populations (Strom and Loukos,…”

“A beautiful example is the peptide " A-factor " excreted by Amoeba proteus, which inhibits phagocytosis and is used for self recognition to avoid cannibalism (Kusch, 1999).”

“·2), widespread in marine microalgae, can be broken down into a gas, DMS (dimethylsulfide), and acrylate, which may serve to repel grazers such as copepods (Wolfe, 2000; Van Alstyne and Houser, 2003).”

“Intricacies of predator– prey relationships, e.g., by chemical communication, remain to be discovered (Wolfe 2000).”

“In other species, toxins are secreted into the media by the algae to avoid negative interactions [70].”

“Such a mechanism could also be partly responsible for the significantly reduced feeding levels on high-lyase phytoplankton by other microzooplankton taxa (Strom et al. 2003a; Wolfe 2000).”

“In contrast to benthic and terrestrial realms, the study of grazer defences in the plankton is in its infanc”

“1987) and have been reported to discriminate between similar-sized prey for some unknown chemical reason (Stoecker et al. 1986; Sanders 1988; Verity 1991; Jürgens & DeMott 1995; Christaki et al. 1998; Wolfe 2000).”

“Chemical defences in plankton have not received much attention (Wolfe 2000), and SO plankton even less.”

“Alternatively, single-celled cyanobacteria may be ingested more readily than filamentous algae, because of grazer gape limitations (Gliwicz and Siedlar 1980), and these smaller prey may contain undescribed secondary metabolites that function as toxins only when consumed (Wolfe 2000).”

“It is striking that the activated defences of phytoplankton that have been discovered so far depend on primary metabolic processes [ 41 ,63].”

“The acrylic acid in seawater may act as a chemical deterrent against protozoan grazers (Wolfe et a!., 1997; Wolfe, 2000).”

“The chemical defense ecology of marine unicellular plankton was recently reviewed by Wolfe (2000).”

“DMSP cleavage activity varies between strains and responds to several environmental cues such as light, and shear ( Wolfe, 2000; Wolfe et al., 2002) and E. huxleyi strains with high DMSP-lyase activity have also been shown to be resistant to virus infection (Schroeder et al., 2002).”

“Production of molecules with multiple functions (allelopathy, defence) is an efficient competitive strategy (Wolfe 2000).”

“Increased toxin production could therefore provide a benefit by reducing the grazing pressure on nearby genetically identical cells (Wolfe 2000).”

“huxleyi strains DMSP High-activity strains rejected or avoided in mixed diet; grazing rates reduced by 79% in sole diet relative to low-DMSP prey – Wolfe, Steinke & Kirst (1997)”

“However, there will be a benefit to the population of genetically closely related or identical diatoms present in the water column during a bloom period of the diatoms because the pool of grazers will be reduced (Wolfe, 2000).”

“Although some aquatic microorganisms can respond to chemical signals through movement (Wolfe 2000), the ciliates in our experiment could not escape the effect of A. tamarense exudates.”

“The synthesis of toxins, which contribute to the observed vertebrate toxicity of cyanobacterial and algal blooms and are constitutively present in the cells, has been shown to be responsible for reduced grazing (Wolfe 2000).”

“Other explanations for the production and release of allelopathic agents include defense against predators (24) and maybe parasites, where allelopathic effects may occur at high cell densities as a side effect.”

“The best documented case of chemical deterrence of protist grazing is that by dimethylsulfoniopropionate-producing algae, e.g. the coccolithophorid Emiliania huxleyi (Wolfe 2000, Strom et al. 2003, Strom 2008).”

“DMSP is considered to be nontoxic and serves as an excellent compatible osmolyte (Dickson and Kirst, 1987) and may additionally act as a cryoprotectant (Karsten et al., 1996).”

“Most investigations of chemically mediated interactions in the plankton have focused either on algal-algal interactions (traditionally defined as allelopathy, see Legrand et al., 2003) or on grazer inhibitiondeterrence properties of algal–borne secondary metabolites (Wolfe, 2000).”

