© 2001 by The Society for Integrative and Comparative Biology
Secondary Metabolites as Mediators of Trophic Interactions Among Antarctic Marine Organisms1
1 Department of Biology, University of Alabama at Birmingham, Birmingham, Alabama 35294-1170
2 
Department of Chemistry, Florida Institute of Technology, Melbourne, Florida 32901
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Secondary metabolites are widespread among lower phyla and understanding their functional role(s) in the producing organism has been under study in recent decades. Considerable progress has been made in understanding chemical ecological interactions among terrestrial organisms, and similar research in the marine realm has been initiated in recent years. Polar regions are more difficult to access and thus progress has been slower. Nevertheless, the extreme and often unique marine environments surrounding Antarctica as well as the many unusual trophic interactions in antarctic marine communities might well be expected to select for novel secondary metabolites and/or novel functional roles for secondary metabolites. Indeed, recent studies have documented novel, chemically-mediated interactions between molluscs and amphipods, between algae, urchins and anemones, and between sponges and their predators. The Porifera are the dominant phylum on the McMurdo Sound benthos, and representatives of this phylum have been shown to elaborate sea star feeding deterrents, inhibitors of fouling or infectious organisms, and metabolites which mediate predation via molt inhibition. As a result of studies on Antarctic sponges, new insights into functional roles of pigments and the ability of sponges to sequester metabolites have been gained, and a new mechanism of chemical defense has been described. Herein we describe recent results of our studies of trophic interactions between sponges and their predators that are mediated by specific sponge secondary metabolites. Moreover, we highlight unusual chemically-mediated interactions in antarctic marine invertebrates other than sponges.
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INTRODUCTION |
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Sessile or sluggish organisms must defend themselves from predation or encroachment of competitors since their lack of mobility precludes evasion (Harborne, 1994
). Many organisms have been found to defend themselves by producing toxins or other bioactive small molecules (i.e., M.W. <1,000). Many more organisms are known to produce small molecule "secondary metabolites," possessing unknown functional roles. In Antarctica, where trophic relationships have evolved under differing ecological and physical constraints than are found in temperate and tropical ecosystems (Dayton et al., 1994), we have been interested in the nature of chemical defense agents and their functional role(s) (McClintock and Baker, 1997; Amsler et al., 2001a).
Secondary metabolites, also known as natural products, are biochemicals which might be described as lacking a role in the "internal economy" of the producing organism (Williams et al., 1989; Williams and Maplestone, 1992). A characteristic of secondary metabolites is their limited phylogenetic distribution; while primary metabolites such as the common amino acids, carbohydrates, and nucleosides, are chemically identical in virtually all organisms, both simple and advanced, secondary metabolites are generally limited to a specific species or even a chemotypical subset of a species.
There are a number of classes of natural products, recognized on the basis of their biosynthetic origin, such as polyketides, terpenes and alkaloids. For example, in the marine realm, representative polyketides include the red tide and similar toxins, such as the brevetoxins (Lin et al., 1981) and ciguatoxin (Murata et al., 1989; Scheuer, 1994) (Fig. 1). Polyketides are built primarily of acetate (two carbon, C2) units, with occasional propionate (C3) or, rarely, larger building blocks (Herbert, 1981). Terpenes are characterized by the number of C5 isoprene units in their structure. Monoterpenes such as halomon (Fuller et al., 1994), an antitumor compound from a red macroalga, contain two isoprene units and are therefore C10 compounds, while sesquiterpenes such as the sponge-derived 9-isocyanopupukeanane (Burreson et al., 1975) (Fig. 1) contain three isoprene units, diterpenes have four, sesterterpenes, such as the analgesic manoalide (De Silva and Scheuer, 1980) (Fig. 1) have five, and diterpenes, have six isoprene units. Larger terpenes are uncommon, with the exception of polymeric isoprene, well known as rubber. Shikimates generally derive from phenylalanine and include many of the aromatic natural products, such as hydroquinones found in Sargassum (see Faulkner, 1999). Other amino acid derived natural products include the small linear or cyclic peptides, which are often composed of unmodified amino acids connected by peptide bonds, but can incorporate modified amino acids, ester bonds (the depsipeptides), and even polyketide portions. The cytotoxic didemnin depsipeptides (Rinehart et al., 1981) are examples of this class of natural products (Fig. 1). Derivatives of other primary metabolites, including nucleosides, carbohydrates, and fatty acids can also be found as secondary metabolites, though they are less common. The final major class of natural products is the alkaloids, which are nitrogen-containing, often aromatic, compounds which primarily derive their nitrogen from the amino acid pool but have lost much of the appearance of the amino acids. Examples of marine alkaloids include the bastidins (Kazlauskas et al., 1981), ecteinascidins (Wright et al., 1990; Rinehart et al., 1990), and papuamine (Baker et al., 1988), with decreasing degrees of similarity to their amino acid progenitors (Fig. 1).
