CYANOBACTERIA 59

Fig. 2.41 Cyanobacteria in an endosymbiotic relationship with corals are able to maintain anaerobic conditions necessary for nitrogenase activity by the Mehler reaction. The dinoflagellate zooxanthellae produce glycerol which is transferred to the cyanobacteria. Glycolytic breakdown of glycerol produces hydrogen atoms that reduce oxygen molecules produced in photosynthesis. This creates the hypoxia necessary for nitrogenase activity and nitrogen fixation.

Ecology of cyanobacteria

Marine environment

Littoral zone

Cyanobacteria in the littoral zone occur as a black encrusting film on rocks at the upper limit of the high-tide mark. This zone is sandwiched

between the lower barnacle zone (the grazing of the molluscs in this zone limits the cyanobacteria) and a higher zone of maritime lichens such as Verrucaria and Lichina (Fig. 2.38), the latter containing the cyanobacterium Calothrix (Fig. 2.42(d)) as the phycobiont. The brackish cyanobacterial zone is composed of various species of Calothrix (Fig. 2.42(d)), Phormidium (Figs. 2.18(c), 2.56(c)), Nodularia (Fig. 2.42(a)), Gloeothece (Fig. 2.56(a)), and Rivularia (Fig. 2.57(d)) (Little, 1973). The vertical extent of this zone tends to be greater with increasing exposure of the shore; the greater the spray, the wider the zone. In most exposed areas it forms a thin, adhering film, but in sheltered areas the growth may be much thicker, up to 5 mm. The nature of the rock is of some importance, with soft or granular rocks such as chalk

Fig. 2.42 (a) Nodularia spumigena.

(b) Lynbya sordida.

(c) L. majuscula. (d) Calothrix

scopulorum. (e) Microcoleus

(a)

chthonoplastes. (H) Heterocyst. ((b),(c),(e), after Desikachary, 1959.)

(b)

(c)		(d)
				(e)

60 THE PROKARYOTIC ALGAE

Fig. 2.43 Left: The endolith Hyella immanis inside a carbonate ooid sand grain. Right: The fossil endolith Eohyella dichotoma penetrating an ooid sand grain from the Late Proterozoic. (From Al-Thukair and Golubic, 1991.)

and sandstones, respectively, sustaining the greatest growth. Most of the cyanobacteria in the littoral zone are nitrogen fixing, and they make a significant contribution to the productivity of rocky shores and coral reefs (Mague and HolmHansen, 1975).

Ooids are spherical (0.2–2.0 mm in diameter), concentrically laminated, carbonate grains that form by carbonate accretion in agitated, shallow tropical marine environments. Hyella spp. are cyanobacterial endoliths that bore into, and live in, ooids (Fig. 2.43) (Al-Thukair and Golubic, 1991). Extant Hyella spp. are similar to extinct Eohyella in 800 million-year-old ooids (Fig. 2.43).

Open ocean cyanobacteria

In the open ocean, most of the total photosynthetic capacity is made up of pico- phytoplankton (phytoplankton cells unable to pass through a filter with 2- m-diameter holes). The picophytoplankton is made up principally of tiny coccoid cyanobacteria at concentrations of around 10 000 cells per milliliter (Glover et al., 1986). The coccoid cyanobacteria Synechococcus (Figs. 2.19(c), 2.31), Synechocystis (Fig. 2.8), and Prochlorococcus are the major organisms present (Ferris and Palenik, 1998). Although these cyanobacteria are small, they can be easily seen

because their phycobiliproteins undergo autofluorescence in a fluorescence microscope. The picophytoplankton cyanobacteria have negligible sinking rates; thus they are ideally suited for planktonic life. The high surface : volume ratios, combined with steep diffusion gradients that are set up around small cells, allow them to take up nutrients at a high rate. Furthermore, a given amount of photosynthetic pigment dispersed in small cells absorbs more light than an equivalent amount of pigment packaged in large cells. Therefore, these cells grow best at low light intensities of less than 1⁄50 of full sunlight. The picophytoplanktonic cyanobacteria are more evident in nutrient-poor offshore waters where larger phytoplankton are less successful, because the larger phytoplankton are less able to utilize low concentrations of nutrients. Although the picophytoplanktonic cyanobacteria occur throughout the euphotic zone, they are concentrated at the bottom of the zone, not because they sediment out, but because they grow best under these conditions; they use the low irradiance efficiently to support growth and benefit from nutrients transported up from richer waters below. These algae contain large amounts of phycoerythrin that allows them to absorb the blue-green light penetrating into deep water (Fogg, 1986).