“Nevertheless, because phytoplankton generally exist under flow regimes dominated by viscous rather than turbulent forces (Wolfe 2000), the release of noxious substances that kill or repel competitors to maximize one’s access to essential nutrients and light remains a viable and undertested…”

“It is probable that considerably higher concentrations would, at least transiently, characterize the region near a phytoplankton cell (Wolfe 2000).”

“In comparison, DMSP is particularly enriched in marine flagellates, including several prymnesiophytes (Chrysochromulina, Phaeocystis and Emiliania) and dinoflagellates (Alexandrium, Amphidinium, Gonyaulax and Gymnodinium) [44].”

“Indeed the only case of an HR known so far in an algal system (albeit only microscopically, without any mechanistic details) is from the diatom Asterionella formosa infected by Rhizophydium planktonicum (Canter and Jaworski, 1979; Wolfe, 2000).”

“They may select between seemingly similar prey, even of the same species, clone or growth stage, on the basis of biochemical composition (Houde and Roman 1987; Wolfe 2000; Dutz and Koski 2006; Long and Hay 2006).”

“For example, model calculations on the distribution of DMS on the surface of small cells after brief (5 s) release of DMS indicate concentrations of 15 mmol L21 and 1 mmol L21 DMS at distances from the organism of 1 mm and 20 mm, respectively (Wolfe 2000).”

“, 2010; Aktories, 2011), protists (Sykes & Huntley, 1987; Turner, Tester & Hansen, 1998; Wolfe, 2000; Ianora et al., 2006),”

“Wolfe et al. (1997) reported that strains of the related genus Emiliania, which contained low levels of DMSP-lyase were preferred by grazers over strains with high DMSP-lyase levels.”

“Using cell extracts from nontoxic phytoplankton, a few compounds with a proven regulative role in plankton ecology, including dimethyl sulfide and polyunsaturated aldehydes, have been identified (Pohnert 2005; Wolfe 2000).”

“…abilities (Sibbald et al. 1987, Bennett et al. 1988, Snyder 1991) and have been reported to discriminate between similar-sized prey for some chemical reason (Stoecker et al. 1986, Sanders 1988, Landry et al. 1991, Verity 1991, Jürgens & De Mott 1995, Christaki et al. 1998, Wolfe 2000).”

“These findings are important because there are other factors, biotic (e.g., allelopathy) and abiotic (e.g., nutrient depletion), that can also significantly affect phytoplankton cell mortality (Fritz & Nass 1992, Brussaard et al. 1997, 1998, Berges & Falkowski 1998, Wolfe 2000).”

“Although reduction of herbivory through chemical deterrence plays a fundamental role in the ecology and evolution of terrestrial and marine benthic communities (Hay & Fenical, 1988; Spencer, 1988; Tollrian & Harvell, 1999), the phenomenon of chemical defense has received much less attention from marine plankton ecolog…”

“Inducible defence Microorganisms have complex and sophisticated sensory and behavioural adaptations to respond to changes and chemical signals that occur in their environment (Wolfe, 2000).”

“predators (Wolfe 2000; Zimmer and Butman 2000).”

“However, copepods and other zooplankton may select between seemingly similar prey, even of the same species, on the basis of biochemical composition (Houde and Roman 1987; Wolfe 2000).”

“In turn, prey cells may use structural or chemical defenses against protistan predation (Wolfe, 2000; Jurgens and Matz, 2002; Matz et al., 2004).”

“There is evidence that some dinoflagellates not only may be important producers of DMSP (Keller 1989) but also can enzymatically convert DMSP to DMS (Kadota & Ishida 1968, Steinke et al. 1996, Niki et al. 2000, Wolfe 2000).”

“Several Prorocentrum species, includ ing P. minimum, reportedly synthesize okadaic acid and are rich in dimethylsulfoniopropionate (DMSP) both of which can function as grazing deterrents (Zhou and Fritz, 1994; Wolfe, 2000).”

