The algae in the Heterokontophyta usually have cells with an anterior tinsel and posterior whiplash flagellum (Fig. 10.1). The plastids contain chlorophylls a and c along with fucoxanthin. The storage product is usually chrysolaminarin in cytoplasmic vesicles.

Based on molecular evidence (Horn et al., 2007 ; Kai et al., 2008 ; Schmidt et al., 2012 ; Yang et al., 2012), the algae in the Heterokontophyta can be divided into three clades.

Since some of these classes have only a few representatives, and because this is a basic textbook, I have chosen not dealt with the algae in the Synchromophyceae, Chrysomerophyceae, Schizocladiophyceae, and Aurearenophyceae. The following classes are covered here (Andersen, 2004):

Chrysophyceae (golden-brown algae) (Chapter 10)

Synurophyceae (Chapter 11)

Eustigmatophyceae (Chapter 12)

Pinguiophyceae (Chapter 13)

Dictyochophyceae (silicoflagellates) (Chapter 14)

Pelagophyceae (Chapter 15)

Bolidophyceae (Chapter 16)

Bacillariophyceae (diatoms) (Chapter 17)

Raphidophyceae (chloromonads) (Chapter 18)

Xanthophyceae (yellow-green algae) (Chapter 19)

Phaeothamniophyceae (Chapter 20)

Phaeophyceae (brown algae) (Chapter 21).

CHRYSOPHYCEAE

The Chrysophyceae are distinguished chemically by having chlorophylls a, c 1, and c 2 (Andersen and Mulkey, 1983) and structurally by two flagella inserted into the cell perpendicular to each other, one photoreceptor on the short flagellum that is usually shaded by an eyespot in the anterior portion of the chloroplast, contractile vacuoles in the anterior portion of the cell, chloroplast endoplasmic reticulum, and radially or biradially symmetrical silica scales (if they are present). The storage product is chrysolaminarin. Many members of the class produce statospores enclosed in a silicified wall with a terminal pore. The Chrysophyceae/Synurophyceae probably originated about 268 Ma (million years ago) (Brown, 2010).

Most of the species in the Chrysophyceae are freshwater species, and occur in soft waters (low in calcium). Many of the freshwater species are in the plankton of lakes where they are present in abundance. The coccoid and filamentous genera are found mostly in cold springs and brooks, where they occur as gelatinous or crustous growths on stones and woodwork.

The Raphidophyceae, or chloromonads, have chlorophylls a and c, and two membranes of chloroplast endoplasmic reticulum. The anterior flagellum is commonly tinsel, whereas the posterior flagellum is naked (Figs. 18.1, 18.2, 18.3). The freshwater species of the Raphidophyceae are green, whereas the marine forms are yellowish and contain the carotenoid fucoxanthin (Vesk and Moestrup, 1987). The closest relatives of the Raphidophyceae are the Eustigmatophyceae and the Chrysophyceae (Cavalier-Smith and Chao, 1996).

Marine species are euryhaline and eurythermic (tolerant of a wide salinity and temperature range) and occur in temperate and subtropical waters worldwide (Tobin et al., 2013). Marine genera are Chattonella (Fig. 18.3), Fibrocapsa (Fig. 18.1(b)), and Heterosigma (Fig. 18.1(a)). Many of the marine species produce neurotoxic compounds that are similar to brevetoxin (Fig. 18.2). Uptake of the toxin by fish results in depolarization of nerves supplying the heart. This reduces the heart rate, thereby lowering blood pressure, which in turn affects the transfer of oxygen to the gill lamellae, creating hypoxic conditions that lead to fish mortality (Tyrrell et al., 2001).

Toxic red-tide blooms of the marine Chattonella antiqua and Heterosigma carterae (Taylor, 1992) have occurred in the Seto Inland Sea in Japan (Watanabe et al., 1988). These red tides occurred in the summer when a salinity and temperature stratification occurred at a depth of 5–10 m. There was little mixing of waters above and below the stratified layer resulting in the upper layer being deficient in nutrients while the bottom layer was anaerobic. Heterosigma carterae flourishes under these conditions because it has a daily vertical migration of 10–15 m and this allows the alga to move between the stratified layers. This migration enables H. carterae to use the nutrients in the lower layers, and light and oxygen in the upper layer, resulting in the red-tide blooms of the organism. The migration is correlated with the production and degradation of cytoplasmic fat particles (Wada et al., 1987).

