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CLASSIFICATION OF THE ALGAE

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Huisman & Saunders : Phylogeny and Classification: 1 PHYLOGENY AND CLASSIFICATION OF THE ALGAE

John M. Huisman1 & Gary W. Saunders2

 

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Huisman & Saunders : Phylogeny and Classification: 1 PHYLOGENY AND CLASSIFICATION OF THE ALGAE

John M. Huisman1 & Gary W. Saunders2

Introduction

It is commonly held that algae are ubiquitous organisms, found worldwide in virtually all habitats. The limits to their distribution are seemingly non-existent: most people will be accustomed to seeing a green scum during a lakeside walk, or large kelps along a rocky coastline, but few could imagine finding algal cells living in the flesh of corals, or breaking open rocks to reveal these simple photosynthetic organisms beneath the surface! For it is true that even in the harshest of environments, from dry deserts to snowfields to hot springs, one will almost certainly encounter algae.

From this seemingly universal presence it would be easy to conclude that the algae are a particularly successful group - one that has flourished in all manner of circumstances and inhabits the seemingly inhospitable - but, in truth, their widespread distribution can be attributed only partly to their purported success as colonisers. The broad range of habitats occupied by the algae is also a reflection of their broad evolutionary diversity. It may seem an exercise in semantics - but essential to grasp if one is to understand 'the algae' - to say that this group is a cluster of organisms not united by a common ancestor. In phylogenetic terms the algae are polyphyletic, that is, they are derived from a number of ancestral lineages that, for the most part, are not closely related to each other. One cannot equate the algae with, for example, the angiosperms, a group that is widely acknowledged to have evolved from a single ancestor. In its present use, the term 'algae' is applied to a phylogenetically artificial cluster of unrelated or distantly related groups of organisms. Each group is internally coherent, their members being, as far as is known, related to one another, but for the algae as a whole one cannot make the same claim.

So what is it that unites the algae? Essentially, it is chlorophyll 'a' photosynthesis, the process of utilising the sun's energy to create carbohydrates from inorganic compounds. Combine this with a relatively simple level of organisation and we have what are called 'algae'. But, as will be seen below, the ability to photosynthesise has been acquired by a wide variety of unrelated organisms. For this reason the term 'algae' can be regarded only as one of convenience, and discussing the phyogeny of the algae as an entity unto itself is impossible.

This chapter defines what is meant by 'algae', describes how they are viewed phylogenetically, and attempts to place them in an overall scheme of living organisms. It also describes the way in which algae have been classified, both historically and currently, and how they will be dealt with in the present series.

What are algae?

One of the more frustrating questions often asked of newcomers to the study of algae is: What is an alga? Perhaps the frustration arises from the inability to define succinctly all that is presently encompassed by the term, without seeming overly abstruse. Algae (plural, from the Latin alga, seaweed) both historically and currently have been variously defined (Ragan, 1998). Stearn (1992) gave the literal translation as 'seaweed, a thing of little value', a definition that is entertaining in its quaintness, but not exactly informative. For the algae are both more and less than seaweeds. More, in that the term is now also applied to a large number of unicellular as well as thallose organisms

1 School of Biological Sciences and Biotechnology, Murdoch University, Murdoch, Western Australia 6150, Australia

2 Department of Biology, University of New Brunswick, Fredericton, E3B 6E1, New Brunswick, Canada.

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occupying a variety of habitats that include freshwater and terrestrial, as well as marine. Less, in that the term 'seaweed' sometimes encompasses marine angiosperms, i.e. the seagrasses that have recolonised the oceans and are more closely related to trees than they are to any of their photosynthetic co-inhabitants of the marine environment.

Other authors have attempted to define the algae by exclusion, e.g. 'cyanobacteria plus photosynthetic eukaryotes and their immediate relatives, but excluding green plants' (Ragan, 1998), or 'simple photosynthetic organisms not included among the mosses, liverworts (and other bryophytes) or the vascular plants' (Entwisle et al., 1997). Others again adopt a more circular explanation, e.g. 'those organisms studied by phycologists' (Entwisle & Huisman, 1998), phycologists being those scientists who study algae! Yet others take a historical view, essentially including those organisms traditionally regarded as algae and their close relatives (the editors of the present series). Papenfuss (1955, p. 115) defined the algae as, '...plants...[in which]... reproductive organs lack a primarily produced sterile jacket of cells', but qualified this by giving the Charophyta as an exception. Bold & Wynne (1978) amended the definition to include organisms that, when unicellular, may function directly as gametes, when multicellular producing either unicellular or multicellular gametangia; in the latter case every gametangial cell is fertile. This definition separates the algae from other green plants, but only serves to define the group partially (excluding as it does the many asexual taxa).

Although an accurate definition of the algae appears to be elusive, the reason for our seeming inability to define what we are talking about is more straightforward, for the term is applied to an artificial cluster of unrelated or distantly related groups of organisms. In fact, it is imperative that this aspect of the 'algae' be stressed if there is to be any understanding of their place in the overall scheme of life. So what do we mean when we talk of algae? In essence it is a term of convenience, one that describes a concept rather than a taxonomic group. If pushed, we would describe the algae, and please note the intentional vagueness, as 'mostly simply constructed, mostly photosynthetic, plant-like organisms and their close relatives'. As will be seen in the remainder of this chapter, this definition includes organisms with disparate phylogenetic heritages ranging from bacteria to simple 'animals'. It will also be shown how modern researchers have come to establish the all-important issues of 'relatedness'.

The protist perspective

For some time it has been recognised that the traditional 'plant or animal' separation does not apply to a vast number of organisms, including many of those included in the algae. Over the last thirty or so years there has been a resurgence of interest in the 'protists', the collective name for the large, heterogeneous group of (mainly) unicellular organisms - some plant-like, some animal-like, some with features of both kingdoms - that comprise the 'lower' eukaryotes. In many phylogenetic schemes the protists are regarded as ancestral to (or arising from the ancestors of) the higher plants, animals, and true fungi (e.g. Whittaker, 1969). Corliss (1994) included in the protists 'essentially all protozoa, eukaryotic algae and "lower fungi"', but this delineation is not universally accepted. Others include only the unicellular eukaryotes (e.g. Melkonian, 1999). The growing acceptance of the protists as a distinct kingdom and the recognition that their study necessitates dismantling traditional (but artificial) plant/animal and algal/protozoan/fungal boundaries has become known as the 'protist perspective'. The history of the resurgence of protistology was documented entertainingly by Corliss (1986).

Recognition of protists began in the late 19th and early 20th centuries and was linked to early microscopical work that, for the first time, revealed the diversity of the 'miniature' plants and animals (e.g. Kützing, 1834). Several formal kingdoms were proposed to include these micro-organisms, of which the kingdom Protista (Haeckel, 1866) was the most widely accepted. The early Protista included all microscopic organisms, including bacteria and blue-green algae, plus the fungi, slime moulds and seaweeds (Andersen, 1998). Many of these were subsequently removed as a greater understanding of their relationships evolved. The recognition of the fundamental differences between prokaryotes and eukaryotes resulted in the erection of the kingdom Monera for the former, the green algae being placed in the Plantae in light of their ancestral relationship with the higher plants (Copeland, 1938, 1947). The fungi were placed in their own kingdom, Fungi, by Whittaker (1957, 1959, 1969). As then constituted, the Protista contained the protozoa, eukaryotic algae, slime moulds and some 'lower' fungi. Acceptance of the kingdom, however, was

 

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not universal. The eminent phycologist G.F.Papenfuss, in his review of algal classification (1955), stated that '... a separate kingdom Protista ... was later found untenable and generally has been abandoned'.

The recent revival of the Protista and acceptance of protistology as a legitimate field of research was greatly enhanced by the resurgence of the concept of endosymbiosis as the means by which eukaryotic cells gained their subcellular organelles. Numerous studies (e.g. Gibbs, 1978, 1981, 1993; Cavalier-Smith, 1982, 1983; Gray, 1992; Bhattacharya & Medlin, 1995; McFadden & Gilson, 1995; Gilson & McFadden, 1997) demonstrated that subcellular organelles, including plastids, are not autogenous and that many animals (in the broad sense) had secondarily attained plastids and therefore become plants (also in the broad sense). Many taxa included in the Protista had apparently undergone this process and provided excellent models for the study of endosymbiosis. These studies did not support a single, phylogenetically coherent kingdom Protista, but did lead to increased usage of the protists as an informal aggregate as it confirmed that many organisms could no longer be readily placed in either the plant or animal kingdoms. The subsequent increased interest in the protists led to new phylogenetic insights and reinforced earlier perceptions that all lower eukaryotes could not be accommodated comfortably in a single kingdom (e.g. Whittaker, 1957). Most contemporary workers adopt a more phylogenetically defensible approach and recognise multiple kingdoms within the eukaryotic assemblage that include a number of discrete algal groups (e.g. Cavalier-Smith, 1983).

