510 CHLOROPLAST E.R.: EVOLUTION OF TWO MEMBRANES

6Non-nitrogren compounds containing ladder-frame polyethers. Brevetoxin (Fig. 23.4(f )), ciguatoxin

(Fig. 23.4(f )), and yessotoxin (Fig. 23.4(f )). Brevetoxins are formed by species of the dinoflagellate Karenia (Gymnodinium) (Figs. 7.19, 7.59) and by the raphidophytes Chattonella (Fig. 18.3) and Heterosigma (Fig. 18.1(a)). Ciguatoxins are produced by species of the tropical and subtropical benthic dinoflagellate Gambierdiscus (Figs. 7.6, 7.32). Yessotoxins are produced by the dinoflagellate Proroceratium.

Toxic algae and the end-Permian extinction

All eukaryotic toxic algae contain chloroplast endoplasmic reticulum around the chloroplast and have evolved through a secondary endosymbiosis. Algae derived from secondary endosymbioses evolved during the middle to late Permian Period (Medlin et al., 1997).

There was extinction of approximately 90% of marine species during the late Permian (about 270 million years ago) (Sepkoski, 1984; Erwin, 1993) (Fig. 23.5). Before this extinction, the Paleozoic oceans were dominated by epifaunal (attached to a substrate in the adult form) invertebrates that were filter feeders, sieving food particles out of the water, or passive carnivores. The Permian Period is demarcated from the Triassic by the extinction of

this fauna, and this boundary established the close of the Paleozoic era from the start of the Mesozoic era. The Mesozoic oceans comprise a different fauna with a much reduced number of filter feeders. The animals were more highly mobile with an expansion of predators and of a fauna that burrowed more deeply into the sediment.

Thus, the marine fauna that suffered the greatest extinction at the end of the Permian was attached to the seafloor in the adult form and filtered organic material from the water. In addition, those marine invertebrates with larvae that filtered plankton from the seawater had greater extinction rates than those invertebrates that did not feed on plankton (Christiansen and Fenchel, 1979; Jablonski and Lutz, 1983; Valentine and Jablonski, 1986). Filter feeding by sieving organic material from the seawater appears to be the one unifying characteristic of invertebrates that became extinct during the late Permian.

The evolution of toxic algae derived from secondary endosymbioses paralleled the decline of invertebrates during the end-Permian extinction. It appears that the attached filter-feeding invertebrates that characterized the Paleozoic seas were susceptible to the toxins produced by the newly evolved algae at the end of the Permian Period. This resulted in selective pressure that resulted in their decline and the evolution of a new fauna that was more mobile and less susceptible to the toxic algae in the marine environment.

Fig. 23.5 Location of the end-Permian extinction in the

geological time scale.

ALGAE AND THE ENVIRONMENT	511

Cooling of the Earth, cloud condensation nuclei, and DMSP

Algae adjust to changes in external salt concentration by adjusting the osmolarity of the cell protoplasm through the production of glycerol in freshwater algae (Fisher et al., 1994) or dimethylsulfoniopriopionate (DMSP) in marine algae (Wolfe et al., 1997). The higher the external salt concentration, the greater the concentration of glycerol or DMSP in the protoplasm. DMSP and glycerol are used because they do not interfere with cellular function as do some organic salts (Keller and Korjeff-Bellows, 1996).

The production of DMSP by marine algae is an important factor in the formation of clouds and the temperature of the Earth’s atmosphere. After a marine alga dies, DSMP is released into the ocean where it is broken down into the gas dimethyl sulfide (DMS) and propenoic acid (acrylic acid) (Fig. 23.6) (Liss et al., 1997). Dimethyl sulfide gas dissolves in the seawater and eventually some dimethyl sulfide escapes into the atmosphere. In the atmosphere, dimethyl sulfide is oxidized into methane sulfonic acid (MSA) and sulfuric acid. MSA and sulfuric acid have relatively low vapor pressures so they precipitate into atmospheric aerosols that produce cloud condensation nuclei. Cloud condensation nuclei are small particles of hygroscopic material on which liquid water condenses (Cox, 1997). This produces rain and cloud albedo. Albedo refers to the ability of clouds to reflect sunlight back out of the atmosphere. The more clouds the greater the reflectivity and albedo, and the less heating of the Earth (Charlson et al., 1987). This counters heating of the Earth by the greenhouse effect where anthropogenic (related to human activities) burning of fossil fuels has resulted in increased atmospheric carbon dioxide concentrations and heating of the Earth (Jones and Slingo, 1997).

Atmospheric sulfuric acid is also produced by burning of fossil fuels. Anthropogenic sulfuric acid in the atmosphere is mostly over land and in the Northern Hemisphere (Liss et al., 1997). In contrast, over the oceans, cloud condensation nuclei are produced mostly from dimethyl sulfide oxida-

tion. Prymnesiophytes (haptophytes) and dinoflagellates produce more DMSP per cell than other marine algae (e.g., diatoms) and are the main contributors to the cloud condensation nuclei over oceans (Malin, 1996).