Heterosigma carterae has a wide salinity tolerance in culture (3–50%) and loses its motility at temperatures below 10 °C. At 5–10 °C, the alga forms non-motile masses capable of surviving in continuous darkness for up to 15 weeks (Han et al., 2002).

The Pelagophyceae are a group of basically unicellular algae that are cytologically similar to the Chrysophyceae, in which they were previously classified (Andersen et al., 1993). The cells are very small, members of the ultraplankton (cells less than 2 μm) and appear as small spheres with indistinct protoplasm under the light microscope. Recent studies on the sequences of small-subunit RNA nucleotides in these algae have shown them to be closely related to each other and distinct from other members of the Heterokontophyta (Saunders et al., 1997). While these algae have been shown to be distinct from other members of the Heterokontophyta based on molecular data, they do not have cytological or morphological characters which are very different from other members of the phylum.

Pelagomonas calceolata is a very small (1.5 μm. 3 μm) ultraplanktonic marine alga with a single tinsel flagellum and basal body, and a single chloroplast and mitochondrion (Fig. 15.1(c)) (Andersen et al., 1993). Another member of the marine ultraplankton is Pelagococcus subviridis, a green-gold spherical non-motile cell (2.5–3.0 μm) with a single chloroplast, mitochondrion, and nucleus (Fig. 15.1(a)) (Vesk and Jeffery, 1987).

Members of the class are economically important because some of the algae produce “brown tides” (Ong et al., 2010). Aureoumbra lagunensis (Fig. 15.1(b)) is the causative agent of brown tides in Texas (DeYoe et al., 1997), while Aureococcus anophagefferens forms brown tides along the coasts of New Jersey, New York, and Rhode Island. The numbers of cells in brown tides can be so large that they can exclude light from the benthic eelgrass (Zostera marine), resulting in elimination of the eelgrass. The larvae of the bay scallop feed off eelgrass, and the bay scallop industry was virtually wiped out for a number of years after a brown tide in the waters off the northeast United States (Nicholls, 1995).

Aureoumbra lagunensis (Fig. 15.1(b)) is able to grow at its maximum rate at salinities as high as 70 PSU (practical salinity units ; seawater is about 35 PSU). Few algae are able to survive these hypersaline conditions. In addition, the surface of the cells are covered with a slime layer that reduces predation (Liu and Buskey, 2000).

The Cyanophyceae or blue-green algae are, today, usually referred to as the cyanobacteria (blue-green bacteria). The term cyanobacteria acknowledges that these prokaryotic algae are more closely related to the prokaryotic bacteria than to eukaryotic algae.

It has been hypothesized that the cyanobacteria evolved in freshwater at some time before 2.50 billion years ago (bya) (Blank, 2013) and that they spread into the marine environment at about the time of the Great Oxidation Event (GOE) (about 2.35 bya) where, through photosynthesis, the cyanobacteria raised oxygen levels in the atmosphere, enabling the evolution of aerobic life and dramatically changing life on the planet (Schirrmeister et al., 2014). The argument for a freshwater evolution of the cyanobacteria (Blank, 2013) involves sucrose synthesis, which originated in the cyanobacteria. Sucrose synthesis is strongly associated with a low-salinity environment.

Cyanobacteria have chlorophyll a (some also have chlorophyll b or d), phycobiliproteins, glycogen as a storage product, and cell walls containing amino sugars and amino acids. At one time, the occurrence of chlorophyll b in cyanobacteria was used as a criterion to place the organisms in a separate group, the Prochlorophyta. Modern nucleic-acid sequencing, however, has shown that chlorophyll b evolved a number of times within the cyanobacteria and the term Prochlorophyta has been discarded (Palenik and Haselkorn, 1992 ; Urback et al., 1992).

Morphology

The simplest morphology in the cyanobacteria is that of unicells, free-living (Figs. 2.14(c)) or enclosed within a mucilaginous envelope (Figs. 2.38, 2.43(a), (b)). Subsequent evolution resulted in the formation of a row of cells called a trichome (Fig. 2.12). When the trichome is surrounded by a sheath, it is called a filament (Fig. 2.12). It is possible to have more than one trichome in a filament (Figs. 2.43(e), 2.45(b)). The most complex thallus is the branched filament (Fig. 2.45(a)). Such a branched filament can be uniseriate (composed of a single row of cells) or multiseriate (composed of one or more rows of cells).