Thus the revived, single kingdom Protista saw an early demise. Ragan (1998) suggested that the protists could be considered a phylogenetically coherent group only if all their descendants are included, which would mean including all eukaryotes. In those terms, 'protist' becomes meaningless. Corliss (1994) stated that 'a single kingdom Protista as such must be laid to rest', but the term 'protist' persists as a convenient and perfectly acceptable way of describing the 'lower' eukaryotes. In the words of Andersen (1998), 'The Protista represent, at best, a grade, not a clade, and there appears to be little hope that this group will ever again be considered to represent a natural taxonomic unit, i.e. the Kingdom Protista'. Despite this, there is little doubt that protistology will continue as a legitimate field of research.

So where does this leave 'algae', another epithet of convenience used to describe a diverse but overlapping group of organisms? The emergence of protistology and its 'global' view might seem to consign traditional terms such as 'algae' and 'protozoa' to the level of historical oddities, but for the moment, at least, this is not the case. The answer essentially remains one of historical precedent and practicality. Phycologists will undoubtedly continue to talk of the algae, protistologists of protists, and zoologists of protozoa. As long as the concepts of all terms are understood, there is no particular reason to discontinue their use. Table 1 gives some examples of the varying classifications of the taxa regarded herein as algae. Corliss (1994) is essentially the 'protist' perspective, van den Hoek et al. (1995) a more traditional approach.

How many Kingdoms?

Until relatively recently, all living organisms were conveniently (if not realistically) divided between the two kingdoms proposed by Linnaeus (1753): the Animalia and Vegetabilia (the latter now generally known as Plantae, see Corliss, 1994). This enforced categorisation as plant or animal was rarely questioned by early biologists, and the algae (due to their photosynthetic nature) were placed in the Kingdom Plantae along with the seed plants, ferns, bryophytes and mosses. Some argument ensued when flagellate, unicellular taxa displaying both animal and plant characteristics were discovered (e.g. certain euglenoids and dinoflagellates), but in general an uneasy consensus prevailed. Recognition of protists in the mid- to late-19th century did little to upset the status quo.

When Chatton (1925), then Stanier and others (Stanier & van Niel, 1962; Stanier et al. 1963) recognised and promoted the fundamental differences between the prokaryotes and eukaryotes, a revolution was set in motion. While not immediately affecting the classification of the algae, increased attention to the diversity of the lower eukaryotes resulted in a more realistic appraisal of their evolutionary relationships, one consequence being a resurgence in acceptance of the Protista (see above) as apart from plants and animals (Corliss, 1984).

 

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Most recent texts have adopted the five kingdoms proposed by Whittaker (1969). This scheme includes the prokaryotes as Kingdom Monera (following Copeland, 1938, 1947), and four kingdoms of eukaryotes, the Fungi, Animalia, Plantae and Protista (alternatively known as Protoctista, see Margulis, 1990). Of the eukaryote kingdoms, only the Animalia, Plantae and 'true' Fungi remain tenable when subjected to the strict application of monophyly. Indeed, many who support the five kingdoms recognise the artificial nature of at least some of the taxa. Margulis (1990, p. xvi) stated: 'Our five-part scheme, in which the protoctists are raised to kingdom status, makes no claim to monophyly'. Following such a scheme must, therefore, acknowledge the artificial nature of some of the taxa. Despite this, the five-kingdom scheme, due to its relative simplicity, remains popular for educational and other essentially non-research uses (Corliss, 1998; Margulis & Schwartz, 1998). Some recent authors have proposed more phylogenetically acceptable classification schemes for the eukaryotes, and there has been much discussion on the relative merits of the various proposals (see Cavalier-Smith, 1981, 1986, 1989a, 1989b; Corliss, 1984, 1994). Cavalier-Smith (1983) recognised six kingdoms of eukaryotes, five of which contain protists, and his scheme was followed by Corliss (1994, see Table 1). What are traditionally termed 'algae' were distributed in three kingdoms, with the majority in the Chromista and Plantae and the euglenoids (Euglenozoa) and dinoflagellates (Dinozoa) in the Protozoa. These six kingdoms are included in the 'Empire Eukaryota' [the prokaryotes are included in either a single empire 'Bacteria' or divided into the empires 'Eubacteria' and 'Archaebacteria', see Mayr (1998) and Woese (1998) for arguments]. Even with this increased number of higher-level taxa, the schemes of Cavalier-Smith and Corliss retain some artificial groups, most notably the Protozoa. Möhn (1984) has taken the relatively extreme view of recognising three kingdoms ('Reich') of prokaryotes and 15 kingdoms of eukaryotes, with protists distributed through 11 of them and alone comprising 10 (see Table 1). His scheme has certainly reduced the incidence of polyphyly, but the large number of kingdom-level taxa has met with some resistance. Due to the incomplete data for many groups, some of these schemes are considered provisional by their authors. Nevertheless, these attempts to give some phylogenetic basis to the higher-level classification of organisms are to be applauded and will eventually lead to a more natural classification.

Classification of the Algae

Historical

Many organisms that we now regard as algae have, of course, been long recognised, although mostly not under their present names. Prior to Linnaeus's introduction of the revolutionary binomial system for naming organisms, many plants and animals were generally given a short 'phrase' name. For example, Galaxaura rugosa (Ellis & Solander) J.V.Lamour. (Huisman & Townsend, 1993) was recorded as Fucus marinus coralloides minor fungosus albidus teres segmentis in summitate planis by Sloane (1707). The term 'algae' was first used as a taxonomic category by Linnaeus (1753), as the ordo Algae in the class Cryptogamia, but included only the genera Conferva, Ulva, Fucus and Chara of the algae as presently understood. Linnaeus acknowledged that these 'genera' were for artifical convenience as he had little interest or expertise in them. He also included lichens, sponges, liverworts and some fungi. Several other taxa presently regarded as algae, such as Corallina, were later placed by Linnaeus in classes thought to lie somewhere between plants and animals (Linnaeus, 1758). Linnaeus's total of 80 species in ten genera represents about 47 modern genera (Silva, 1980).

During the next half-century the algae were generally classified following the Linnaean system, which was based on gross morphology. Other than reasonably well-known entities such as Chara, all filamentous species were placed in Conferva, all membranous species in Ulva, and all fleshy species in Fucus. Eventually some botanists realised the restrictive nature of Linnaeus's system and erected new genera. One of the more notable was Stackhouse (1795-1801, 1809, 1816), who divided Fucus into 67 genera. Stackhouse's work lay undiscovered for many years because most copies were destroyed when Napoleon's army sacked Moscow in 1812.

The first inklings of the modern groupings of algae arose with Lamouroux (1813), who recognised families based on structure and colour. Colour was, in essence, a biochemical character and remains in use to this day for delineating algae at the division level. Many of Lamouroux's

 

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'ordres' correspond, at least in part, to taxonomic groups as recognised in modern classification schemes. Thus his Fucacées is largely equivalent to the Phaeophyceae, the Floridées to the Rhodophyta, the Dictyotées to the Dictyotaceae, the Ulvacées to the Chlorophyceae, the Spongodiées to the Codiaceae and so on (Silva, 1980). Lamouroux's scheme was adopted with minor changes by C.Agardh (1817, 1824) and Harvey (1836), the latter dividing the algae into four divisions: the Chlorospermeae (green algae), Rhodospermeae (red algae), Melanospermeae (brown algae) and Diatomaceae (diatoms and desmids).

During the early part of the 19th century, many voyages of discovery contributed new taxa and diversity to the algal repository. The study of microalgae also increased in prominence as the quality of microscopes improved (Kützing, 1834; Ehrenberg, 1838). By 1842, 52 families of algae had been described (Silva, 1980). In 1843, Kützing published his Phycologia Generali... , in which 96 families were recognised, 62 of them new. Kützing's work is of major significance in the history of algal classification.

