Algae: Phylogeny andEvolutionØjvind Moestrup, University of Copenhagen, Copenhagen, Denmark

Ideas on the phylogeny and evolution of the algae are presently based on a combination of

ultrastructural, biochemical andmolecular data. Following the discovery that chloroplasts

of eukaryotic algae arose after one ormore symbiotic events, the term algae is now used as

a colloquial term for primitive plants, including both prokaryotic and eukaryotic species.

Definition of Algae

Algae is a general term for primitive plants, i.e. organismsusing the green pigment chlorophyll a in photosynthesis butlacking the features of more advanced organisms (e.g. flow-ering plants) such as a vascular system for internal transportof water and nutrients. Algae were until recently believed toconstitute a natural group of organisms, i.e. a group of re-lated species. Prokaryotic forms were classified as the divi-sion blue-green algae,while eukaryotic formswere classifiedin several divisions. However, the single feature uniting thealgae, the chlorophyll-a-based photosynthesis, is located inthe chloroplasts of eukaryotic algae, and chloroplasts havenow been shown unequivocally to be symbionts. This haschanged present ideas of algal phylogeny dramatically.See also: Algal photosynthesis; Chlorophyll: structure andfunction;Molecular phylogeny reconstruction; Prokaryoticsystematics: a theoretical overview

The ancestors of the eukaryotic algae are presently be-lieved to be phagotrophic amoebae and/or flagellates, i.e.organisms feeding on and digesting other organisms infood vacuoles in the cell (‘protozoa’). The chloroplast ofthe eukaryotic algae was at first thought to represent aningested, somewhat modified, blue-green alga. This idea isstill considered to be correct for some groups of algae.Instead of digesting the prey, the preywas retainedmore orless intact in the food vacuole of the host and photosyn-thesis was able to continue. Products from photosynthesissuch as carbohydrateswere subsequently transferred to thehost through the food vacuole membrane and utilized inthe metabolism of the host. This symbiosis was so suc-cessful that the host in many cases gave up phagotrophyaltogether and became an obligate phototroph. The blue-green alga remained in the cell of the host, separatedfrom the cytoplasm by two membranes. The innermostmembrane was thought to be the cell membrane of theblue-green alga, the outer membrane the food vacuolemembrane. Most of the deoxyribonucleic acid (DNA)from the blue-green algal genome was transferred to thehost nucleus. See also: Algal symbioses

Ultrastructural evidence accumulating from 1960s on-wards has shown that in many groups of algae this idea is

too simple. The chloroplasts are in many algal groups sep-arated from the cytoplasm by three or more membranes,whose origin was initially difficult to explain. However, thefinding of a second nucleus associated with the chloroplastof cryptophyte flagellates by Dennis Greenwood at Impe-rial College, London in 1974 served as an eye-opener. Itbecame suddenly clear that the chloroplast of cryptophytesis not a blue-green alga but an entire eukaryotic alga. Thisalga, however, was the result of a symbiosis between aprotozoan host and a blue-green alga. In other words, thechloroplast of cryptomonads arose as a result of two suc-cessive symbioses. Additional studies showed that thechloroplasts of other eukaroytic algae arose as a result of asmany as three consecutive symbioses, andF. J.R.Taylor in1974 coined the phrase ‘the serial endosymbiosis theory’.In some cases, chloroplasts were lost during subsequentevolution of the algae, complicating matters considerably.Studies of DNA base sequences have confirmed that

chloroplasts arose by one or more symbioses. They havealso given informationon the identity of theorganisms thatwere takenupduring the secondaryand tertiary symbioses.The organisms formerly classified as protozoa, algae andprimitive fungi are now grouped together as protists, andthe following account discusses the evolutionary origin ofthe algal groups of protists, based on ultrastructural, bio-chemical and molecular data. The term protist (KingdomProtista) goes back to the famous German zoologist ErnstHaeckel (1866, a contemporary of Charles Darwin), whoincluded under this term a number of the smaller-sizedalgae, in addition to Foraminifera, Myxomycetes (slimemoulds) and certain other groups of heterotrophic organ-isms. Protoctista was introduced byH. F. Copeland (1956)to include also larger algae such as brown and red algae.This term is now generally considered superfluous, how-ever, and Haeckel’s term protist is used for all primitiveeukaryotes previously known as algae, primitive fungi orprotozoa. See also: Darwin, Charles Robert; Foramini-fera; Protozoa; Protist systematics

