EVOLUTIONARY BIOLOGY: ON THE EVOLUTION OF PHYTOPLANKTON

http://scienceweek.com/2004/sa040910-1.htm

ScienceWeek EVOLUTIONARY BIOLOGY: ON THE EVOLUTION OF PHYTOPLANKTON

The following points are made by P.G. Falkowski et al (Science 2004 305:354):

1) Coined in 1897, the term "phytoplankton" describes a diverse, polyphyletic group of mostly single-celled photosynthetic organisms that drift with the currents in marine and fresh waters (1). Although accounting for less than 1% of Earth's photosynthetic biomass, these microscopic organisms are responsible for more than 45% of our planet's annual net primary production. Whereas on land, photosynthesis is overwhelmingly dominated by a single clade (the Embryophyta) containing nearly 275,000 species, there are fewer than 25,000 morphologically defined forms of phytoplankton; however, they are distributed among at least eight major divisions or phyla.

2) Numerically, the vast majority of phytoplankton in the contemporary oceans is composed of cyanobacteria, the only extant prokaryotic group of oxygenic photoautotrophs. The basic photosynthetic apparatus in all cyanobacteria consists of two photochemical reaction centers, designated Photosystem I (PSI) and PSII (3). PSII oxidizes water and passes the electrons through a cytochrome b6/f complex to PSI, while simultaneously creating a cross-membrane proton gradient that is used to generate adenosine 5'-triphosphate (ATP). PSI, operating in series with PSII, generates a biochemical intermediate with a sufficiently low redox potential to drive the enzymatic reduction of CO2 to form organic molecules. Because water provided a virtually infinite supply of reductant for carbon fixation (4), within several hundred million years oxygenic photoautotrophs spread across the sunlit surface of the planet, making possible the oxidation of Earth's surface oceans and atmosphere 2.4 billion years ago (Ga) (5).

3) Oxygenic photosynthesis appears to have evolved only once, but it subsequently spread via endosymbiosis to a wide variety of eukaryotic clades. The earliest oxygenic photosynthetic eukaryotes are thought to have arisen from the wholesale engulfment of a coccoid cyanobacterium by a eukaryotic host cell that already contained a mitochondrion. The engulfed cyanobacterium would become a membrane-bounded organelle called the "plastid". The mitochondrion and plastid are the only two organelles that appear to have been appropriated via endosymbioses. Gene loss through time essentially reduced both symbionts to metabolic slaves within their host cells.

4) A schism early in the evolution of oxygenic eukaryotic photoautotrophs gave rise to two major plastid lineages. One group, united by the use of chlorophyll b as an accessory pigment, is overwhelmingly dominated by the green algae and their descendants, the land plants. Collectively, this "green" plastid lineage is much more closely related by plastid phylogeny and photosynthetic physiology than by the evolutionary history of the host cells. The second lineage includes the red algae (rhodophytes), which retain the most features of cyanobacterial pigmentation, and a diverse set of phytoplankton and seaweeds whose plastids (but again, not their host cells) are evolutionarily derived from rhodophytes. With the exception of the red algae themselves, members of this "red" plastid lineage utilize chlorophyllide c and its derivatives as accessory photosynthetic pigments. Of the eight major eukaryotic phytoplankton taxa in the contemporary ocean, all but one possess "red" plastids. In contrast, with the minor exception of some soil-dwelling diatoms and xanthophytes, all terrestrial algae and plants have "green" plastids.

5) In summary: The community structure and ecological function of contemporary marine ecosystems are critically dependent on eukaryotic phytoplankton. Although numerically inferior to cyanobacteria, these organisms are responsible for the majority of the flux of organic matter to higher trophic levels and the ocean interior. Photosynthetic eukaryotes evolved more than 1.5 billion years ago in the Proterozoic oceans. However, it was not until the Mesozoic Era (251 to 65 million years ago) that the three principal phytoplankton clades that would come to dominate the modern seas rose to ecological prominence. In contrast to their pioneering predecessors, the dinoflagellates, coccolithophores, and diatoms all contain plastids derived from an ancestral red alga by secondary symbiosis.

References (abridged):

1. P. G. Falkowski, J. A. Raven, in Aquatic Photosynthesis (Blackwell Scientific, Oxford, 1997), p. 375

2. C. Field, M. Behrenfeld, J. Randerson, P. Falkowski, Science 281, 237 (1998)

3. Structural and sequence analyses indicate that the reaction center of PSII is derived from purple nonsulfur bacteria, whereas that from PSI is derived from green sulfur bacteria, neither of which can split water to form oxygen (81)

4. J. A. Raven, P. G. Falkowski, Plant Cell Environ. 22, 741 (1999)

5. J. Farquhar, H. Bao, M. Thiemens, Science 289, 756 (2000)

Science http://www.sciencemag.org

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Related Material:

ON PHYTOPLANKTON

The following points are made by Jed Fuhrman (Nature 2003 324:1001):

1) With the sequencing of microbial genomes now almost routine in some circles, one could be forgiven for feeling a little jaded. It is possible to lose sight of just how much can be learned from such an exercise. But recent reports powerfully demonstrate how genomic studies can lead to a new understanding of biodiversity, ecology, biological efficiency and biogeochemistry.