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The complexity, diversity, and common occurrence of secondary metabolites raises the question of their functional roles. That natural products have a reputation as toxins and noxins (vide supra) addresses one functional role as deterrents of predation, and certainly this role for natural products has been the most thoroughly studied to date (Paul, 1992
; Pawlik, 1993; Hay, 1996; McClintock and Baker, 1997, 2001; Amsler et al., 2001a). Other functional roles which have been studied include inhibition of fouling and/or infection and mediation of spatial competition (Sammarco and Coll, 1992; Rittschof, 2001). What is clear is that secondary metabolites are produced under selective evolutionary pressure; energy expenditure for the biosynthesis of natural products detracts from that available to growth and reproduction and therefore must serve a purpose (Barnes and Hughes, 1988; Herms and Matteson, 1992; Berenbaum, 1995). Studies of chemical ecology seek to identify a chemical basis of organismal interrelationships. |
THE ANTARCTIC MARINE BENTHOS |
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Early biogeographic comparison of the incidence of chemical defense predicted an inverse relationship with latitude (Bakus and Green, 1974
). This theory suggested that polar marine invertebrates lack sufficient fish predation to drive natural selection for chemical means of protection. However, when this theory was proposed, little was known of the predatory-prey interactions of benthic marine invertebrates in Antarctica, much of which has come to light through subsequent studies (Dayton et al., 1974; Dayton 1979; McClintock and Baker, 1997; Amsler et al., 2000). In McMurdo Sound (77°S, 164°E), for example, benthic invertebrates are exposed to significant predation, primarily by sea stars (Dayton et al., 1974; McClintock, 1997), they are under pressure from fouling diatoms (Amsler et al., 2001b), invertebrate larvae, algal spores, and potentially infectious water-column microorganisms, and they must compete for scarce hard substrate upon which to settle. These are characteristics which would suggest Antarctic marine benthic organisms are likely to evolve chemically-mediated defensive strategies.
The benthos of McMurdo Sound is characterized by extensive cover by sponges, which can occupy as much as 55% of the benthos (Dayton et al., 1974). The fast growing, potentially space dominating sponge Mycale acerata is kept in check by the spongivorous sea star Perknaster fuscus. P. fuscus includes a number of other sponges in its diet and is therefore a major predator of the sponges. Because sponges are well known to elaborate natural products (Faulkner, 1999), the relationship between P. fuscus and sponges has been a primary focus of our investigation of chemical ecological relationships in McMurdo Sound, Antarctica. Herein we describe the trophic relationships of five McMurdo Sound sponges and their predators.
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TROPHIC RELATIONSHIPS INVOLVING ANTARCTIC SPONGES |
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Among the common members of the sponge community are several conspicuously colored species. Isodictya erinacea and Dendrilla membranosa are bright yellow sponges and lack structural defenses, being devoid of spicule armamentation (Dayton et al., 1974
). Neither of these two sponges are among those consumed by P. fuscus (Dayton et al., 1974). Latrunculia apicalis is a deep green sponge which also has not been observed to be preyed upon by P. fuscus. Perhaps the most striking sponge is the fire-red Kirkpatrickia variolosa. This sponge comprises only a minor component of the diet of P. fuscus and is composed of soft, fleshy tissue. The seeming lack of predation by P. fuscus on these sponges which lack physical deterrence make them likely candidates for chemical investigation (Dayton et al., 1974).