Kützing's classification has since undergone gradual revision and improvement. Of the earlier workers, Silva (1980) acknowledged major contributions from Carl W.Nägeli, Jacob G.Agardh, C.J.Friedrich Schmitz, Heinrichs L.Skuja, and Harald Kylin in the red algae; Frans R.Kjellman, Ernst H.P.Kuckuck, William A.Setchell and Nathaniel L.Gardner, and Gontran G.H.Hamel in the brown algae; Frederick F.Blackman and Arthur G.Tansley, George S.West, Johan N.F.Wille, Aleksandr A.Korshikov, Pierre Bourrelly, and Bohuslav Fott in the green algae; Aleksander A.Elenkin and Lothar Geitler in the blue-green algae; Albert Grunov, Giovanni B.De Toni, Ernst J.Lemmerman, and Konstantin S.E.Mereschkowsky in the diatoms; and Carl A.Ehrenberg, Friedrich Stein, William S.Kent, Johann A.O.Bütschli, Ernst J.Lemmermann, Adolf Pascher, Erich Lindemann, Josef Schiller, Heinrichs L.Skuja, and Pierre Bourrelly in the flagellates. Garbary & Wynne (1996), in their Prominent Phycologists of the 20th Century, also acknowledged Felix E.Fritsch, Jadwiga Woloszynska, Friedrich C.Hustedt, M.O.P.Iyengar, Mary A.Pocock, Gibert M.Smith, Mary Parke, and Gerald W.Prescott for their contributions to microalgal systematics; and Kintaro Okamura, Frederik Børgesen, Yukio Yamada, George F.Papenfuss, Aylthon B.Joly, E.Yale Dawson, and William R.Taylor for their contributions to macroalgal systematics. The modern list of Garbary & Wynne (1996) includes only deceased phycologists, and many contemporary (and living) workers also deserve recognition for their contributions.

Despite major advances in algal systematics, relationships between the various groups were rarely considered as each appeared internally coherent but externally unique. A lack of shared characteristics made phylogenetic speculation difficult, and it is only quite recently that methods have become available whereby realistic appraisals of ancestral relationships can be proposed with any confidence.

For further information regarding the historical development of algal classification and nomenclature the reader is referred to the excellent accounts by Papenfuss (1955) and Silva (1980).

Major conceptual or methodological advances

Ultrastructure

The advent of electron microscopy and its use in the examination of the ultrastructure of algal cells led to major advances in our understanding of algal phylogeny and diversity. As highlighted by Andersen (1998), before electron microscopy there were 12 algal classes; at present there are over 30. Electron microscopy has had a significant impact on the higher-level classification and phylogeny of virtually all groups of algae. Examples include: the arrangement of the flagellar root assemblages and cell division processes in the Chlorophyta, which led to the erection of many new classes and the refinement of our understanding of the evolutionary pathway that gave rise to the higher plants (van den Hoek et al., 1995); the delineation of the orders of the Rhodophyta by examination of pit-plug ultrastructure (Pueschel & Cole, 1982); recognition of several new classes of phytoplankton [the Haptophyceae Christensen ex Silva (1980), Eustigmatophyceae Hibberd & Leedale (1971), Dictyochophyceae Silva (1980), Chlorarachniophyceae Hibberd & Norris (1984), Synurophyceae Andersen (1987), Pelagophyceae Andersen et al. (1993), Phaeothamniophyceae Bailey et al. (1998), and Bolidophyceae Guillou et al. (1999)]; and the recognition that the euglenoids were not closely related to the green algae (Kivic & Walne, 1984). Of the many

 

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important aspects revealed by electron microscopy, perhaps the most significant is the increased support for the concept of the endosymbiotic origin of chloroplasts.

Serial endosymbiosis

At least twice during the evolution of the photosynthetic eukaryotes, prokaryotes have been incorporated into host eukaryote cells as organelles in a process known as serial endosymbiosis (Margulis, 1970, 1981a; Gray & Doolittle, 1982; Cavalier-Smith, 1982; Figure 1). Thus the chloroplasts and mitochondria of what we now know as phototrophic eukaryotes have had independent origins, the chloroplasts from cyanobacteria (blue-green algae) and the mitochondria from alpha-proteobacteria. Eukaryotes are, therefore, composite or chimeric organisms derived from several sources. This theory was originally proposed by Mereschkowsky (1905) but was ignored for many years. Evidence for the symbiotic origin of organelles was initially derived from biochemical and ultrastructural observations, in particular the striking similarities between the Cyanophyta and the chloroplasts of the Glaucocystophyta and the Rhodophyta. All three produce chlorophyll a but not chlorophylls b or c, and their accessory pigments include phycocyanin and allophycocyanin, contained in phycobilisomes attached to the thylakoids. Ultrastructural evidence for the endosymbiotic origin of organelles includes the multiple membranes surrounding them. In the Glaucocystophyta, Rhodophyta and Chlorophyta the chloroplasts are surrounded by a double membrane envelope and are considered the result of a primary endosymbiotic event of a cyanobacterium (Figure 1). In such cases the inner membrane is interpreted as derived from the plasmalemma of the original endosymbiotic cyanobacterium, whereas the outer membrane is thought to have originated from the ancestral host's food vacuole. In the other photosynthetic eukaryotes (the Euglenophyta, Heterokontophyta, Chlorarachniophyta, Haptophyta, Dinophyta and Cryptophyta), the chloroplasts are surrounded by a three- or four-layered membrane and are thought to be derived from the secondary endosymbiosis of a phototrophic eukaryote by a heterotrophic eukaryote. In the case of a four-layered membrane, the additional layers are interpreted as the vestigial plasmalemma of the phototrophic endosymbiont plus the food vacuole membrane of the secondary host. Therefore, the initial ingestion would have been via endocytosis. Where only three layers occur (the Dinophyta and Euglenophyta), van den Hoek et al. (1995) and others suggested that the plasmalemma layer is missing due to the feeding habits of the host, which might have punctured the plasmalemma of the prey and sucked out the cytoplasm without ingesting the membrane. Alternative hypotheses suggest that one of the membranes has been lost during evolution (Lee, 1977) or perhaps two have somehow fused to become one (Gibbs, 1970; also Saunders et al., 1997a and references therein).

Given the overwhelming evidence for the endosymbiotic origin of organelles it is, therefore, no longer possible to discuss the evolutionary history of a given eukaryotic organism as though it were a single entity, since it is also important to consider the origins of the organelles with their individual ancestries. Fortunately, plastids have a genome (Ris & Plaut, 1962) that both betrays their ancestry and enhances understanding of their phylogeny, while at the same time providing strong support for the endosymbiont theory of their origin. Given the large variety of plastids and pigments in photosynthetic organisms, it was initially postulated that multiple symbiotic events must have occurred, each incorporating a different prokaryotic organism, i.e. a polyphyletic origin to plastids. The discovery of the green prokaryote Prochloron (Lewin, 1976, 1977) appeared to provide additional evidence, as it was postulated to be similar to the ancestral chloroplast. DNA studies of chloroplast and bacterial genomes have, however, shown the prochlorophytes to be unrelated to the plastids of green plants, and it is now believed that all plastids have arisen from a single symbiotic event, i.e. a monophyletic origin (Delwiche & Palmer, 1997). The variety of pigments and plastids is considered, therefore, to be the result of evolution following an initial symbiotic event (Figure 2). The arguments for this are convincing, although the acquisition of plastids through separate endosymbiotic events involving closely related cyanobacteria cannot be discounted entirely (Stiller & Hall, 1997).

While current evidence suggests that the primary endosymbiotic event occurred only once, secondary (and even tertiary) endosymbiotic events have occurred several times. Thus the photosynthetic lineages of many algae arose through separate endosymbiotic events (Battacharya & Medlin, 1995; Medlin et al., 1997; Figures 2, 3). This scenario is supported by the presence of

 

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numerous heterotrophic taxa that are closely related to photosynthetic algae which are believed to have arisen via secondary endosymbioses.

Plastids, as mentioned earlier, are believed to be monophyletic and derived from the cyanobacteria. The plastids of the Glaucocystophyta, Rhodophyta and green plants form discrete monophyletic lineages (Medlin et al., 1997), whereas those of the Heterokontophyta, Haptophyta and Cryptophyta, Dinophyta and apicomplexans are variously related to the red algae. This indicates that the plastids of the latter groups (but not the host cells) are derived from the endosymbiotic inclusion of a red alga, or at least something closely related (Medlin et al., 1997). Recent evidence suggests that the plastids of these groups all arose from a common endosymbiosis involving a red alga (see review by Palmer, 2003). Similarly, the plastids of the Euglenophyta and Chlorarachniophyta are related to green algal plastids, whereas their host eukaryotic cells are related to divergent flagellate and amoeboid species, respectively. A review of the origin of plastids was provided by Delwich & Palmer (1997) and Palmer (2003). Figures 2 and 3 summarise plastid phylogeny and the changes that have occurred during their evolution.