“The microzones are thought to persist in the boundary layer of small particles for some time (Wolfe 2000) and the existence of robust microzones, stable for about 10 min, around point sources has been shown (Blackburn et al.”

“Moreover, DMSP plays a critical role in marine microbial food webs, both as a chemical signal (Wolfe, 2000; Zimmer-Faust et al., 1996), and as the main carrier of reduced S and a significant carrier of C within and among trophic levels (Kiene et al., 2000; Simó et al., 2002).”

“…compound, dimethyl sulphide (DMS) seems to be important (i) in the context of anti-feeding through its relation with acrylate production (Wolfe, 2000), (ii) as an attractant signalling molecule to bird species at higher trophic levels (Nevitt et al., 1995, Nevitt, 2000), (iii) for its…”

“These dinoflagellate toxins have been implicated in human intoxications resulting from consumption of poisonous fish and shellfish [159; 164].”

“…that certain HAB species deter grazing through the production of toxins (Huntley et al. 1986, Ives 1987, Uye & Takamatsu 1990, Teegarden 1999, Wolfe 2000) and recent evidence suggests that Karlodinium veneficum falls within this category (Vaqué et al. 2006, Adolf et al. 2007, Adolf et al. in…”

“These might be exploited by copepods as indicators for their food selection (Wolfe, 2000).”

“The function of acrylic acid has been well studied as an anti-microbial agent and deterrent to algal grazing by protozoans (reviewed by Wolfe 2000), and it is generally assumed that this benefit has been the major selective pressure for DMSP-lyase (but see also Steinke et al. 2002).”

“, 2002; Bucciarelli & Sunda, 2003) and a molecular defense against grazing, thanks to the toxicity of acrylate produced during DMSP catabolism (Wolfe et al., 1997; Wolfe, 2000).”

“In addition, O. marina has been used to model bi- and tritrophic grazing interactions (Wolfe & Steinke 1996), dimethyl sulphide production and grazing selectivity (Wolfe et al. 1997, Wolfe 2000), and the potential control of red-tide organisms (Jeong et al. 2003, Johnson et al. 2003).”

“Both chemical and mechanical stimuli have been reported effective in eliciting phytoplankton responses [22,28] and exchanges of chemical information within and among trophic levels can directly impact population structure [26,29,40].”

“Surface-associated compounds signaling chemical cues for rejection to predators have previously been recognized in planktonic protists [4, 51, 58].”

“The importance of prey-associated chemical compounds which deter predator grazing is a recurrent theme in marine literature [65, 73–75].”

“In addition to mechanical protection conferred by the silica frustules, diatoms possess defensive capabilities involving complex and highly evolved chemical defenses against competing species (Wolf 2000, Pohnert 2005, 2010).”

“…continual production and release of unknown lytic toxins, which may be complex metabolites requiring intricate biosynthesis pathways to produce, while avoiding self-toxicity, is often assumed, and widely stated in the literature, to be costly (Wolfe, 2000; Legrand et al., 2003; Gross et al., 2012).”

“High levels of acrylate may deter herbivorous microzooplankton and could result in selective grazing on phytoplankton with lower potential for DMS and acrylate production (Wolfe et al., 1997; Wolfe, 2000).”

“Some toxic algae may also form dense blooms, 49 potentially promoted by their toxicity and consequent grazer deterrent effects, and a 50 defensive role of toxin production is thus often assumed [4, 9].”

“Some planktonic bacteria and phytoplankton appear to have developed mechanisms to deter grazing ( Wolfe, 2000; Strom, 2002; Hamm et al., 2003).”

“allelochemicals, allelopathy has long been believed to play a crucial role in phytoplankton bloom formation and succession in both freshwater and marine ecosystems (Pratt, 1966; Keating, 1977; Rice, 1984; Lewis Jr., 1986; Wolfe, 2000; Rengefors and Legrand, 2001; Vardi et al., 2002; Tillmann and John 2002; Legrand et…”

“Chemical signals are easily transported in water (Wolfe, 2000), but can also be degraded bymicrobial activity (von Elert and Loose, 1996; Hagström et al.”