To understand patterns of spongivory in Perknaster fuscus to McMurdo Sound sponges, we developed a tube-foot retraction assay (McClintock et al., 1994). When placed on their aboral side in a finger bowl of fresh, ambient temperature (–1°C) sea water, the tube-feet of the sea star are readily accessible. The tube-feet are chemosensory, used by the sea star for, among other things, assessment of prey suitability (Sloan, 1980). Contact of the tube-feet with sponge extracts elicits a characteristic chemosensory response; an unsuitable extract, applied to a glass rod for accurate positioning, may elicit a retraction for up to 60 sec, whereas extracts from acceptable sponges or controls typically causes attachment of the tube-foot to the glass rod (McClintock et al., 1994; 2000). We have used this assay to assess McMurdo Sound sponge extracts for the presence of chemical agents which might deter predation (McClintock et al., 1994; 2000).
Validation of the tube-foot retraction assay was achieved by its ability to accurately predict sea star feeding preferences in the field (Dayton et al., 1974; Amsler et al., 2000). Primary dietary sponges of P. fuscus, for example, elicit a response commensurate with controls, while several sponges known to elaborate toxic chemistry display characteristically long tube-foot retraction times. Compare, for example, P. fuscus commonly preyed upon sponges M. acerata, Homaxinella balfourensis, Haliclona scoti (Dayton et al., 1974; personal observations by the authors) with the composite control response (Fig. 2). Similarly, sponges eliciting the longest tube-foot retraction times, such as Isodictya spingerosa and Latrunculia apicalis, are not found among the sponges preyed upon by P. fuscus (Dayton et al., 1974; personal observations of the authors).
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CHEMICAL ANALYSES OF BIOACTIVE MCMURDO SOUND SPONGES |
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Extracts from Latrunculia apicalis elicit a significant tube-foot retraction response in Perknaster fuscus (McClintock et al., 1994
). Fractionation of the extract yielded discorhabdin alkaloids (Yang, 1994; Yang et al., 1995). This group of pigments was first reported from sponge species found in temperate and tropical waters, and they are routinely toxic (Perry et al., 1988). Discorhabdin C and G (Fig. 3) were found in L. apicalis from McMurdo Sound and were bioactive in both the tube-foot retraction assay and in antimicrobial assays using sympatric or other bacteria; discorhabdin C is a potent mammalian cytotoxin, emphasizing its bioactive nature (Yang 1994; Yang et al., 1995). The discorhabdins are clearly serving a role in L. apicalis as defensive agents, both toward predators and potential infectious agents.
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It is noteworthy that the sea star feeding deterrent bioactivity mediated by the discorhabdins is an interaction that takes place near the sponge surface. Sea stars feed by extruding their cardiac stomach over their prey, thus predation begins at the pinacocytic layer. This contrasts with tropical marine systems where spongivory occurs primarily by fish or turtles and their biting activities encroach deeply in the mesohyle. To test the ability of L. apicalis to sequester chemical defenses at this most vulnerable site, an analysis of discrete sponge layers was undertaken (Furrow et al., in preparation). While interspecific variation of discorhabdin G content was found among these layers, mean levels of discorhabdin G were highest in the outer surface (top 2 mm) of the sponge and fell off rapidly toward the center (Furrow et al., in preparation). Other instances of sponges sequestering natural products in more susceptible tissues have been demonstrated (Thompson et al., 1983
; Schupp et al., 1999), though this is the first example of sequestration near the surface of a sponge.
Dendrilla membranosa is among the few antarctic sponges known to produce terpenes (Amsler et al., 2001a). Membranolide and 9,11-dihydrogracillin (Fig. 3) are reported to have antibiotic activity (Molinski and Faulkner, 1987), though the most potent biological activity is associated with the alkaloids from D. membranosa, such as the yellow isoquinoline pigment (Fig. 3), which has antibiotic activity (Molinski and Faulkner, 1988), and picolinic acid, which has tube-foot retraction activity (Baker et al., 1993, 1995).