2) About half of global photosynthesis and oxygen production is accomplished by single-celled planktonic organisms (phytoplankton) that live in the top layer of the ocean, where enough light penetrates to support their growth. The most plentiful of these are the cyanobacteria -- tiny, chlorophyll-containing phytoplankton that have no membrane-bound nucleus. There are two basic types. The Synechococcus strains have a diameter of about 0.9 microns and were discovered to be abundant in seawater in 1979. With a diameter of about 0.6 microns, meanwhile, the Prochlorococcus strains are the smallest of all the phytoplankton; they are also the most abundant, yet were discovered only 15 years ago.

3) The complete genomes of three strains of Prochlorococcus and one strain of Synechococcus have recently been sequenced and analyzed. The results are remarkable for what they show not only about the differences between these close relatives, but also about the extent to which some strains economize on DNA. Indeed, two of the Prochlorococcus strains have genomes so small -- about 1.7 million base pairs -- that they might represent the minimal genome of an oxygen-generating, photosynthetic organism.

4) Why economize on DNA? A genome represents the complete genetic repertoire of an organism: it contains specifications for all the machinery needed to create the organism and to regulate its operation, growth and reproduction. Control of genome size involves a trade-off between efficiency and versatility. A small genome reduces the amount of extra "baggage" that must be maintained and propagated, but also limits an organism's ability to exploit different resources. Larger genomes provide for this possibility, and also permit back-up should a gene be damaged or lost. But they require more material and energy to maintain.

Nature http://www.nature.com/nature

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DEFENSE MECHANISMS IN PHYTOPLANKTON

The following points are made by Victor Smetacek (Nature 2001 411:745):

1) Forests and algal *blooms fix approximately the same amount of carbon (a few grams per square meter per day), because both are based on essentially the same photosynthetic machinery fuelled by *chlorophyll-alpha in *chloroplasts, the descendants of free-living *cyanobacteria that have since evolved into plant organelles by *endosymbiosis. Chloroplasts provide their host cells with food in return for resources and protection. The range of defense systems in phytoplankton is only now coming to light.

2) The size range of phytoplankton spans 3 orders of magnitude, but that of its predators spans 5 orders of magnitude, from micron-scale *flagellates to shrimp-sized krill. Pathogens (viruses and bacteria) pose a further challenge. Most predators and pathogens of phytoplankton feed or infect selectively. Smaller predators hunt individual cells, whereas larger predators use feeding currents, mucous nets, or elaborate filters to collect phytoplankton en masse. Captured cells are pierced, ingested, engulfed, or crushed, but have evolved specific defense measures. The phytoplankton can escape by swimming or by mechanical protection; mineral or tough organic cell walls ward off piercers or crushers. In adapting to the deterrence of predators, phytoplankton cells have increased in size, formed large chains and colonies, or grown spines. Noxious chemicals also provide defense.

Nature http://www.nature.com/nature

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Notes by ScienceWeek:

phytoplankton: Small, usually microscopic, aquatic plants capable of photosynthesis; e.g., unicellular algae. Phytoplankton and plankton are not equivalent. The term "plankton" is a general designation for various drifting microscopic aquatic organisms in the upper regions of the oceans, both photosynthetic and non-photosynthetic.

blooms: In this context, the term "bloom" refers to an explosive increase in the density of phytoplankton within an area.

chlorophyll-alpha: (chlorophyll-a) Chlorophylls are magnesium complexes of various closely related porphyrins or chlorins. Chlorophylls a and b are dihydroporphyrins.

chloroplasts: The chloroplasts containing several photosynthetic pigments (chlorophylls). Chloroplasts are found in all photosynthetic plant cells, but not in photosynthetic prokaryotes (i.e., not in cells without membrane-bound organelles). The typical higher plant chloroplast is lens-shaped, approximately 5 microns across the larger dimension, and the number of chloroplasts per cell can vary from 1 to 100 depending on the type of cell. A mature chloroplast is typically bounded by two membranes, an inner membrane and an outer membrane, the membranes possessing significantly different chemical constituents. In addition to a number of enzymes involved in photosynthesis, chloroplasts also contain in their interior a circular DNA molecule and protein synthetic machinery typical of prokaryotes. The current consensus is that chloroplasts may have originated from *cyanobacteria that became endosymbionts.

cyanobacteria: A phylum of bacteria characterized by blue-green (cyan) photosynthetic pigments, abundant in a variety of habitats, particularly in fresh water and soil. Cyanobacteria are responsible for generating a large portion of the free oxygen in the Earth's atmosphere. They apparently produced stromatolite limestone deposits, as well as the bulk of modern petroleum deposits. (Stromatolites are laminated calcareous microbial fossil deposits formed principally by cyanobacteria and algae.)

endosymbiosis: An arrangement in which one organism lives inside another organism, but the term is usually restricted to arrangements of mutual benefit, thus not including parasite-host relationships. A number of eukaryotic cell organelles (including mitochondria) are believed to have originated from endosymbiotic relationships between eukaryotic cells and simpler cells.

flagellates: Organisms possessing one or more flagella. A flagellum is a long threadlike extension providing locomotion for a cell.

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