Nucleotide sequence studies

The development of methodologies that allow sequencing and comparison of genetic material has provided a powerful analytical tool. In theory, these methods allow us to view the blueprints by which organisms are constructed, and to compare them for slight or major changes. As a result, algal phylogenetic studies, in fact phylogenetic studies in general, are presently in the midst of one of their most exciting phases. For the first time it is possible to propose phylogenetic trees that are based on analysis of the genotype, rather than the easily misinterpreted phenotype. The impact of these new methods can be gauged by the flood of papers appearing in many scientific journals, and the widespread acceptance of sequence studies as the method for phylogenetic speculation.

Sequence studies have been undertaken, at least in part, on all major algal groups and have revealed many unexpected associations. Many of these are, in hindsight, logical; others have prompted the search for new or previously under-appreciated phenotypic characters to buttress the molecular results. The search for the origins of plastids was also greatly enhanced by the development of molecular methods that enabled portions of genes to be sequenced and compared. By sequencing plastid and host genes separately, phylogenetic trees can be inferred for the two entities. Sequence studies have greatly enhanced higher-level phylogenies, and an example of an early phylogeny based on SSU rDNA (small subunit ribosomal DNA) is given in Figure 4 (modified from Patterson & Sogin, 1993). Most studies indicate that there was a relatively late and rapid evolutionary explosion, the resultant groups being known as the 'crown taxa' (after Knoll, 1992). They include most eukaryotic algae. Despite the impressive results obtained using these molecular methods, some caution is appropriate in the interpretation of their phylogenetic significance. Philippe & Adoutte (1998) compared trees derived from 18S rRNA genes with those from protein coding genes and found contradictory results. They suggested that inequalities in evolutionary rates could generate falsely resolved trees. One consequence of their studies is that many of the groups previously thought to lie in the middle zone (which, in the algae, includes the Euglenophyta) more probably belong to the crown taxa, and they have termed this the 'big bang' hypothesis (Figure 5). A number of high-level monophyletic groups can still be identified (Alveolates, Stramenopiles, Metazoa + Fungi + Microsporida, Chlorobionta + Rhodobionta), but their relationships to other groups are difficult to discern. An introduction to the methods used in phylogenetic studies of the algae was provided by Bhattacharya (1997).

Phylogeny of the Algae

Given that we accept a broad definition of the algae to include a cluster of taxonomic divisions that are not necessarily closely related, it would appear best to consider individual phylogenies separately. Andersen (1992) recognised at least seven distinct phylogenetic algal lineages amongst the eukaryotes, each appearing monophyletic. He described three major lineages, each with large numbers of species and substantial diversity, and four minor lineages. The former includes the red (Rhodophyta), green (Chlorophyta) and chromophyte (Heterokontophyta) algae, the latter the dinoflagellates (Dinophyta), euglenophytes (Euglenophyta), cryptophytes (Cryptophyta), and the

 

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glaucocystophytes (Glaucocystophyta). Recent research now supports the segregation of the Haptophyta and Chlorarachniophyta (Hibberd & Norris, 1984; McFadden et al., 1997). The addition of the prokaryotic Cyanophyta brings the number of distinct algal lineages to ten.

These lineages are apparently monophyletic and, in most cases, have arisen as part of the 'crown-group radiation' of eukaryotes, the highly derived collection of independent lineages that also includes those that gave rise to the animals, higher plants and fungi (Figures 4, 6). Included in the algae are two exceptions, the prokaryotic Cyanophyta and the Euglenophyta which, although eukaryotic, represent an early divergence predating the crown explosion. The position of the Euglenophyta is controversial, however, some authors placing them in the crown group (Philippe & Adoutte, 1998; Figure 5). The groups including algae are highlighted in Figure 4, illustrating their independent origins.

It must be noted that with the current high level of research into algal phylogeny utilizing nucleotide sequences, phylogenetic schemes are constantly being revised and improved. The details of what we discuss here might well be out of date by the time of publication, and if not then, they will certainly be in a very short time. The reader is strongly advised to consult recent literature.

EVOLUTIONARY LINEAGES

Prokaryotes

Division Cyanophyta, including the 'Prochlorophyta'  the photosynthetic bacteria

The Cyanophyta are also known as the Cyanobacteria, a name that more accurately reflects the division's affinities with the Kingdom Bacteria or, to be more precise, the Kingdom (or Empire, or Domain) Eubacteria (Figure 4). The Cyanophyta includes prokaryotic organisms and is, therefore, considered the most ancestral of the divisions included here as algae. The division is related only remotely to the rest of the algae but is regarded as the source of at least some ancestral organisms that have been incorporated as eukaryotic plastids through endosymbiosis. In a phylogenetic analysis of SSU rRNA sequences from the Cyanophyta, Turner (1997) confirmed earlier studies showing that the plastids of photosynthetic eukaryotes constitute a monophyletic branch/clade within the cyanobacterial line of descent (Figure 7). The plastids of the Rhodophyta are very similar in form and pigment composition to cells of the Cyanophyta, and the plastids of the Glaucocystophyta are so cyanobacteria-like that, in the past, they were referred to as 'cyanelles' and considered to be endosymbiotic cyanophytes. The phylogenetic affinities of plastids are shown in Figure 3.

The Prochlorophyta was proposed by Lewin (1975, 1976, 1977) following the discovery of chlorophylls a and b in Prochloron, a photosynthetic prokaryote living in a symbiotic relationship with didemnid ascidians. This discovery was considered highly significant as Prochloron was promoted as a progenitor of the green plastid. Earlier hypotheses had suggested a scenario in which multiple primary endosymbiotic events occurred, with the 'red algae' the result of a symbiosis with a cyanophyte and the 'green algae' the result of a symbiosis with an unknown (at the time) prokaryote producing chlorophyll b (Sagan, 1967; Raven, 1970). Thus Prochloron was thought to be the missing link in this process. Since its discovery, two other prokaryotes with chlorophylls a and b have been recognised, the filamentous Prochlorothrix and the unicellular Prochlorococcus. Understandably, these organisms have been the subject of intensive scrutiny, particularly their nucleotide and derived amino acid sequences, in an attempt to ascertain their phylogenetic relationships and possible connection with the green chloroplasts. Most work, however, has shown that none of the prochlorophytes is specifically related to green plastids (Turner et al., 1989; Urbach et al., 1992), although these results have been disputed (Lockhart et al., 1993). It also appears that only a single primary endosymbiotic event occurred in the evolution of photosynthetic eukarotes. However, the possibility that a photosynthetic bacterium related to green plastids might be discovered cannot be ruled out entirely (Turner, 1997). In addition, the prochlorophyte group has been found to be polyphyletic and, therefore, artificial (Turner et al., 1989; Palenik & Haselkorn, 1992, Urbach et al., 1992; Palenik & Swift, 1996). The

 

Huisman & Saunders : Phylogeny and Classification: 9

prochlorophytes should not be regarded as an independent class and are best viewed as aberrant cyanobacteria.

An analysis of the intradivisional relationships of the Cyanophyta, based on SSU rRNA sequence analysis, was given in Turner (1997) and is reproduced as Figure 7.

Eukaryotes

Division Rhodophyta  the Red Algae

The Rhodophyta were long considered to be an early offshoot of the Eukaryota, mostly due to the division's 'similarities' to the prokaryotic Cyanophyta (similar chloroplast structure and accessory pigments) and lack of flagellated stages, the latter traditionally regarded as an ancestral condition (rather than a secondary loss). More recently, the recognition of the flagellated Glaucocystophyta, with chloroplasts similar to those of the Rhodophyta, has suggested a possible ancestor to the latter group, which would have arisen after the evolution of flagella and secondarily lost motility. The genus Glaucosphaera was regarded as an evolutionary 'link' between the two groups (Cavalier-Smith, 1982, 1987). Unfortunately, a direct connection between the Glaucocystophyta and the Rhodophyta is not supported by sequence studies (Bhattacharya & Schmidt, 1997), and Glaucosphaera is now regarded as a red alga. Nevertheless, recent molecular studies do confirm the Rhodophyte lineage as part of the 'crown radiation' (Figures 5, 6), supporting the contention that motility has been secondarily lost. Initial results suggested that the group emerged before the common ancestor of the the other crown taxa (Patterson & Sogin, 1993; Stiller & Hall, 1998), but recent evidence places the Rhodophyta as a sister group to the green plants (Ragan & Gutell, 1995; Philippe & Adoutte, 1998). This scenario agrees with studies that indicate a monophyletic origin to plastids and that only a single endosymbiotic event occurred in the primary acquisition of chloroplasts, rather than the multiple events previously postulated. One consequence is that the plastids of the Chlorophyta producing chlorophyll a and b are now regarded as having evolved from plastids similar to those of the Rhodophyta producing only chlorophyll a. Thus in recent classification schemes the Rhodophyta are included with the Chlorophyta as part of the Kingdom Plantae (Corliss, 1994; Saunders & Hommersand, 2004).