Article Contents

Introductory article

. Definition of Algae

. Prokaryotic Algae

. Some Comments on the Evolution of Eukaryotes

. Algae whose Chloroplasts Arose after a Single

Symbiotic Event

. Algae whose Chloroplasts Arose by Secondary

Endosymbiosis

. Algae whose Chloroplasts Arose by Tertiary

Endosymbiosis

. Conclusions

doi: 10.1038/npg.els.0004231

1ENCYCLOPEDIA OF LIFE SCIENCES & 2005, John Wiley & Sons, Ltd. www.els.net

Prokaryotic Algae

Most prokaryotic algae possess a single type of chloro-phyll, chlorophyll a, while phycobilins and carotenoidsserve as accessory pigments. Such algae are classified asblue-green algae (or cyanobacteria, see below) and theyform one of the oldest groups of organisms on Earth, dat-ing back to the earliest days of organic evolution 3.5–4thousandmillion years ago. The oxygen of the present-dayatmosphere is thought to have evolved as a result of thephotosynthetic activity of blue-green algae. In the 1970s aunicellular prokaryote containing both chlorophylls a andb was discovered (Prochloron), growing as a symbiont insome tropical, marine ascidians. Subsequently, two addi-tional but free-living genera of what became known asprochlorophytes were discovered, one in marine and theother in freshwater plankton. The three genera were for awhile considered to comprise a second group of photosyn-thetic prokaryotes. However, gene studies have indicatedthat the three genera are only distantly related to eachotherand that they are related to different species of blue-greenalgae. This has resulted in the idea that chlorophyll b de-veloped from chlorophyll a several times: three times in thethree ‘prochlorophyte’ genera, and once in the progenitorof the green algal chloroplasts. Or, alternatively, thatchlorophyll b was present from very early on but was sub-sequently lost in many groups of algae. The class Pro-chlorophyta has nowbeen abandoned and the three generaare classified among the blue-green algae. Phylogeneticallyspeaking, the blue-green algae are related to Gram-nega-tive Eubacteria and this has given the group the nameCyanobacteria. Both the terms cyanobacteria and cyano-phyta (blue-green algae) are valid, the former stressingthe phylogenetic relationship to heterotrophic bacteria ofthe group Eubacteria, the latter the algal nature ofthe group (i.e. utilizing chlorophyll a for photosynthesis).See also: Algal photosynthesis; Algal pigments

Some Comments on the Evolution ofEukaryotes

The most recent studies have indicated that the eukaryotesfall into six major evolutionary groups (Figure 1). There areindications from DNA sequencing that all groups arosemore or less simultaneously during the geological historyof the Earth, and this origin probably dates back to at least1.5 billion years ago. Present evidence does not allow de-termination of the relative temporal appearance of the sixgroups (‘kingdoms’). A few smaller groups of protozoa donot seem to fit into any of the sixmain groups, and the totalnumber of kingdoms may increase when these organismsare examined in more detail. Based on sequencing of 18 sribosomal DNA (rDNA), it was for a time thoughtthat certain groups of organisms that lack chloroplasts,

mitochondria or even the Golgi apparatus were more an-cient, perhaps dating back to pre-chloroplast and pre-mi-tochondrial times. However, studies of other genes haveshown this to be incorrect, the organelles were lost sec-ondarily. See also: Eukaryotes and multicells: origin;Universal tree of life

Algae whose Chloroplasts Arose after aSingle Symbiotic Event

Kingdom Plantae

The chloroplasts of twoof themain groups of algae, the redand the green algae, are separated from the cytoplasm byonly two membranes, indicating that they arose by inges-tion and transformationof a blue-green alga. This has beenconfirmed by molecular studies. In the phylogenetic trees,red and green algae are often sister groups, indicatingthat they have a common ancestor. The kingdom contain-ing red algae and green plants also contains the classGlaucophyta (Glaucocystophyta), whose few members(less than 10 species) contain the so-called cyanelles in thecells. The cyanelles are undoubtedly blue-green algae, eachlocated in a vacuole and sometimes retaining a thin cellwall. The ultrastructure of the flagellar apparatus supportsthe idea of a phylogenetic relationship between glauco-phytes and green algae (red algae lack flagella altogether).The green plants (green algae,mosses and vascular plants),red algae and glaucophytes appear to form a natural groupthat has been given the somewhat misleading name ‘Plant-ae’. As mentioned above, the outer chloroplast membraneis thought to represent the food vacuole membrane of thehost. Recently, blue-green algal proteins have been foundin this membrane, leading to interpretation of the mem-brane as being of blue-green algal origin. In the blue-greenalgae, these proteins occur in the outermost layer of the cellwall, sometimes – and very confusingly – also termed amembrane. This terminology gives rise to misunderstand-ings and confusion. Blue-green algae are, like cells of otherorganisms, surrounded by a single membrane (the cellmembrane or plasmalemma). Chloroplasts of green or redalgae, however, are surrounded by two typicalmembranes.See also: Glaucocystophytes

