Bill J. Baker

Marine chemical ecology

Over the last four decades, the isolation and structure elucidation of biomedically important marine natural products has been a fruitful area of research for organic chemists. Compilations of marine structures reveal that by 1993 nearly 7000 different marine structures had been documented; these metabolites represent all the major structural classes of natural products, including terpenes, alkaloids, polyketides, peptides, and shikimate-derived metabolites, as well as compounds of mixed biogenesis. Some phylogenetic trends have been recognized; for example, the majority of coelenterate metabolites are terpenoid in origin. Other phyla display broad structural diversity; metabolites of the polyketide, terpene, and alkaloid families, as well as compounds of mixed biosynthesis, have all been isolated from sponges (see Chapter 1, this volume).Background Introduction to the Chemical Ecology of Marine Natural Products, M.K. Harper, T.S. Bugni, B.R. Copp, R.D. James, B.S. Lindsay, A.D. Richardson, P.C. Schnabel, D. Tasdemir, R.M. VanWagoner, S.M. Verbitski, and C.M. Ireland Ecological Perspectives on Marine Natural Product Biosynthesis, M.J. Garson Marine Natural Products Chemistry as Evolutionary Narrative, G. Cimino and M.T. Ghiselin Organismal Patterns in Marine Chemical Ecology Chemical Ecology of Mobile Marine Invertebrates: Predators and Prey, Allies and Competitors, J.J. Stachowicz The Chemical Ecology of Invertebrate Meroplankton and Holoplankton, J.B. McClintock, B.J. Baker, and D.K. Steinberg Chemical Mediation of Macroalgal-Herbivore Interactions: Ecological and Evolutionary Perspectives, V.J. Paul, E. Cruz-Rivera, and R.W. Thacker Secondary Metabolites from Antarctic Marine Organisms and their Ecological Implications, C.D. Amsler, K.B. Iken, J.B. McClintock, and B.J. Baker Spatial Patterns in Macroalgal Chemical Defenses, K. Van Alstyne, M.N. Dethier, and D. Duggins Resource Allocation in Seaweeds and Marine Invertebrates, G. Cronin Chemical Mediation of Surface Colonization, P.D. Steinberg, R. de Nys, S. Kjelleberg Cellular and Physiological Patterns in Marine Chemical Ecology Effects of Secondary Metabolites on Digestion in Marine Herbivores, N.M. Targett and T.M. Arnold Chemotaxis and Chemokinesis in Marine Bacteria and Algae, C.D. Amsler and K.B. Iken Natural Chemical Cues for Settlement and Metamorphosis of Marine-Invertebrate Larvae, M.G. Hadfield and V.J. Paul Contributions of Marine Chemical Ecology to Chemosensory Neurobiology, H.G. Trapido-Rosenthal Chemical Defenses of Marine Organisms Against Solar Radiation Exposure: UV-Absorbing Mycosporine-Like Amino Acids and Scytonemin, D. Karentz Applied Marine Chemical Ecology Marine Chemical Ecology: Applications in Marine Biomedical Prospecting, S.H. Sennett Natural Product Antifoulants and Coatings Development, D. Rittschof Metabolites of Free-Living, Commensal, and Symbiotic Benthic Marine Microorganisms, V.S. Bernan

Ecology of Antarctic Marine Sponges: An Overview'

Abstract Sponges are important components of marine benthic communities of Antarctica. Numbers of species are high, within the lower range for tropical latitudes, similar to those in the Arctic, and comparable or higher than those of temperate marine environments. Many have circumpolar distributions and in some habitats hexactinellids dominate benthic biomass. Antarctic sponge assemblages contribute considerable structural heterogeneity for colonizing epibionts. They also represent a significant source of nutrients to prospective predators, including a suite of spongivorous sea stars whose selective foraging behaviors have important ramifications upon community structure. The highly seasonal plankton blooms that typify the Antarctic continental shelf are paradoxical when considering the planktivorous diets of sponges. Throughout much of the year Antarctic sponges must either exploit alternate sources of nutrition such as dissolved organic carbon or be physiologically adapted to withstand resource constraints. In contrast to predictions that global patterns of predation should select for an inverse correlation between latitude and chemical defenses in marine sponges, such defenses are not uncommon in Antarctic sponges. Some species sequester their defensive metabolites in the outermost layers where they are optimally effective against sea star predation. Secondary metabolites have also been shown to short-circuit molting in sponge-feeding amphipods and prevent fouling by diatoms. Coloration in Antarctic sponges may be the result of relict pigments originally selected for aposematism or UV screens yet conserved because of their defensive properties. This hypothesis is supported by the bioactive properties of pigments examined to date in a suite of common Antarctic sponges.