The bright red sponge Kirkpatrickia variolosa produces the unusual variolin alkaloids (Trimurtulu et al., 1994; Perry et al., 1994), such as variolin A (Fig. 3). Despite considerable cytotoxicity (Perry et al., 1994), variolin A does not cause significant tube-foot retraction in Perknaster fuscus. Other pigments in the polar extract of this sponge have been implicated as sea star feeding deterrents, though none has been isolated to date (Baker et al., 1994).
Suberites sp. is a common McMurdo Sound sponge that has a muted yellow coloration. Suberitenones A and B, originally described from King George Island (Shin et al., 1995) were also isolated from McMurdo Sound collections of the sponge (Baker et al., 1997). Suberitenones were active in both the tube-foot retraction assay and in an antibiotic assay using sympatric bacteria. Similar to the situation with Latrunculia apicalis, Suberites sp. is a spherical sponge amenable to layer removal, and the bioactivity of the natural products suggested that sequestration on the surface would be advantageous to the sponge. Quantitative analysis a single specimen located 90% of suberitenone A in the outer layer of the sponge (Tipton, Baker and McClintock, unpublished results).
The discorhabdins from Latrunculia apicalis, the isoquinoline pigment from Dendrilla membranosa, the variolins from Kirkpatrickia variolosa, and, to a lesser extent, the suberitenones from Suberites sp., are all pigments. It is compelling to note that these pigments are bioactive toward a predator, Perknaster fuscus, which lacks visual orientation. The role of pigments in aposomatic coloration (Guilford and Cuthill, 1991) has recently been questioned (Chanas and Pawlik, 1995); the evolution of pigmented chemical defenses in an ecosystem devoid of visually oriented predators argues against aposomatic roles. Pigments are almost exclusively employed in energy capture or serve as antioxidants in other sessile organisms such as marine and terrestrial plants (Lobban and Harrison, 1994). These are unlikely roles for pigments of benthic marine invertebrates. There is little information on whether pigments from temperate or tropical benthic marine invertebrates may serve as antifeedants.
Not all bioactivity of McMurdo Sound sponges investigated to date is limited to tube-foot retraction and/or antibiotic activity. Isodictya erinacea, for example, has yielded a number of secondary metabolites (Moon, 1997; Moon et al., 1998), at least one of which appears to be involved in an unusual trophic relationship. A host of purines and nucleosides, including the cytotoxic erinacean, was found in I. erinacea, and p-hydroxybenzaldehyde was identified as the metabolite responsible for tube-foot retraction activity of the lipophilic extract (Moon et al., 1998).
The yellow pigment eribusinone (Moon, 1997), an apparent tryptophan catabolite (Fig. 4), has also been isolated from Isodictya erinacea. Tryptophan catabolites are involved in crustacean molt regulation (Naya et al., 1993). Kynurenine (Fig. 4) and xanthurenic acid, for example, lie on the molt regulatory pathway. Xanthurenic acid inhibits the cytochrome P450 enzyme which is responsible for hydroxylation of ecdysone to 20-hydroxyecdysone, the molt hormone in crustaceans. Structural similarity of kynurenine and eribusinone (Fig. 4) led to studies of the functional role of eribusinone in crustacean molt regulation.
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The amphipod Orchomene plebs, a voracious omnivorous predator (personal observations), was fed a diet enriched in eribusinone. Despite the fact that O. plebs consumed more eribusinone-enriched diet than control (krill enriched), diet, molt events were significantly reduced and mortality significantly increased (Moon et al., 2000
). This is the first example of molt regulation as a potential mechanism of chemical defense in the marine realm and differs from terrestrial molt regulation mechanisms in being molt inhibitory, rather than stimulatory, as is found among land plant chemical defenses against insects (Harborne, 1994). |
OTHER CHEMICALLY-MEDIATED TROPHIC INTERACTIONS OF NOTE |
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This report focuses largely on the interactions of sponges and their predators. However, in the context of Antarctic chemical ecology investigations, a number of other significant trophic interactions are noteworthy (McClintock and Baker, 1997
). The unusual relationship between the pelagic mollusc Clione antarctica, a pteropod, and its amphipod (Hyperiella dilatata) abductor (McClintock and Janssen, 1990) has been described as "antagonistic symbiosis" (McClintock and Baker, 1998). Clione antarctica elaborates a fish feeding deterrent, pteroenone (Bryan et al., 1995; Yoshida et al., 1995), which protects it from several sympatric fish predators. Hyperiella dilatata is a major prey item of these same fish predators and has evolved the ability to capture C. antarctica from the water column, position it on its dorsum, and thus avoid fish predation (McClintock and Janssen, 1990).