Algae whose Chloroplasts Arose bySecondary Endosymbiosis

The large majority of algae obtained their chloroplasts bysecondary endosymbiosis. They are here grouped under sixheadings: cryptophytes, heterokonts, haptophytes, dino-flagellates and other alveolates, chlorarachniophytes andeuglenoids. Phylogenetically, they fall into three of the sixkingdoms in Figure 1. See also: Endosymbionts

Algae: Phylogeny and Evolution

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Kingdom Chromalveolata

The algae in this large group of organisms constitute Chris-tensen’sChromophyta (Christensen, 1962, 1980).Thegrouphas now extended to include also major groups formerlyclassified as Protozoa, notably ciliates and sporozoa (api-complexa), and heterokont fungi (e.g. Oomycetes) and hasbeen given the name Chromalveolates.

Cryptophytes

The cryptophytes stand out from all other algae particu-larly in the structure of the flagellar apparatus, but theyappear to be related to the haptophyte/heterokont assem-blage. Cryptophyte flagella are lined with flagellar hairsresembling the hairs on the anterior flagellum of het-erokonts but details are slightly different. Also, mi-tochondria of cryptophytes contain flat cristae-like redand green algae, rather than the tubular cristae of hetero-konts, dinoflagellates, haptophytes and numerous otherprotists. Sequence data have shown that the chloroplast incryptophytes is a transformed red alga, which lost all or-ganelles after ingestion except the chloroplast and the nu-cleus (now known as the nucleomorph). An additionalchlorophyll (of the chlorophyll c group) developed withinthe chloroplast, probably from chlorophyll a. Phycobilinschanged from forming distinct phycobilisomes on the thy-lakoid surface, as in red andblue-green algae, into lesswell-defined contents in the thylakoid lumen of cryptophytechloroplasts. Most of the nuclear DNA was transferred tothe host nucleus, leaving only three small chromosomesbehind in the nucleomorph.

Heterokonts and other stramenopiles

The heterokonts constitute a large group of organismspreviously classified as algae, fungi and protozoa. It wasshown early on by ultrastructural studies that these arerelated and form a natural group, and this has been con-firmedby gene sequencing.The algal heterokonts comprisethe chrysophyceans (golden algae), bacillariophyceans (di-atoms), raphidophyceans, xanthophyceans, eustigmato-phyceans and phaeophyceans (brown algae). Severalsmaller groups are sometimes classified as separate classes(synurophyceans, pelagophyceans, dictyochophyceans,etc.). The heterokonts are readily identified by the struc-ture of the motile stage, which is typically biflagellate. Theanterior flagellum carries two opposite rows of tripartitehairs, while the second, often posteriorly directed flag-ellum, is smooth. The chloroplast, if present, is surroundedby four membranes, indicating that a eukaryotic prey wasengulfed and transformed into a chloroplast, as happenedin cryptophytes. During this transformation all organelleswere lost except the chloroplast and a few cisternae. Thecombination of pigments includes chlorophyll a and vari-ous types of chlorophyll c, plus the carotenoid fucoxan-thin. This combination is shared with haptophytes. Theancestor of the chloroplast in these groups may also be ared algae, but DNA studies have indicated that heterotro-phic heterokonts arose before the phototrophic ones. Theterm stramenopiles (straminopiles) is sometimes used as acommon term for heterokonts (i.e. species with one hairyflagellum carrying tripartite flagellar hairs and one smoothflagellum) and related organisms such as opalinids, pro-teromonads, etc. whose flagella are different.

Plantae

Green algae,mosses, vascularplants

GlaucophytesRed algae

Amoebozoa(Lobose amoebae)

Mycetozoan slime moulds

Pelobionts,Entamoebae

OpisthokontaAnimals

Choano-flagellates

IchthyosporeaNucleariid amoebae

Fungi (inc.microsporidia)

Chromalveolata

AlveolatesStramenopiles

HaptophytesCryptophytes Rhizaria

RadiolariaCercozoa (inc. Foraminifera?)