Cold-water marine natural products

Marine natural products isolated from organisms collected from cold-water habitats are described. Emphasis is on bioactive compounds from tunicates, sponges, microbes, bryozoans, corals, algae, molluscs and echinoderms. Synthetic studies of several important classes of cold-water compounds are highlighted.

LACK OF DEFENSE OR PHLOROTANNIN INDUCTION BY UV RADIATION OR MESOGRAZERS IN DESMARESTIA ANCEPS AND D. MENZIESII (PHAEOPHYCEAE)1

Phlorotannins are polyphenoloic metabolites occurring only in the Phaeophyceae that have numerous putative primary roles (e.g. cell‐wall construction and storage) as well as secondary metabolic roles, which include herbivore feeding deterrence and protection from UV radiation. The proposed role of phlorotannins in the defense against UV radiation is of particular importance in the Antarctic due to depletion of the stratospheric ozone layer in that area. Several studies of brown algae have found evidence of an induction response (the production of defensive metabolites, including phlorotannins) after grazing by various mesograzers, after simulated grazing/wounding, and after exposure to increases in UV radiation. This study aimed to determine if phlorotannin production or other defenses in two dominant, endemic Antarctic species (Desmarestia menziesii Montagne and Desmarestia anceps J. Agardh) could be induced by an increase in exposure to UV radiation or by natural and artificial grazing. An in situ experiment failed to detect any effect of UV radiation on phlorotannin concentrations in either species or on subsequent palatability in feeding bioassays. A laboratory‐based experiment did not detect any effect of mesoherbivore grazing or simulated grazing (wounding) on palatability or the concentration of phlorotannins in D. menziesii. Instead, phlorotannin concentrations increased in all treatments in both experiments, consistent with an increase in overall resource availability due to an increase in available PAR compared with the in situ irradiance at the algal collection sites.

The Chemistry of Algal Secondary Metabolism

Natural product chemistry is a branch of organic chemistry that touches upon many other fields of science, especially applied sciences such as medicine, agriculture, and engineering. It is fundamentally a basic science, involved in the discovery, characterization and cataloging of new chemical substances found in nature. Among other basic scientists, biologists and ecologists recognized some time ago that natural products might help explain species composition, distribution, and diversity in some settings, establishing the field of chemical ecology (Harborne 1989). The field has developed largely around collaborations of chemists and biologists, each bringing their own knowledge base to chemical ecological questions. This chapter is intended as an overview of natural product chemistry with an emphasis on the chemical aspects of algal defensive metabolites. It is our hope that algal ecologists will gain insight into the chemistry in the same manner that chemists will acquire a deeper understanding of the ecology from the remaining chapters of this book.

Filamentous algal endophytes in macrophytic Antarctic algae: prevalence in hosts and palatability to mesoherbivores

Amsler C.D., Amsler M.O., McClintock J.B. and Baker B.J. 2009. Filamentous algal endophytes in macrophytic Antarctic algae: prevalence in hosts and palatability to mesoherbivores. Phycologia 48: 324–334. DOI: 10.2216/08-79.1. Five individuals, each from 13 common species of large macroalgae (‘macrophytes’) from the western Antarctic Peninsula, were surveyed for the presence of filamentous algal endophytes both macroscopically and microscopically using dissecting and compound microscopes. Of the 13 species surveyed, endophytes were either rare or absent in five. The remaining species all supported endophytes in most or usually all individuals with maximum endophyte densities per species ranging from 3% to 75% of the thallus area. Thallus fragments from all individuals with endophytes were placed into culture, and 99 unialgal, filamentous brown algal strains were isolated. The ITS1 gene was sequenced in each strain to sort these into distinct genotypes. Brown algal endophytes grew well in culture, and 10 distinct filamentous genotypes were present. The green endophytes did not grow well in culture, and only two green algal species present in the thallus fragments were isolated. No-choice feeding rate bioassays were performed with thallus fragments of all 13 macrophyte species and with cultures of seven filamentous brown endophytes and both green endophytes. Feeding rates on the endophytes were 2–3 orders of magnitude higher than rates on 12 of the macrophyte species and 2- to 6-fold higher than on the only truly palatable macrophyte, Palmaria decipiens. These data support the hypothesis that Antarctic macrophytes are commonly endophytized and that the endophytes benefit from the association by being protected, at least in part, from amphipod herbivory.