Another unique trophic interaction is a "feeding triangle" involving defensive interactions of macroalgae, sea urchins, and sea anemones. The sea anemone Isotealia antarctica is a voracious, opportunistic predator of macroinvertebrates (Dayton et al., 1970) and is involved in a mutualistic relationship between one of its prey, the sea urchin Sterechinus neumayeri, and two of the urchin's potential prey items, the macroalgae Phyllophora antarctica and Iridaea cordata (Amsler et al., 1999). S. neumayeri preferentially covers itself with these macroalgae and this cover significantly increases the likelihood of escape from I. antarctica because the anemones' tentacles attach to the algae which the anemone or both the urchins and anemone then release. Macroalgae benefit from this relationship because fertile drift plants are retained in the photic zone where they continue to contribute to the gene pool. Both macroalgal species are chemically defended against herbivory by S. neumayeri (Amsler et al., 1998). Hence this relationship differs from the antagonistic symbiosis of Clione antarctica and Hyperiella dilatata by being a true defensive mutualism benefiting both the macroalgae and urchins.
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SUMMARY |
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Chemical ecological investigations of antarctic sponges have demonstrated that chemical defenses have evolved in numerous species. This contradicts corollaries of early theories concerning biogeographic variation in predation and in chemical defense but agrees with predictions that could have been made based on the intense predation demonstrated by more recent investigators. The Antarctic offers unique opportunities to study selected ecological relationships, such as the role of pigments in chemical defense in the absence of visually oriented predators, and the role of secondary metabolite sequestration in predators which attack surface tissues. We have also documented several unique chemically-mediated trophic relationships, including a new mechanism of chemical defense in the marine realm (molt inhibition), antagonistic symbiosis, and an unusual chemically-mediated "feeding triangle."
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ACKNOWLEDGMENTS |
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Much of the work reported in this symposium review was carried out by colleagues whose names appear on papers cited in the references. Additional laboratory assistance of B. Moon, F. B. Furrow, J. Tipton, Y. C. Park and J. A. Baker is gratefully acknowledged. Field assistance provided by the Antarctic Support Associates, Inc., the Antarctic Support Services of the National Science Foundation, and the US Naval Antarctic Support Force enabled these studies. We are particularly thankful to Dr. Polly Penhale, National Science Foundation (NSF) Program Manager for the Office of Polar Programs, for her generous support of the present symposium via a grant to CDA, JBM and BJB. The research described within was supported by NSF grants to BJB and JBM. The NSF also provided funds in support of the purchase an NMR instrument at Florida Institute of Technology, which was used extensively in this work.
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FOOTNOTES |
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1 From the Symposium Antarctic Marine Biology presented at the Annual Meeting of the Society for Comparative and Integrative Biology, 4–8 January 2000, at Atlanta, Georgia.
2 Corresponding author: Bill J. Baker, Department of Chemistry, Florida Tech, 150 West University Blvd, Melbourne, FL 32901. E-mail: bbaker{at}fit.edu Phone: (321) 674-8951. Fax: (321) 674-8951.
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Amsler, C. D., J. B. McClintock, and B. J. Baker. 2000. Chemical defenses of antarctic marine organisms: A reevaluation of the latitudinal hypothesis. In W. Davison, C. Howard-Williams, and P. Broady (eds.), Antarctic ecosystems: Models for wider ecological understanding. New Zealand Natural Science, New Zealand.
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