In the Rhodophyta, some schemes (e.g van den Hoek et al.,1995) recognise two classes: the Bangiophyceae and Florideophyceae (traditional treatments generally recognise a single class with two subclasses), with others also including the Cyanidiophyceae. The Bangiophyceae is apparently polyphyletic and encompasses three or more individual lineages that are yet to be resolved satisfactorily (Ragan et al., 1994), whereas monophyly of the Florideophyceae is well supported (Ragan et al., 1994; Saunders & Bailey, 1997). A major revision of the higher-level classification of the Rhodophyta was proposed by Saunders & Hommersand (2004). They placed the red algae as a subkingdom in the Plantae and recognized two phyla: the Cyanidiophyta with one class, the Cyanidiophyceae; and the Rhodophyta with four classes, the Rhodellophyceae, Compsopogonophyceae, Bangiophyceae, and Florideophyceae. Saunders & Kraft (1997) reviewed the relationships of the orders constituting the Florideophyceae and presented a phylogenetic tree based on SSU rDNA sequences. Their scheme recognises four lineages within the class (Figure 8). The intradivisional relationships in the Rhodophyta have been reviewed and/or modified by Fredericq & Hommersand (1989), Freshwater et al. (1994), Ragan et al. (1994), Saunders & Kraft (1994, 1996, 1997), Fredericq & Norris (1995), Oliviera et al. (1995), Ragan & Gutell (1995), Fredericq et al. (1996), Saunders & Bailey (1997), Saunders et al. (1999), Huisman et al. (2003).

Division Glaucocystophyta

The Glaucocystophyta includes some nine genera and thirteen species and displays a variety of morphologies, including flagellate, coccoid and palmelloid taxa. Their plastids are regarded as primitive and similar to cyanobacteria, as they contain only chlorophyll a and phycobilin pigments, phycobilisomes, carboxysomes and concentric (unstacked) thylakoids. For many years the plastids of the Glaucocystophyta were thought to be cyanobacterial endosymbionts and were termed 'cyanelles', but recent studies have demonstrated a closer relationship of cyanelles to extant plastids than to cyanobacteria. Similarities between glaucocystophyte cyanelles and the plastids of the Rhodophyta led to suggestions that the two were sister taxa, but this is not supported by SSU rDNA data. It would appear that the features thought to indicate a common

 

Huisman & Saunders : Phylogeny and Classification: 10

ancestry to these taxa producing chlorophyll a are ancestral and found in the cyanobacterium that gave rise to plastids. The host cells of the Glaucocystophyta are thought to be a sister group to the Cryptophyta (Bhattacharya & Schmidt, 1997).

Divisions Chlorophyta and Streptophyta (in part)  the Green Algae

Sequence studies of the major lineages of green plants (Friedl, 1997) suggest that two well-resolved, monophyletic clades exist: one containing the majority of the green algae and representing the Chlorophyta;, the other including the Charophyceae (as well as the Zygnemophyceae and Klebsormidiophyceae sensu van den Hoek et al., 1995, plus the Chaetosphaeridiophyceae, Coleochaetophyceae, and Chlorokybophyceae sensu Sluiman & Guihal, 1999) and the embryophytes (the 'higher' plants; Figure 9). This second clade represents the Streptophyta sensu Bremer (1985). The evolutionary relationships of the Chlorophyta and Streptophyta are shown in Figures 10 and 11, emphasizing the streptophytes (Figure 10) or the chlorophytes (Figure 11). These sequence studies are supported by ultrastructural observations, notably differences in the arrangement of flagellar roots in the two groups; those of the Chlorophyta are in a cruciate arrangement, whereas those of the Streptophyta are unilateral and are associated with a multi-layered structure. Given this fundamental distinction, it is no longer tenable to follow the scheme of van den Hoek et al. (1995) and others in which the Charophyceae and some other 'algal' classes are included in the Chlorophyta.

The evolution of the 'higher' plants from a green algal ancestor has been a popular hypothesis for many years. Pickett-Heaps (1967, 1969, 1972a, b, 1975) and Pickett-Heaps & Marchant (1972) described the ultrastructural details of cytokinesis in the green algae and recognised two groups: those in which microtubules are oriented in the plane of cell division (known as a 'phycoplast') and where the interzonal spindle apparatus collapses after mitosis; and those in which the microtubules are oriented perpendicularly to the plane of cell division (a 'phragmoplast') and the interzonal spindle persists. The former condition is found in many green algae, whereas the latter occurs in the Charales (Charophyceae), Conjugales (Zygnemophyceae), Coleochaetales (Coleochaetophyceae), Klebsormidiales (Klebsormidiophyceae) and the 'higher' plants. Thus a phylogeny was proposed in which two evolutionary lineages occur in the green algae, one of which gave rise to the higher plants. The essential elements of this hypothesis remain widely accepted and the resultant phylogeny is generally supported by sequence studies. It also appears that parallel evolution of these features has occurred in some Chlorophyta (Graham, 1993), as phragmoplast-like cytokinesis occurs in the Trentepohliales (Chapman & Henk, 1986) and persistent spindles are found in the Ulvophyceae (Sluiman, 1991), groups that, on molecular grounds, are strongly allied to the green algae.

The question of which of the extant algal lineages of the Streptophyta is sister taxon to the higher plants remains unresolved (Huss & Kranz, 1997; Sluiman & Guihal, 1999). Bhattacharya et al. (1998) and Karol et al. (2001) undertook phylogenetic analyses and proposed the 'prasinophyte' Mesostigma viride Lauterborn as the earliest divergence within the Streptophyta. If so, the ancestor of the land plant lineage is likely to be a scaly, biflagellate, unicellular green alga. Of the multicellular taxa, Sluiman et al. (1999) suggested that the filamentous Hormidiella may be the closest known algal relative of the embryophyte land plants.

Included in the green algae are taxa that are amazingly diverse at the morphological, ultrastructural and genetic levels. The number and delineation of classes of green algae are presently in a state of flux. Based on SSU rRNA sequences, Friedl (1997) recognised at least four classes within the Chlorophyta sensu stricto (i.e. excluding the Streptophyta): the Prasinophyceae (a paraphyletic group according to Nakayama et al., 1998), Ulvophyceae, Chlorophyceae, and Trebouxiophyceae. This differs from the eight classes of van den Hoek et al. (1995) that are based essentially on ultrastructural evidence and which did not include the Trebouxiophyceae. Sluiman & Guihal (1999) recognised a further class, the Oedogoniophyceae, again based on sequence studies. Clearly the picture is far from complete, and future modifications are inevitable. Gibbs (1998) suggested that, until more data supporting the sequence-generated revisions become available, we should not discount ultrastructural characteristics. The classification scheme adopted here (see below) is based on that of van den Hoek et al. (1995) with modifications resulting from recent sequence studies (e.g. Zechman et al., 1990; Friedl, 1997; Sluiman & Guihal, 1999). We have maintained the classes of van den Hoek et al. (1995) unless their rejection is clearly indicated by later studies.

 

Huisman & Saunders : Phylogeny and Classification: 11

Most classification schemes include the Chlorophyta as part of the Kingdom Plantae, with the higher plants forming a subkingdom variously known as ViridiPlantae (Cavalier-Smith, 1993; Corliss, 1994) or Chlorobionta (Bremer, 1985).