Excavata

Euglenozoa, Heterolobosea, Jakobids

Diplomonads,Retortamonads,Carpediemonas,Parabasalids

Oxymonads,Trimastix

Malawimonas

Apusomonads

Centrohelid HeliozoaCollodictyonids

Eukaryotes

Prokaryotes

Figure 1 Phylogenetic tree, illustrating present ideas on the relationships between algal and other groups of protists. Six main branches (‘kingdoms’)

have been drawn to radiate from approximately the same point, indicating that the branches appeared at approximately the same time during the historyof the Earth. (After Simpson and Roger (2004).

Algae: Phylogeny and Evolution

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Haptophytes

The haptophytes differ from other algae particularly in thestructure of the flagellar apparatus and in the possession ofa haptonema, an organelle, not known in any other groupof protists. The chloroplast is very similar to that of manyheterokonts, but several types of the pigment fucoxanthinoccur. Haptophytes share numerous ultrastructural fea-tures with chrysophyceans. In DNA studies, the ha-ptophytes usually form a sister group to the heterokonts.Heterotrophic haptophytes also exist but whether this is aprimitive condition within the class is not known.

Dinoflagellates

Dinoflagellates belong to the other major section of thechromalveolates. They constitute a relatively well-definedgroup, now known to be related to ciliates and apicom-plexanprotozoa (the latter groupalso knownas sporozoa).They differ from other algae particularly in the structure ofthe nucleus, mitosis and details of the flagellar apparatus.The cell wall, if present, is composed of cellulosic platesdeposited in flat cisternae beneath the plasma membrane.Similar cisternae are present in ciliates and apicomplexans,and nucleotide sequencing has confirmed that the threegroups are interrelated. Together they are now known asthe ‘Alveolata’. A small group of parasites known as theperkinsids appears to form a phylogenetic link betweendinoflagellates and apicomplexans.Only half of the knowndinoflagellates are photosynthetic. Many others arephagotrophic, some ingesting their prey (other algae, evenweakened cells of their own kind) by sucking out the con-tents of the prey through the so-called peduncle. Thisprobably accounts for the chloroplast diversity found indinoflagellates. It indicates that endosymbiosis took placeindependently several times. The cytoplasm of the end-osymbiontwas retained in food vacuoleswhile the prey cellmembrane was usually left behind. Some dinoflagellateseven obtained their photosynthetic apparatus by tertiarysymbiosis (see below). See also: Phagocytosis

Kingdom Rhizaria

Chlorarachniophytes

The chlorarachniophytes resemble cryptomonads in pos-sessing a nucleomorph-containing chloroplast, but theyare otherwise very different. When originally studied byelectron microscopy, they were found to share features ofthe brown and the green lines of evolution but we knownow that they are not related to any other algae. The fewspecies known are green, containing both chlorophylls aand b, and they probably obtained the chloroplast fromingestion and transformation of a green alga. Ultrastruc-turally, they are very unlike any other group of protists.Their relationship to other protist groups remains unre-

solved but someDNA sequencing have indicated that theybelong in a diverse assemblage, ‘Rhizaria’, which com-prises species formerly classified as Protozoa, and includesRadiolaria, Foraminifera and cercomonads. See also:Chlorarachniophytes

Kingdom Excavata

Euglenoids

The euglenoid flagellates form a well-defined group ofphototrophic and heterotrophic organisms. They differfrom other algae in the ultrastructure of almost all cellorganelles and they are related to none of these. They are,however, related to two groups of heterotrophic flagellates,the bodonid and trypanosome protozoa, forming a sistergroup to these two groups. Together the three groups areknown as the ‘Discicristata’ because of their disc-shapedmitochondrial cristae. The chloroplast of euglenoids al-most certainly originated by ingestion of a green alga. Pig-ments of the two groups are similar but formation of starchin the chloroplast of green algae was replaced after estab-lishment of symbiosis with formation of another carbohy-drate, paramylon, in the cytoplasm. It has been suggestedthat the chloroplast of euglenoids arose after uptake ofgreen algal chloroplasts rather than whole cells of greenalgae. This is not likely, however, since chloroplasts do notcontain all the genetic material necessary for their contin-uous function, essential genes reside in the nucleus. Thediscicristate protists are now classified in Kingdom Exca-vata that includes many very unusual organisms such asdiplomonads and parabasalids, whose cells lack mi-tochondria. See also: Trypanosoma

Algae whose Chloroplasts Arose byTertiary Endosymbiosis

A few dinoflagellates group together under this heading.They are not all related, indicating that tertiary endosym-biosis took place independently in the three groups men-tioned below.Several freshwater dinoflagellates are of a blueish colour

and contain either a little-transformed blue cryptophyte, ora more normal-looking but blue chloroplast surrounded bythree membranes. The chloroplasts in all cases representtransformed cryptophytes, in other words a tertiary symbi-osis. The cryptophytes have in some species been retainedrelativelyunchanged,while inother species theyare stronglymodified, having lost most organelles and membranes.A few brown or yellow-brown dinoflagellates, well

known as fish killers in the sea, contain aberrant pigmentsin their three-membraned chloroplasts (Karenia brevis,K. mikimotoi, Karlodinium veneficum). The chloroplasts

Algae: Phylogeny and Evolution

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almost certainly have their origin in the haptophytes,whose chloroplasts may contain very similar pigments.