Cyanobacteria larger than picophytoplankton often form a significant part of oceanic phytoplankton. Massive development of filaments of the nitrogen-fixing Trichodesmium (Figs. 2.31,

CYANOBACTERIA 61

2.56(g)) (Carpenter et al., 1992) occurs in certain tropical waters. Each colony of Trichodesmium consists of a mass of filaments that secrete a flocculent mucilage which supports bacterial colonies; these in turn are fed on by different protozoa. The large surface area produced by the algal filaments forms a miniature ecosystem (Andersen, 1977). Trichodesmium is a major component of the Caribbean Sea plankton, comprising 60% of the total chlorophyll a in the upper 50 m and about 20% of the primary production. It is also an important source of nitrogen, fixing 1.3 mg of nitrogen per square meter per day (Carpenter and Price, 1977). The cells produce gas vacuoles which, under calm conditions, cause the cells to accumulate at the water surface, giving rise to the phenomenon known to sailors as “sea sawdust,” or long orange or gray windrows of algae. One such bloom stretched 1600 km along the Queensland coast of Australia, extending from the shore to the Great Barrier Reef, and occupying an area of 52 000 km2 (Ferguson-Wood, 1965). Trichodesmium also occurs in the Red Sea and it was probably the color produced by blooms of the alga that gave the Red Sea its name (Hoffman, 1999).

Trichodesmium moves up in the water column by means of gas vesicles, and moves down in the water column by carbohydrate ballasting (Romans et al., 1994). The cells become progressively heavier from morning to evening as carbohydrates and polyphosphate bodies are produced. In the Caribbean, Trichodesmium cells have been found down to 200 m. The gas vesicles of this cyanobacterium are much stronger and more difficult to collapse than those found in any freshwater alga (Walsby, 1978). The gas vesicles are able to stand up to 20 atm of pressure, enabling Trichodesmium to rise from great depths.

Freshwater environment

Freshwater blooms of cyanobacteria are common. Most freshwater blooms of cyanobacteria consist of Microcystis (Figs. 2.48, 2.56(b)), Anabaena (Figs. 2.16, 2.18(d), 2.57(b)), Aphanizomenon (Fig. 2.57(b)), Gloeotrichia (Fig. 2.18(a)), Lyngbya (Fig. 2.42(b), (c)) or Oscillatoria (Fig. 2.19(a), (b)). Although they occur in lakes over the whole year, it is usually only in late summer and early autumn that they reach bloom proportions.

This because of (Tang et al., 1997):

1the superior light-capturing abilities of cyanobacteria when self-shading is the greatest.

2their high affinity for nitrogen and phosphorus when nutrient limitation is most

severe.

3their ability to regulate their position in the water column by gas vacuoles to take advantage of areas richer in nutrients and/or light.

4their higher temperature optima for growth and photosynthesis (greater than 20 °C).

Similar to marine environments, freshwater plankton is dominated by the picoplankton cyanobacteria, particularly species of Synechococcus (Fig. 2.31) (Postius and Ernst, 1999).

Even in the Arctic and Antarctic, cyanobacteria dominate the algal flora in the late summer. These cyanobacteria are psychrotrophs, able to tolerate the severe conditions during the winter and then grow in the warmer summer months (as contrasted to psychrophiles that are able to grow at temperatures less than 15 °C; (Tang et al., 1997; Nadeau and Castenholz, 2000).

Hot-spring cyanobacteria

Cyanobacteria are important in the colonization of non-acidic hot springs throughout the world. Some cyanobacteria have the ability to grow at temperatures as high as 70 to 73 °C, a much higher temperature tolerance than occurs in eukaryotic algae. In thermal environments above 56 to 60 °C, both photosynthetic and nonphotosynthetic eukaryotic algae are always absent. In acid springs (pH less than 4), no cyanobacteria are present, and at temperatures above 56 °C in these springs there are no photosynthetic organisms at all (Brock, 1973). Mastigocladus laminosus (Fig. 2.44(a)) is a cyanobacterium that occurs in thermal springs throughout the world, whereas other cyanobacteria such as

Synechococcus lividus and Oscillatoria terebriformis have more restricted ranges (Castenholz, 1973). The cyanobacteria normally occur as mats mixed with flexibacteria, the cyanobacteria usually being more prevalent in the upper portion of the mat. The thermophilic cyanobacteria are especially adapted to live at elevated temperatures.

62 THE PROKARYOTIC ALGAE

(b)

(c)

(d)

(a)

Fig. 2.44 (a) Mastigocladus laminosus. (H) Heterocyst. (b)

Porphyrosiphon notarisii. (c) Microcoleus vaginatus. (d)

Plectonema notatum. ((c),(d) after Prescott, 1962.)