Division Heterokontophyta  the Golden Algae

The Heterokonta is an assemblage of diverse organisms ranging from unicellular diatoms to large kelps as well as various heterotrophic flagellates and saprophytic organisms such as the oomycetes, the last traditionally grouped with the fungi (Leipe et al., 1994). The photosynthetic members of the Heterokonta (i.e. those traditionally regarded as 'algae') form a monophyletic lineage within the group (Guillou et al., 1999), here termed the Heterokontophyta as by van den Hoek et al. (1995). The larger group was informally named the 'Stramenopiles' by Patterson (1989), its defining features including the possession (in flagellate cells) of an anterior flagellum bearing tripartite hairs (also known as mastigonemes) composed of a basal section, a long hollow shaft, and terminal fine hairs. This form of flagellum is known as a pleuronematic flagellum. The posterior flagellum, when present, lacks these structures. In most members of the group, pleuronematic flagella occur in the vegetative phase but in some, such as the diatoms and brown algae, they are present only in reproductive cells. The host cells of the Heterokonta form part of the 'crown group radiation' of eukaryotes whose immediate relatives are not obvious, although many recent studies have indicated a relationship between the group and the alveolates (Medlin et al., 1997; Leander & Keeling, 2004). The chloroplast of the photosynthetic heterokontophytes is thought to be derived from the ingestion and subjugation of a glaucophyte-like alga. Relationships within the Heterokontophyta are discussed by Saunders et al. (1995, 1997b), Medlin et al. (1996b, 1996c, 1997), Guillou et al. (1999), Draisma et al. (2001), and Kooistra et al. (2003), and are shown in Figure 12. On the basis of comparative morphological and ultrastructural studies, the Haptophyta were also once considered closely related to the Heterokontophyta (e.g. Cavalier-Smith, 1989; Corliss, 1994), but this relationship is not supported by recent molecular studies (Leipe et al., 1994; Medlin et al., 1997).

Division Euglenophyta  the Green Photosynthetic Protozoa

The euglenoids include phagotrophic, green autotrophic, and mixotrophic species that are closely related to one another but not to any other group of algae. Their phylogenetic affinities remained enigmatic for many years. It was commonly suggested that their nearest relatives were among the zooflagellates, in particular the Kinetoplastida (e.g. Dodge, 1973). These affinities were supported by ultrastructural evidence (summarised in Kivic & Walne, 1984), and the euglenoids were the first of the photosynthetic algae to be clearly aligned with non-photosynthetic relatives. Recognition of the heterotrophic ancestry of the euglenoids also provided strong support for acceptance of the theory of secondary endosymbiosis and prompted the reappraisal of many other algal groups. Current molecular evidence emphatically aligns the euglenoid host cells with non-photosynthetic flagellates, their plastids being thought to be derived from a chlorophyte ancestor. Thus the euglenoids most likely arose through the incorporation of a chlorophyte by a heterotrophic euglenoid. The Euglenophyta is often described as the only group of eukaryotic algae where the host cell arose well before the 'crown radiation' of eukaryotes, but this interpretation has been challenged by the results of Phillipe & Adoutte (1998; Figure 5; see earlier discussion). Intradivisional relataionships of the euglenoids have been examined by Nudelman et al. (2003).

Division Chlorarachniophyta

The Chlorarachniophyta is a group of four genera characterised by amoeboid cells with pseudopodia and grass-green plastidial endosymbionts with pyrenoids. The endosymbiont retains the plastid, plasma membrane, some cytoplasm, and a vestigial nucleus known as a nucleomorph (Figure 1). McFadden et al. (1997) discussed the relationships of the Chlorarachniophyta, concluding that the host is closely related to filose amoebae and sarcomonads, whereas the affinities of the endosymbiont are with the green algae.

Division Dinophyta  the Dinoflagellates

 

Huisman & Saunders : Phylogeny and Classification: 12

Dinoflagellates are distinctive organisms characterised by the arrangement of their flagella and the presence, in most, of an unusual nucleus in which the chromosomes are permanently condensed and lack histone proteins (dinokaryotic nucleus) Dodge (1965, 1966) postulated that this condition was intermediate, in evolutionary terms, between the prokaryotic and eukaryotic conditions and adopted the term 'mesokaryote', suggesting also that the dinoflagellates were one of the first groups to diverge from the early eukaryotic line. Although enticing, this hypothesis has not been supported by molecular investigations, most of which suggest that dinoflagellates are only remotely related to the prokaryotes and arose among the 'crown group radiation' of eukaryotes (Liu et al., 1984; Herzog & Maroteaux, 1986). The closest relatives of the dinoflagellates are the heterotrophic apicomplexans and ciliates (Lenaers et al., 1989; Gajadhar et al., 1991; Inagaki et al., 1997; Leander & Keeling, 2004), the three groups included in a monophyletic clade known as the 'Alveolates' (Cavalier-Smith, 1993). This larger grouping is characterised by cell surfaces underlain by a series of abutting sacs or alveoli.

The dinoflagellates, like the euglenoids, haptophytes, cryptophytes and heterokontophytes, represent heterotrophic organisms that have become secondarily photosynthetic via the incorporation of eukaryotic endosymbionts. Approximately 50 percent of dinoflagellates are photoautotrophic, with many characterised by a 'chromophyte'-like plastid (typical dinoflagellate plastid) (Saunders et al., 1997a, and references therein). However, dinoflagellate evolution is a web of complex plastid gains and losses (Saldarriaga et al., 2001), with many extant photosynthetic dinoflagellates having apparently acquired plastids by independent secondary and even tertiary symbiotic events, involving the incorporation of glaucophytes, heterokontophytes, cryptophytes, and chlorophytes (Schnepf & Elbraechter, 1988; Lucas & Vesk, 1990; Watanabe et al., 1990; Schnepf, 1992).

The intradivisonal relationships of the Dinophyta have been examined and reviewed by Saunders et al. (1997a), whose phylogenetic scheme is reproduced as Figure 13.

Division Haptophyta

The Haptophyta includes species with biflagellate unicells characterised by (among other features) the possession of a unique appendage, the haptonema, thought to be involved in phagotrophy or attachment. The division, once grouped with the cluster of taxa that now forms the Heterokontophyta (e.g. Bold & Wynne, 1973), is now regarded as a distinct taxonomic group, not closely related to any other eukaryotic algal lineage (Medlin et al., 1997; Daugbjerg & Andersen, 1997; Fujiwara et al., 2001). As in most algal groups, the host cells evolved as part of the 'crown-group' radiation. Medlin et al. (1997) thought that the endosymbiont of the haptophytes was derived from a pre-red algal ancestor and calculated molecular clock dates. They postulated that the host-cell of the Haptophyta appears to be more ancient than its plastids (around 850 million years before present for the host cell, 293 million years for the plastid). They suggested that the endosymbiotic event occurred late in the group's evolutionary history and that the early haptophytes were heterotrophic. Relationships within the Haptophyta were discussed by Medlin et al. (1996a, 1997), Edvardsen et al. (2000), Fujiwara et al. (2001), and Lenning et al. (2003).

Division Cryptophyta

Cryptophytes are small, unicellular biflagellates with flattened, asymmetrical cells. The group includes photoautotrophic and heterotrophic taxa, the latter either lacking a plastid or containing a plastid devoid of pigments (a leucoplast). The plastidial taxa represent a symbiosis between a eukaryotic host cell and what was a photosynthetic eukaryotic endosymbiont but is now reduced to a plastid, i.e. a secondary endosymbiosis (Figure 1; McFadden, 1990, 1993; McFadden et al., 1994). The plastid is unusual in that the membrane layers surrounding it diverge, creating what is known as a periplastidial space that retains some of the eukaryotic components of the original endosymbiont, including a reduced nucleus (known as the nucleomorph) and cytoplasm. Ribosomal RNA genes have been sequenced for both the nucleomorph and the host-cell nucleus, suggesting that the plastid is closely related to the red algae (Maier et al., 1991; Leitsch et al., 1999), whereas the host is related to the phagotrophic flagellate Goniomonas (McFadden et al., 1994). Both McFadden et al. (1994) and Marin et al. (1998) suggested that Goniomonas represents an extant relative of the precursor host component, one that diverged from the cryptomonad lineage before the endosymbiotic event leading to photoautotrophic species. The genus is now

 

Huisman & Saunders : Phylogeny and Classification: 13

included in the Cryptophyta (Marin et al., 1998). The alternative view was presented by Cavalier-Smith et al. (1996) who considered that Goniomonas had lost its plastid secondarily and that the common ancestor of the group was photosynthetic. In either case, cryptophytes are unique in that there are extant organisms closely related to both components of the symbiosis (McFadden et al., 1994). Corliss (1994) included the Cryptophyta as part of the Kingdom Chromista (which also includes the Heterokontophyta as treated here), but the results of McFadden et al. (1994) and Cavalier-Smith et al. (1996) suggest that it is an independent lineage. A phylogeny based on 18S rDNA sequences analyses was presented by Deane et al. (2002), which indicated that the plastid containing genera formed a monophyletic clade.

Nomenclature, Classification and the Algae of Australia

Why Algae?