Cells of Peridinium balticum (also known as Durinskiabaltica) contain an entire chloroplast-containing eukaryo-tic cell within its cytoplasm, and there are indications fromgene sequencing that this endosymbiont is a transformeddiatom. It lacks the siliceous frustule. The diatom cyto-plasm is separated from the dinoflagellate cytoplasm by asingle membrane, probably a food vacuole formed bythe dinoflagellate, which may have obtained the end-osymbiont by sucking out the contents of a diatom into thefood vacuole.

Finally, a very unusual transformation has taken placein a small group of dinoflagellates whose chloroplast hasbecome modified into an eyespot (Kryptoperidiniumfoliaceum, Peridinium quinquecorne, etc.), still surroundedby three membranes. These species – or more preciselytheir common ancestor – apparently engulfed a secondeukaryotic alga and transformed it into another chlorop-last! Thus the cell contains two endosymbionts, obtainedby two tertiary endosymbioses. One of the symbiontsserves as eyespot, the other as chloroplast. Recent studieshave indicated that the few known species with this com-plement of organelles are interrelated, and apparently alsorelated to D. baltica mentioned above.

The implications of this series of endosymbioses on thecell’s genetic material are difficult to imagine. Consider-ing that genes are transferred from the symbionts to thehost nucleus following the establishment of a symbiosis,the nucleus of Kryptodinium and its relatives may beexpected to contain genetic material from both the ter-tiary endosymbioses and from the cell’s mitochondria, inaddition to its own genetic material. However, as theeyespot and the chloroplast both arose after a secondaryendosymbiosis they may also be expected to containgenetic material from several organisms! And some ofthis may actually have been transferred to the dinoflag-ellate nucleus. This exceedingly complex situation isdifficult to assess, the dinoflagellate is a Pandora’s boxin which genetic material is transferred between theboxes.

Conclusions

It is clear from the data presented above that the algae donot form a natural group of phylogenetically related organ-isms. One group is more related toGram-negative bacteria,others are related to different groups of protozoa, othersagain to higher plants. The term algae is still useful, but itshould now be regarded as a term on par with ‘trees’,‘xerophytes’, etc. There are similar problems with delinea-tion of ‘bacteria’, ‘animals’, ‘protozoa’, ‘plants’ and ‘fungi’.Numerous cases have been found in which algae possessinga fully functional photosynthetic apparatus are also capableof phagotrophy, the food-uptake process associated withanimal cells. This so-called mixotrophy applies to manychrysophycean heterokonts in particular, and to dinoflag-ellates and haptophytes. It gives the cells the capability toswitch between phototrophy and phagotrophy, dependingon external conditions such as light, prey availability, etc.It seems likely that such organisms were previouslyphagotrophs and retained the capability of phagotrophyafteroneof theprey cellswas establishedas aphotosyntheticsymbiont. See also: Algal taxonomy: historical overview

Further Reading

Bhattacharya D (1997) Origins of Algae and their Plastids. Vienna:

Springer.

Christensen T (1980) Algae. A Taxonomic Survey, fasc. 2. Odense: AiO

Print.

Gibbs SP (1981) The chloroplasts of some algal groupsmay have evolved

from endosymbiotic algae. Annals of the New York Academy of Sci-

ences 361: 193–208.

Green JG, Leadbeater BSC and Diver WL (1989) The Chromophyte

Algae. Problems andPerspectives. The Systematics Association, special

vol. 38. Oxford: Clarendon Press.

Irvine DEG and John DM (1984) Systematics of the Green Algae. The

Systematics Association, special vol. 27. London: Academic Press.

Ragan MA (1998) On the delineation and higher-level classification of

algae. European Journal of Phycology 33: 1–15.

Simpson AG and Roger AJ (2004) The real ‘kingdoms’ of eukaryotes.

Current Biology 14: R693–R696.

van den Hoek C, Mann DG and Jahns HM (1995) Algae. An Introduc-

tion to Phycology. Cambridge: Cambridge University Press.

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