Characterization of the Microbial Community and Polyketide Biosynthetic Potential in the Palmerolide-Producing Tunicate Synoicum adareanum

Palmerolide A (1) is a macrolide isolated from the Antarctic tunicate Synoicum adareanum that is of interest due to its potential as an antimelanoma drug. Biosynthesis is predicted to occur via a hybrid PKS-NRPS pathway within S. adareanum, but the identity of the palmerolide-producing organism (host or putative host-associated microorganism) has not been established. Microscopic observation revealed a dense microbial community inside the tunicate, and evidence from 16S rRNA gene DGGE profiles and clone library sequences suggests that the bacterial community has moderate phylogenetic complexity. The alpha and gamma classes of Proteobacteria account for ∼75% of the cloned 16S rRNA genes, and the majority of these sequences are affiliated with the genera Pseudovibrio and Microbulbifer. DNA sequences encoding type I PKS ketosynthase (KS) domains were detected by PCR. The S. adareanum KS sequences, which affiliate with the trans-AT clade, are similar to portions of PKS proteins that lack integrated acyltransferase domains in pathways for generating bioactive polyketide compounds, including bryostatin, leinamycin, and pederin.

Epigenetic Tailoring for the Production of Anti-Infective Cytosporones from the Marine Fungus Leucostoma persoonii

Recent genomic studies have demonstrated that fungi can possess gene clusters encoding for the production of previously unobserved secondary metabolites. Activation of these attenuated or silenced genes to obtain either improved titers of known compounds or new ones altogether has been a subject of considerable interest. In our efforts to discover new chemotypes that are effective against infectious diseases, including malaria and methicillin-resistant Staphylococcus aureus (MRSA), we have isolated a strain of marine fungus, Leucostoma persoonii, that produces bioactive cytosporones. Epigenetic modifiers employed to activate secondary metabolite genes resulted in enhanced production of known cytosporones B (1, 360%), C (2, 580%) and E (3, 890%), as well as the production of the previously undescribed cytosporone R (4). Cytosporone E was the most bioactive, displaying an IC90 of 13 µM toward Plasmodium falciparum, with A549 cytotoxicity IC90 of 437 µM, representing a 90% inhibition therapeutic index (TI90 = IC90 A459/IC90 P. falciparum) of 33. In addition, cytosporone E was active against MRSA with a minimal inhibitory concentration (MIC) of 72 µM and inhibition of MRSA biofilm at roughly half that value (minimum biofilm eradication counts, MBEC90, was found to be 39 µM).

The Mg-Calcite Composition of Antarctic Echinoderms: Important Implications for Predicting the Impacts of Ocean Acidification

The Southern Ocean is considered to be the canary in the coal mine with respect to the first effects of ocean acidification (OA). This vulnerability is due to naturally low carbonate ion concentrations that result from the effect of low temperature on acid-base dissociation coefficients, from the high solubility of CO2 at low temperature, and from ocean mixing. Consequently, the two calcium carbonate polymorphs, aragonite and calcite, are expected to become undersaturated in the Southern Ocean within 50 and 100 years, respectively. Marine invertebrates such as echinoderms, whose skeletons are classified as high-magnesium carbonate (>4% mol MgCO3), are even more vulnerable to OA than organisms whose skeletons consist primarily of aragonite or calcite, with respect to both increased susceptibility to skeletal dissolution and further challenge to their production of skeletal elements. Currently, despite their critical importance to predicting the effects of OA, there is almost no information on the Mg-calcite composition of Antarctic echinoderms, a group known to be a major contributor to the global marine carbon cycle. Here we report the Mg-calcite compositions of 26 species of Antarctic echinoderms, representing four classes. As seen in tropical and temperate echinoderms, Mg-calcite levels varied with taxonomic class, with sea stars generally having the highest levels. When combined with published data for echinoderms from primarily temperate and tropical latitudes, our findings support the hypothesis that Mg-calcite level varies inversely with latitude. Sea stars and brittle stars, key players in Antarctic benthic communities, are likely to be the first echinoderms to be challenged by near-term OA.

Chemical defenses against diatom fouling in Antarctic marine sponges

Antarctic sponges are commonly fouled by diatoms, sometimes so heavily as to occlude pores employed in filter feeding and respiration. This fouling becomes heavier during the annual summer microalgal bloom. Polar and non‐polar extracts of eight species of marine sponges from McMurdo Sound, Antarctica were assayed for cytotoxicity against sympatric fouling diatoms. To identify compounds potentially released by sponges as defenses against diatom biofouling, only fractions of crude extracts that were soluble in seawater or 2% methanol in seawater were assayed. Significant bioactivity was present in seven of the eight species. Both Mycale acerata and Homaxinella balfourensis displayed moderate levels of defense against diatoms even though they are not or are only weakly chemically defended against bacteria and predators. Calyx acuarius extracts, which do have antipredator and antibacterial effects, had no effect on diatoms except at levels many fold higher than present in the intact animal. These results strongly suggest some level of specificity for chemical defenses against diatom fouling in antarctic sponges.