Given the seemingly distant relationships between many of the divisions and classes included in the Algae of Australia, it is reasonable to ask why they should be combined under the broad title 'algae'. It is largely because both historical and modern literature abound with algal Floras, and most users will have some concept of the algae, though not necessarily with a strict definition in mind. Apart from these introductory chapters the higher-level classification of the included groups will not be discussed. The decision to name the series Algae of Australia was thus strictly utilitarian and is not meant to confer any formal taxonomic significance on the term 'algae'.

Nomenclature

The preceding sections have illustrated the difficulty (and often futility) in categorising eukaryotes into either 'animals' or 'plants', and it is clear that a more holistic approach to the classification of living organisms is required. Perhaps the most significant hurdle in reaching this unified concept of life is not biological or conceptual, but nomenclatural and 'legal'. Historically the naming of plants and animals has been governed by different sets of rules, the International Code of Botanical Nomenclature (ICBN) for plants and the International Code of Zoological Nomenclature (ICZN) for animals (an accepted nomenclatural code for protists does not exist). Naming of bacteria is governed by the International Code of Nomenclature of Bacteria (ICNB). No guidelines exist as to which code is appropriate for an individual taxon, the decision being essentially the responsibilty of the describing author. While the principles of both codes are similar, they differ in many respects. Generally, this has not caused problems, but in certain cases where taxa were claimed (reasonably, but for different reasons) by both botanists and zoologists, parallel systems of nomenclature were developed (e.g. the dinoflagellates). The incidence of this dual proprietorship, with its substantial nomenclatural baggage, is likely to increase as ultrastructural and molecular studies continue to demonstrate the close relationships of many autotrophic algae with heterotrophic protozoa, taxa referred to as 'ambiregnal' by Patterson (1986). This unfortunate situation is anathema to the tenets of both codes, whose aims include a high degree of stability, universality of usage, and the uniqueness of each taxonomic name (Corliss, 1993). With the renewed recognition of the protists, many members of which are indeed 'ambiregnal', it is clear that this confusion must be resolved. Patterson (1986), Patterson & Larsen (1992), Corliss (1993) and others have addressed aspects of this problem, but as yet no solution amenable to all sides has appeared. The reconciliation of the codes has been attempted by some and a draft 'BioCode' has been proposed (Greuter et al., 1996) but it is unlikely to be accepted (at least formally) for some time.

To add further confusion, some higher-level taxa have been given typified names (i.e. able to be typified by reference to a genus) and also descriptive names (adopted from common names or descriptive terms). These same higher-level taxa can be treated as either phyla or divisions, again depending on the plant/animal bias. All are legal and the use of one over another is often subject to the bias of the user. If we take the example of the dinoflagellates, the group has been variously known as division Dinophyta (descriptive, botanical bias, e.g. van den Hoek et al., 1995), phylum Dinozoa (descriptive, zoological bias, e.g. Corliss, 1994), division Pyrrophyta (descriptive, botanical bias) and division Pyrrophycophyta (descriptive, an especially phycological bias

 

Huisman & Saunders : Phylogeny and Classification: 14

introduced by Papenfuss, 1955). An example of a typified name is the class Fucophyceae (brown algae based on the genus Fucus), which is more commonly known by the descriptive name Phaeophyceae. Table 2 lists the names for some more important groups of algae for which alternatives designations exist.

The situation described above is of particular significance to the Algae of Australia series. The nomenclature of the 'algae' is governed by the ICBN, but, as stressed throughout this chapter, 'algae' can mean different things to different people. Many of the 'algae' to be dealt with in this series are classed as 'protozoa' by zoologists, and the nomenclature of the 'protozoa' is governed by the ICZN. The unfortunate result is that some taxa included in the present series have been named following both the ICBN and the ICZN. Moreover, it is only due to an historical quirk that the Cyanophyta is treated under the ICBN when, biologically speaking, it would be more appropriately dealt with under the International Code of Nomenclature of Bacteria.

Until a more satisfactory system is adopted, any compromise solution will not please all. The editors have chosen to include in this series taxa traditionally regarded as algae, and the algae are traditionally the domain of the botanists and governed by the ICBN. Thus most taxa will be treated under their botanical names. Where parallel nomenclatures exist at lower levels, alternative names will also be given (as was recommended by Patterson & Larsen, 1992). This approach has been already adopted by some authors of protistan taxa. For example, Hill (1991), when describing a family of heterotrophic cryptomonads, coined both the Goniomonadaceae and the Goniomonadidae (ICBN and ICZN, respectively).

Classification

The classification scheme adopted for the present series is taken from van den Hoek et al. (1995), with minor modifications resulting from consultation with contributing authors and the incorporation of recent evidence. Differences from the scheme of van den Hoek et al. are explained in footnotes. In the seemingly ever-changing world of algal classification, and the present molecular-based revolution, absolute consensus is virtually impossible. Thus the scheme adopted here may well undergo revision as taxonomic volumes appear. Nevertheless, the following taxa will be treated in the series.

Prokaryotes

Division Cyanophyta

Class Cyanophyceae, including 'Prochlorophyceae''4

Eukaryotes

Division Glaucocystophyta

Class Glaucocystophyceae

Division Cyanidiophyta

Class Cyanidiophyceae5

Division Rhodophyta6

ClassRhodellophyceae

Class Compsopogonophyceae

Class Bangiophyceae

Class Florideophyceae

Division Heterokontophyta

Class Bolidophyceae8

4 Treated as a separate class by van den Hoek et al. (1995). Recent studies have shown the Prochlorophyceae to be an artificial group of aberrant cyanophytes whose members have evolved chlorophyll b independently. They are, therefore, returned to the Cyanophyceae.

5 See Karsten et al. (1999) for a discussion of this class.

6 Arranged following Saunders & Hommersand (2004).

7 See Karsten et al. (1999) for a discussion of this class.

 

Huisman & Saunders : Phylogeny and Classification: 15

Class Chrysophyceae9

Class Phaeothamniophyceae10

Class Pelagophyceae11

Class Synurophyceae

Class Xanthophyceae

Class Eustigmatophyceae

Class Raphidophyceae

Class Dictyochophyceae12

Class Phaeophyceae

Class Bacillariophyceae

Division Haptophyta

Class Prymnesiophyceae

Class Pavlovophyceae

Division Cryptophyta

Class Cryptophyceae

Division Dinophyta

Class Dinophyceae

Division Euglenophyta

Class Euglenophyceae

Division Chlorarachniophyta

Class Chlorarachniophyceae

Division Chlorophyta13

Class Prasinophyceae14

Class Chlorophyceae

Class Ulvophyceae

Class Trentepohliophyceae16

Class Cladophorophyceae17

Class Bryopsidophyceae

Class Dasycladophyceae

Class Oedogoniophyceae18

Class Trebouxiophyceae19

Division Streptophyta (in part)20, 21

8 Erected by Guillou et al. (1999).

9 Includes the Parmophyceae of van den Hoek et al. (1995), following Andersen (pers. comm.).

10 Erected by Bailey et al. (1998).

11 Includes the Sarcinochrysidophyceae of van den Hoek et al. (1995), which clearly falls within the Pelagophyceae.

12 Includes the Pedinellophyceae.

13 Friedl (1997) recognised at least four classes in the Chlorophyta: the Prasinophyceae, Ulvophyceae, Chlorophyceae and Trebouxiophyceae. Van den Hoek et al. (1995) also included the Pleurastrophyceae, an apparently polyphyletic group whose members have been distributed by Friedl (1997) among the Trebouxiophyceae, Chlorophyceae and Prasinophyceae.

14 Apparently a polyphyletic group (Nakayama et al., 1998).

16 Friedl (1997) and Lopez-Bautista & Chapman (1999) suggest that the Trentepohliophcyeae should be included in the Ulvophyceae, but it is maintained here.

17 Aligns with the Ulvophyceae according to Friedl (1997).

18 Following Sluiman & Guihal (1999).

19 Following Friedl (1997).

 

Huisman & Saunders : Phylogeny and Classification: 16

Class Zygnemophyceae

Class Chlorokybophyceae22

Class Coleochaetophyceae23

Class Klebsormidiophyceae

Class Charophyceae

Class Chaetosphaeridiophyceae24

Acknowledgments

We thank Dr Tim Entwisle (Royal Botanic Gardens, Sydney) who read the manuscript critically. JMH acknowledges financial support from the Australian Research Council and the Australian Biological Resources Study.

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Agardh, C.A. (1824), Systema Algarum. Berling, Lund.

Andersen, R.A. (1987), Synurophyceae classis nov., a new class of algae, Amer. J. Bot. 74: 337-353.

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20 These classes of algae form a sister taxon to the higher plants (Friedl, 1997; Sluiman & Guihal, 1999) and cannot, therefore, be included in the Chlorophyta as was done by van den Hoek et al. (1995).