Synechococcus lividus can grow at temperatures up to 73 °C but ceases to grow in culture when the temperature is lowered to 54 °C, with optimum growth occurring from 60 to 63 °C (Meeks and Castenholz, 1971); the cells will die if kept at 30 °C for 10 days. Enzymes isolated from thermal algae are more stable at higher temperatures than those from other organisms. For example, NADPH2-cytochrome c reductase extracted from the thermal alga Aphanocapsa thermalis showed unimpaired activity after heating to 85 °C for 5 minutes, whereas that from Anabaena cylindrica was completely inactivated by a similar treatment.

Terrestrial environment

Terrestrial cyanobacteria play a major role as primary colonizers in the establishment of a soil flora and in the accumulation of humus. They do this in four main ways:

1They bind sand and soil particles and prevent erosion. They do this with their gelatinous sheaths and by their growth pattern which produces closely intertwined rope-like bundles in and among soil particles. Genera that commonly perform this function are Porphyrosiphon (Fig. 2.44(b)) which covers large eroded areas in Brazil (Drouet, 1937),

Microcoleus (Figs. 2.44(c), 2.45), Plectonema

(Fig. 2.44(d)), Schizothrix and Scytonema (Figs. 2.58(c), (d), 2.59).

2They help to maintain moisture in the soil. Booth (1941), in studies in Oklahoma, found that soil with an algal covering had a moisture content of 8.9% compared to 1.3% in the absence of algae.

3They are important as contributors of combined nitrogen through nitrogen fixation. In grasslands, the soil surface between crowns of grasses may support extensive zones of cyanobacteria and lichens that include cyanobacteria as their phycobiont constituting up to 20% of the ground cover (Kapustka and

DuBois, 1987).

4It has been suggested that cyanobacteria assist higher plant growth by supplying growth substances.

Anhydrobiotics are organisms that can withstand the removal of the bulk of their intracellular water for extended periods of time. The cosmopolitan terrestrial cyanobacterium Nostoc commune is able to tolerate acute water stress and can survive in the air-dry state for many years. Approximately 0.1 g of blackened air-dried colonies becomes an olive-green rubbery mass of more than 20 g wet weight within 30 min of rehydration. In Nostoc commune (Fig. 2.46), rehydration rather than desiccation appears to be the fatal event. To protect the cells during rehydration, a water stress protein and large amounts of the sugar trehalose are

CYANOBACTERIA 63

Fig. 2.45 Scanning electron micrographs of Microcoleus vaginatus. Left: Filament. Right: Filament with clay particles and sand grains embedded in the slime surrounding the cell walls. (From Belnap and Gardner, 1993.)

synthesized that stabilize the phospholipid bilayers of cellular membranes (Potts, 1996, 1999; Qiu et al., 2004).

Cyanobacteria comprise the dominant component of the soil photosynthetic community in hot and cold arid regions where higher plant vegetation is absent or restricted. Desert cryptobiotic crusts are initiated by the growth of cyanobacteria in the soil during episodic events of available moisture. The only cyanobacteria that are initial colonizers are those that have heterocysts, and are therefore able to fix nitrogen; and those cyanobacteria that produce scytonemin, a sunscreen that

accumulates in the cyanobacterial sheaths and absorbs some of the strong sunlight in the near ultraviolet (370–384 nm) (Dillon and Castenholz, 1999). Microcoleus vaginatus (Fig. 2.45) makes up over 90% of cryptobiotic crusts in the arid soil of the Colorado Plateau in the United States (Belnap and Gardner, 1993). Filaments of M. vaginatus are surrounded by thick mucilaginous sheaths that can absorb eight times their weight in water, increasing the water capacity of sandy soils. Clay particles and sand grains become trapped in the cyanobacterial sheaths (Fig. 2.45). The clay particles are negatively charged and bind positive cationic nutrients (e.g., K , Ca2 ) preventing them from leaching into the subsoil. Subsequently, lichens, fungi and moss establish themselves in the crust, enriching and stabilizing the soil.

(a)

(b)

(f )

		(d)
				(e)
(c)

Fig. 2.46 (a) Aulosira fertilissima.

(H) Heterocyst. (b) Nostoc commune.

(c,d) N. verrucosum. (e) Scytonema hofmanni. (f) Chamaesiphon sp., showing formation of exospores. ((a),(e) after Desikachary, 1959;

(b) after Prescott, 1962; (f) after

Waterbury and Stanier, 1977.)