The Prymnesiophyta are a group of uninucleate flagellates characterized by the presence of a haptonema between two smooth flagella. The Prymnesiophyta have two membranes of chloroplast endoplasmic reticulum, as do the Cryptophyta and the Heterokontophyta, but differ in having flagella without mastigonemes. Molecular data also show that the Prymnesiophyta are distinct from the Cryptophyta and Heterokontophyta (Bhattacharya and Ehlting, 1995 ; Medlin et al., 1994). Until 1962, the organisms were considered part of the Chrysophyceae, at which time Christensen split them off into a separate class, the Haptophyceae (named after the presence of the haptonema). The Haptophyceae was a descriptive name and not based on a genus in the class; thus the name was later changed to Prymnesiophyceae, based on the genus Prymnesium (Fig. 22.6) (Hibberd, 1976). The fossil record of the Prymnesiophyceae is known from the Carboniferous (approximately 300 000 000 years ago) (Faber and Preisig, 1994 ; Jordan and Chamberlain, 1997).

The cells are commonly covered with scales. In many cases, the scales are calcified, thereby producing coccoliths. The chloroplasts lack girdle lamellae and most contain chlorophylls a and c 1 / c 2, β-carotene, diadinoxanthin, and diatoxanthin (Zapata et al., 2004 ; Zhao et al., 2015). The storage product is primarily mannitol (Tsuji et al., 2015). The anterior end of the cell has a large Golgi apparatus and sometimes a contractile vacuole.

The Prymnesiophyceae are primarily marine organisms, although there are some freshwater representatives (Shalchian-Tabrizi et al., 2011). While diatoms dominate in nutrient-rich coastal waters, Prymnesiophyceae dominate offshore where nutrients are limiting. Prymnesiophyceae make up a major part of the marine nannoplankton and constitute about 45% of the total phytoplankton cells in the middle latitudes of the South Atlantic. They decrease in frequency toward the poles although some still occur in polar waters (Manton et al., 1977).

Cell Structure

Flagella

Most of the Prymnesiophyceae have two smooth flagella of approximately the same length (Figs. 22.1, 22.2(a)). The Pavlovales is the exception, where one flagellum is longer than the other and is usually covered by small cylindrical to club-shaped hollow scales 70 nm long and 20 nm wide (Fig. 22.2(b)) (van der Veer, 1969 ; Green and Manton, 1970).

The Phaeophyceae, or brown algae, derive their characteristic color from the large amounts of the carotenoid fucoxanthin (Fig. 21.2) in their chloroplasts as well as from any phaeophycean tannins that might be present. The chloroplasts also have chlorophylls a, c 1, and c 2. There are two membranes of chloroplast E.R., which are usually continuous with the outer membrane of the nuclear envelope. The storage product is laminarin (Fig. 21.2). There are no unicellular or colonial organisms in the order, and the algae are basically filamentous, pseudoparenchymatous, or parenchymatous. They are found almost exclusively in the marine habitat, there being only four genera containing freshwater species, that is, Heribaudiella, Pleurocladia, Bodanella, and Sphacelaria (Fig. 21.1) (Schloesser and Blum, 1980). A number of marine forms penetrate into brackish water, where they often form an important part of the salt marsh flora. These brackish water plants have almost totally lost the ability to reproduce sexually, and propagate by vegetative means only. Most of the Phaeophyceae grow in the intertidal belt and the upper littoral region. They dominate these regions in colder waters, particularly in the Northern Hemisphere, where the number of phaeophycean species is less than that of the Rhodophyceae, but the number of phaeophycean plants is much greater. In the tropics, the only place where large numbers of Phaeophyceae are found is the Sargasso Sea of the Atlantic.

The Phaeophyceae probably evolved about 260 Ma ago during the Permian Period (Brown, 2010 ; Kawai et al., 2015) from an organism in the Phaeothamniophyceae, which have motile cells similar to those in the Phaeophyceae, but lack the characteristic unilocular and plurilocular sporangia of the Phaeophyceae (Bailey et al., 1998).

Cell Structure

The cell structure (Fig. 21.3) is in many ways similar to that of the Chrysophyceae, Prymnesiophyceae, Bacillariophyceae, and Xanthophyceae, which are closely related to the Phaeophyceae. The main difference lies in the large amounts of extracellular polysaccharides surrounding the protoplast.

Cell Walls

There are no unicellular members of the Phaeophyceae, so cell walls joining cells are characteristic of the group (Yamagishi et al., 2014). Phaeophycean cell walls are generally composed of at least two layers, with cellulose making up the main structural skeleton (Kloareg and Quatrano, 1988).

This group is composed primarily of flagellates that occur in both marine and freshwater environments. The cells contain chlorophylls a and c 2 and phycobiliproteins that occur inside the thylakoids of the chloroplast. The cell body is asymmetric with clearly defined dorsi-ventral/right-left sides (Figs. 9.1, 9.6). The asymmetric cell shape results in a peculiar swaying motion during swimming. Most cryptophytes have a single lobed chloroplast with a central pyrenoid.

Cell Structure

There are two apically or laterally attached flagella at the base of a depression. Each flagellum is approximately the same length as the body of the cell (Figs. 9.1, 9.2, 9.6). The flagella are anchored in the cytoplasm by microtubular roots, striatedfiber roots, and a rhizostyle (Nam and Shin, 2016). Depending on the species, there are one or two rows of microtubular hairs attached to the flagellum. In Cryptomonas sp., the hairs on one flagellum are 2.5 μm long and in two rows whereas the hairs on the other flagellum are only 1μm long and arranged in a single row (Heath et al., 1970 ; Kugrens et al., 1987). Small organic scales 150 nm in diameter (Fig. 9.1) are common on the flagellar surface and sometimes on the cell body (Lee and Kugrens, 1986). The outer portion of the cell, or periplast (Gantt, 1971), is composed of the plasma membrane and a plate, or series of plates, directly under the plasma membrane, except under the furrow-gullet complex into which the contractile vacuoles empty (Figs. 9.1, 9.2) (Kugrens and Lee, 1987 ; Hoef- Emden, 2014). The number and shape of these plates are used to characterize genera taking into consideration that the haploid and diploid phases of a single genus can have different plates (Hoef- Emden and Melkonian, 2003). New periplast plates are added in an area adjacent to the vestibulum (Brett and Wetherbee, 1996). Sulfated fucose-rich polysaccharides can be excreted outside of the cell (Giroldo and Vieira, 2002).

The chloroplast most likely evolved from a symbiosis between an organism similar to the phagocytic cryptomonad Goniomonas (Figs. 9.5, 9.6) and a red alga (Kugrens and Lee, 1991 ; Liaud et al., 1997 ; McFadden et al., 1994).

The Chlorophyta, or green algae, have chlorophylls a and b, and form starch within the chloroplast, usually in association with a pyrenoid. The Chlorophyta thus differ from the rest of the eukaryotic algae in forming the storage product in the chloroplast instead of in the cytoplasm. No chloroplast endoplasmic reticulum occurs around the chloroplasts. The green algae are classified with the embryophyte higher plants in the Viridiplantae.

The Chlorophyta are primarily freshwater; only about 10% of the algae are marine, whereas 90% are freshwater (Smith, 1955). Some orders are predominantly marine (Caulerpales, Dasycladales, Siphonocladales), whereas others are predominantly freshwater (Ulotrichales, Coleochaetales) or exclusively freshwater (Oedogoniales, Zygnematales). The freshwater species have a cosmopolitan distribution, with few species endemic in a certain area. In the marine environment, the green algae in the warmer tropical and semitropical waters tend to be similar everywhere in the world. This is not true of the Chlorophyta in the colder marine waters; the waters of the Northern and Southern hemispheres have markedly different species. The warmer waters near the equator have acted as a geographical barrier for the evolution of new species and genera.

Cell Structure

In the Chlorophyta, no microtubular hairs occur on the flagella, although fibrillar hairs (Chlamydomonas) and Golgi-produced scales (Pyramimonas (Fig. 5.11), are present in some genera. Cell walls usually have cellulose as the main structural polysaccharide, although xylans or mannans often replace cellulose in the Caulerpales (Huizing et al., 1979). The primitive algae in the Prasinophyceae have extracellular scales, or a wall derived from interlacing scales, composed of acidic polysaccharides (Becker et al., 1996). Algae in the Volvocales have walls composed of glycoproteins (Goodenough and Heuser, 1985).

Chloroplast pigments are similar to those of higher plants; chlorophyll a and b are present. The main carotenoid is lutein. The siphonaceous genera, as well as the unicells Tetraselmis and Mesostigma, are the only green algae to have siphonoxanthin (Fig. 5.1) and its ester siphonein (Yoshi et al., 2003). Accumulation of carotenoids occurs under conditions of nitrogen deficiency, high irradiance, or high salinity (Solovchenko et al., 2010).

The Rhodophyceae, or red algae, comprise the only class in the division Rhodophyta. The Rhodophyceae are probably one of the oldest groups of eukaryotic algae. The red algae are most likely directly descended from a cyanome in the Glaucophyta (see Chapter 3). It is likely that the first red alga evolved into an ecological niche that was unoccupied by cyanobacteria, the only extant photosynthetic alga that evolved oxygen. This ecological niche would have been in waters with a pH less than 5, which, for some unknown reason, cyanobacteria are not able to inhabit (Brock, 1973). Indeed, modern phylogenetic studies utilizing nucleic-acid sequencing have shown that Cyanidium, an alga that lives in acidic waters, is probably the oldest extant red alga (Oliveira and Bhattacharya, 2000).

The Rhodophyceae lack flagellated cells, have chlorophyll a, phycobiliproteins, floridean starch as a storage product, and thylakoids occurring singly in the chloroplast.

A majoity of seaweeds are red algae, and there are more Rhodophyceae (about 4000 species) than all of the other major seaweed groups combined. Although marine red algae occur at all latitudes, there is a marked shift in their abundance from the equator to colder seas. There are few species in polar and subpolar regions, where brown and green algae predominate, but in temperate and tropical regions they far outnumber these groups. The average size of the plants also differs according to geographical region. The larger species of fleshy red algae occur in cool–temperate areas, whereas in tropical seas the Rhodophyceae (except for massive calcareous forms) are mostly small, filamentous plants. The Rhodophyceae also have the ability to live at greater depths in the ocean than do members of the other algal classes. They live at depths as great as 200 m, an ability related to the function of their accessory pigments in photosynthesis. About 200 species of Rhodophyceae occur in freshwater, where they do not reach as great a size as the red seaweeds (Skuja, 1938). The majoity of freshwater red algae occur in running waters of small to midsized streams (Sheath and Hambrook, 1988). Few red algae occur at currents of less than 30 cm s −. This fast flow probably favors red algae because loosely attached competitors are washed out and because of a constant replenishment of nutrients and gases.

The Xanthophyceae contain primarily freshwater and terrestrial algae with a few marine representatives. The class has a poor fossil record. Studies based on molecular genetics indicate the Xanthophyceae probably originated in the Middle Triassic (223 Ma, million years ago)(Brown, 2010) and is most closely related to the Phaeophyceae (Ariztia et al., 1991 ; Potter et al., 1997). Although the class is commonly called the Xanthophyceae, the proper name is the Tribophyceae, since there is no genus in the class that can lend its name to Xanthophyceae (Hibberd, 1981).

The class is characterized by motile cells with a forwardly directed tinsel flagellum and a posteriorly directed whiplash flagellum (Figs. 19.1, 19.4(c)). The chloroplasts contain chlorophylls a and c (Sullivan et al., 1990), lack fucoxanthin, and are colored yellowish-green. The eyespot in motile cells is always in the chloroplast (Figs. 19.1, 19.4(c)), and the chloroplasts are surrounded by two membranes of chloroplast endoplasmic reticulum. The outer membrane of the chloroplast E.R. is usually continuous with the outer membrane of the nucleus. In most non-motile cells the wall is composed of two overlapping halves (Figs. 19.2, 19.3).

Cell Structure

Cell Wall

The cell walls of two Xanthophyceae, Tribonema (Fig. 19.2) (Cleare and Percival, 1973) and Vaucheria (Figs. 19.6, 19.7), are composed of cellulose (Parker et al., 1963). In Vaucheria cellulose comprises 90% of the wall, with the remaining portion being amorphous polysaccharides composed primarily of glucose and uronic acids. Many of the algae in the class have walls composed of two overlapping halves that fit together as do the two parts of the bacteriologist's Petri dish (Figs. 19.2, 19.3). The two-part nature of the wall cannot be delineated with the light microscope unless the cells have been treated with certain reagents such as concentrated potassium hydroxide. A typical example is the wall of Ophiocytium majus (one study places Ophiocytium in the closely related Eustigmatophyceae based on the sequence of mitochondrial cytochrome oxidase (Ehara et al., 1997)), which is tubular in shape (Fig. 19.3). The wall is composed of two parts, a cap of constant size fitted over a tubular basal portion.