21 The Streptophyta is included here at the level of division and, in addition to the charophytes, encompasses the embryophytes (sensu Bremer, 1985). Although at the same taxonomic rank, it does not equate to the division Magnoliophyta as used in the Flora of Australia, which would be equivalent to the class Spermatopsida in Bremer's scheme (1985, table 2).

22 Following Sluiman & Guihal (1999).

23 Following Sluiman & Guihal (1999).

24 Following Sluiman & Guihal (1999).

 

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Huisman & Saunders : Phylogeny and Classification: 25

Table 1. Classification schemes for the algae. Only those groups to be treated in the present series are included.

 

Papenfuss (1955)

Möhn (1984)

Corliss (1994) - eukaryotes only

van den Hoek et al. (1995)

Algae of Australia

Superkingdom Neobacteria

Kingdom Eubacteria

Kingdom Eubacteria

Phylum Schizophyta

Kingdom CYANOBIONTA

Division Cyanophyta

Division Cyanophyta

Class Schizophyceae

Phylum Cyanophyta

Class Cyanophyceae

Class Cyanophyceae

Phylum Prochlorophyta

Class Prochlorophyceae

Empire (?) Eukaryonta

Empire EUKARYOTA

Kingdom EUKARYOTA

Kingdom EUKARYOTA

Kingdom PROTOZOA

Phylum Euglenophycophyta

Kingdom Eugleno-phytobionta

Phylum Euglenozoa

Division Euglenophyta

Division Euglenophyta

Class Euglenophyceae

Class Euglenophyceae

Class Euglenoidea

Class Euglenophyceae

Class Euglenophyceae

Kingdom DINOPHYTOBIONTA

Phylum Pyrrophycophyta

Division Dinophyta

Phylum Dinozoa

Division Dinophyta

Division Dinophyta

Class Dinophyceae

Class Dinophyceae

Class Dinoflagellatea

Class Dinophyceae

Class Dinophyceae

Class Desmophyceae

Class Protalveolatea

Class Ebriaceae

Kingdom Chromophytobionta

Kingdom CHROMISTA

Division Heterokontophyta

Division Heterokontophyta

Phylum Dictyochae

Class Dictyochophyceae

Class Dictyochophyceae

Class Silicoflagellatea

Phylum Pedinellaphyta

Class Pedinellea

Class Pedinellophyceae

Phylum Phaeophycophyta

Phylum Phaeophyta

Phylum Phaeophyta

Class Phaeophyceae

Class Phaeophyceae

Class Phaeophyceae

Class Phaeophyceae

Class Phaeophyceae

Class Laminariophyceae

Class Fucophyceae

Phylum Chrysophycophyta

Phylum Chrysophyta

Class Chrysophyceae

Class Chrysophyceae

Class Chrysophyceae

Class Chrysophyceae

Class Synurophyceae

Class Synurophyceae

Class Synurophyceae

Class Silicoflagellataceae

Class Sarcinochrysidophyceae

Class Pelagophyceae

Phylum Eustigmatophyta

Class Eustigmatophyceae

Class Eustigmatophyceae

Class Eustigmatophyceae

                   

 

Huisman & Saunders : Phylogeny and Classification: 26

Class Xanthophyceae

Phylum Xanthophyta

Class Xanthophyceae

Class Xanthophyceae

Class Xanthophyceae

Class Bacillariophyceae

Phylum Bacillariophyta

Phylum Diatomae

Class Bacillariophyceae

Class Bacillariophyceae

Class Centrophyceae

Class Coscinodiscophyceae

Class Pennatophyceae

Class Fragilariophyceae

Of uncertain position

Class Bacillariophyceae

Class Chloromonadophyceae

Kingdom Chloromonad-ophytobionta

Phylum Raphidophyta

Class Raphidophyceae

Class Raphidophyceae

Class Raphidomonadea

Class Bolidophyceae

Class Cryptophyceae

Kingdom Cryptophytobionta

Phylum Cryptomonada

Division Cryptophyta

Division Cryptophyta

Class Goniomonadea

Class Cryptophyceae

Class Cryptophyceae

Class Cryptomonadea

Phylum Haptophyta

Phylum Haptomonada

Division Haptophyta

Division Haptophyta

Class Isochrysidaceae

Class Pavlovea

Class Haptophyceae

Class Haptophyceae

Class Prymnesiaceae

Class Patelliferea

Phylum Chlorarachniophyta

Division Chlorarachniophyta

Division Chlorarachniophyta

Class Chlorarachniophyceae

Class Chlorarachniophyceae

Class Chlorarachniophyceae

Kingdom CHLOROBIONTA

Kingdom PLANTAE

Phylum Chlorophycophyta

Phylum Chlorophyta

Phylum Chlorophyta

Division Chlorophyta

Division Chlorophyta

Class Chlorophyceae

Class Chlorophyceae

Class Chlorophyceae

Class Chlorophyceae

Class Chlorophyceae

Class Trentepohliophyceae

Class Trentepohliophyceae

Phylum Prasinophyta

Phylum Prasinophyta

Class Prasinophyceae

Class Prasinophyceae

Class Prasinophyceae

Class Prasinophyceae

Cllass Loxophyceae

Class Pedinophyceae

Class Pocillophyceae

Phylum Ulvaphyta

Phylum Ulvophyta

Class Ulvaphyceae

Class Ulvophyceae

Class Ulvophyceae

Class Ulvophyceae

Class Cladophorophyceae

Class Cladophorophyceae

Class Bryopsidophyceae

Class Bryopsidophyceae

Class Dasycladophyceae

Class Oedogoniophyceae

Class Trebouxiophyceae

                   

 

Huisman & Saunders : Phylogeny and Classification: 27

Phylum Charophycophyta

Phylum Charophyta

Phylum Charophyta

Division Streptophyta

Class Charophyceae

Class Charophyceae

Class Charophyceae

Class Charophyceae

Class Charophyceae

Class Klebsormidiophyceae

Class Klebsormidiophyceae

Class Conjugatophyceae

Class Zygnematophyceae

Class Zygnematophyceae

Class Chlorokybophyceae

Class Coleochaetophyceae

Class Chaetosphaeridiophyceae

Phylum Glaucophyta

Division Glaucophyta

Division Glaucocystophyta

Class Glaucophyceae

Class Glaucophyceae

Class Glaucocystophyceae

Kingdom Erythrobionta

Phylum Rhodophycophyta

Phylum Rhodophyta

Phylum Rhodophyta

Division Rhodophyta

Division Rhodophyta

Class Rhodophyceae

Class Rhodophyceae

Class Bangiophyceae

Class Bangiophyceae

Class Bangiophyceae

Class Florideophyceae

Class Florideophyceae

Class Florideophyceae

Kingdom Rhodocyano-bionta

Class Cyanidiophyceae

               

 

Huisman & Saunders : Phylogeny and Classification: 28

Table 2. Botanical, zoological and informal names for some algal groups.

Botanical

Zoological

Informal

Class Bacillariophyceae

Division Bacillariophyta

Phylum Diatomae

diatoms

Class Charophyceae

Division Charophyta

charophytes, stoneworts, brittleworts

Division Chlorarachniophyta

Phylum Chlorarachnida

chlorarachniophytes

Division Chlorophyta

Division Chlorophycophyta

green algae

Division Cryptophyta

Phylum Cryptomonada

cryptomonads, cryptophytes

Division Cyanophyta

blue-green algae, cyanobacteria

Class Dictyochophyceae

Phylum Dictyochae

silicoflagellates

Division Dinophyta

Division Pyrrophyta

Division Pyrrophycophyta

Phylum Dinozoa

dinoflagellates, alveolates (in part)

Division Euglenophyta

Division Euglenophycophyta

Phylum Euglenozoa

euglenoids, euglenids, euglenozoa

Division Haptophyta

Class Prymnesiophyceae

Phylum Haptomonada

haptophytes, haptomonads,

coccolithophorids

Division Heterokontophyta

Division Chrysophycophyta

Kingdom Chromista (in part)

heterokonts (in part), chromists (in part), stramenopiles (in part), golden-brown algae

Class Phaeophyceae

Division Phaeophyta

Division Phaeophycophyta

Class Melanophyceae

Class Fucophyceae

brown algae

Class Raphidophyceae

Phylum Raphidophyta

chloromonads

Division Rhodophyta

Division Rhodophycophyta

red algae

Division Streptophyta

plants

Class Zygnematophyceae

desmids (in part)

       

 

 

  
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