Marine flagellates may use DMSP (instead of glycerol) as an osmolyte because its degradation of DMSP produces propenoic (acrylic) acid. Acidifying seawater makes more carbon dioxide available for photosynthesis (see section on evolution of chloroplast endoplasmic reticulum). Although propenoic acid is metabolized by bacteria, the release of large quantities of propenoic acid from blooms of the prymensiophyte Phaeocystis appears to prevent growth of other microorganisms in the water for some time after the bloom (Savage, 1930).

Chemical defense mechanisms of algae

Herbivore grazing on macroalgae and predation by invertebrates on microalgae cause the greatest loss of algal biomass. Algae have evolved chemical defense mechanisms that can be defined as constitutive or inducible:

1Constitutive defense. The chemicals involved in defense are present all of the time. An example is the toxic “red tide” dinoflagellates that have reduced grazing by copepods (Wolfe, 2000). Coccolithophorids are another example. Emiliana huxleyi has an increased amount of dimethylsulfonopropionate (DMSP) when it is grazed by invertebrates. DMSP lyase breaks down DMSP into dimethylsulfide and acrylate (Fig. 23.6). Water containing the latter

compound is avoided by grazing protozoans (Strom et al., 2003).

2Inducible defense. The chemicals that function in defense are only produced when the alga is under pressure from a consuming organism. Chemicals are costly for the alga to produce so it is more economical for the algal cells to produce the chemicals only when in danger of being consumed. Examples of inducible defense chemicals are the increased production of phlorotannins by brown algae,

512 CHLOROPLAST E.R.: EVOLUTION OF TWO MEMBRANES

Fig. 23.6 The mechanism by which DMSP produces clouds

and cooling in the atmosphere.

ALGAE AND THE ENVIRONMENT	513

and the increased production of halogenated furones by red algae, on grazing by invertebrates (Pavia et al., 2003).

Defense chemicals can also be divided into:

•seriochemicals, which act between individuals of the same species. Pheromones that function in sexual reproduction are examples of seriochemicals.

•allelochemicals, which act between members of different species. Kairomones and synomones are examples of allelochemicals (Cembella, 2003).

Kairomones are chemicals secreted by a predator that induce changes in the behavior, morphology, or life history of the prey.

1Kairomones can be noxious compounds produced by the prey to act as feeding deterrents via olfactory or gustatory responses of the predator at the preingestive stage. Such contact signals could be sequestered on the surface of the prey cells or released into the medium. Often their main purpose would not be to intoxicate the predator, but to discourage “tasting” or to initiate rapid release of the prey following physical handling and capture. For example, grazing experiments exposing the

tintinnid Favella ehrenbergi to cells of the toxic dinoflagellate Alexandrium resulted in the ciliate swimming in retrograde (avoidance) manner once a threshold of dinoflagellate cells was reached (Hansen

et al., 1992).

2Kairomones can be toxic compounds released from ingested cells that result in physical incapacitation or mortality of the predator. The prymnesiophyte alga Phaeocystis contains large amounts of - dimethylsulfoniopropionate (DMSP). Ingestion of the alga releases the intracellular DMSP resulting in reduced grazing by the heterotrophic dinoflagel-

lates Amphidinium, Gymnodinium, Oxyrrhis, and the ciliate Coxliella (Strom et al., 2003).

3Kairomones can be “stealth compounds” of low acute toxicity to adult predators that lead to postdigestive reduction in fecundity (ability

to produce offspring). Postdigestive deterrence would obviously be ineffective for the protection of the individual ingested cell, but group defense would be maintained on a community basis. For example, the ingestion of high concentrations of diatoms by copepods results in the low viability of eggs of the nauplii (larvae) of the copepods (Paffenhofer, 2002; Ianora et al., 2003).

Synomones are produced by prey species to attract predators of their predators at the next level of the food web.

The Antarctic and Southern Ocean

The phytoplankton in the waters around Antarctica support a plethora of marine life. Easterly winds next to the Antarctic continent drive the Antarctic Coastal Current or East Wind Drift (Fig. 23.7). North of this, westerly winds drive one of the largest current systems of Earth, the

Antarctic Circumpolar Current or West Wind Drift (Garrison and Siniff, 1986). This current flows unobstructed around Antarctica, transporting two to three times more water than the Gulf Stream. A region of upwelling occurs between the Antarctic Coastal Current and Antarctic Circumpolar Current. This area of upwelling pulls nutrient-rich deep water to the surface. This nutrient-rich water spills over all the Antarctic waters creating an environment for phytoplankton blooms. The Southern Ocean, comprising about 10% of the world ocean, occurs between the Antarctic continent and the outer edge of the Antarctic Circumpolar Current. There is an intense bloom of phytoplankton in the Southern Ocean during the austral (southern) summer that provides energy for marine food webs. Zooplankton, particularly the Antarctic krill (Euphasia superba), are abundant, providing a food source for vertebrate populations.

The sea ice surrounding the Antarctic continent can be divided into (1) land-fast ice that persists all year long and (2) pack ice that breaks up during the austral summer (December–March) (Fig. 23.7). There are two basic algal communities that exist in the ice in the Antarctic: