DEFINING THE MAJOR LINEAGES OF RED ALGAE (RHODOPHYTA)1

DEFINING THE MAJOR LINEAGES OF RED ALGAE (RHODOPHYTA)1

Hwan Su Yoon

Department of Biological Sciences and Roy J. Carver Center for Comparative Genomics, University of Iowa, 468 Biology

Building, Iowa City, Iowa 52242, USA

Kirsten M. Muller

Department of Biology, University of Waterloo, Waterloo, ON, Canada N2L 3G1

Robert G. Sheath

Office of the Provost, California State University San Marcos, San Marcos, California 92096, USA

Franklyn D. Ott

905 NE Hilltop Drive, Topeka, Kansas 66617, USA

and

Debashish Bhattacharya2

Department of Biological Sciences and Roy J. Carver Center for Comparative Genomics, University of Iowa, 446 Biology

Building, Iowa City, Iowa 52242, USA

Previous phylogenetic studies of the Rhodophytahave provided a framework for understanding redalgal phylogeny, but there still exists the need for acomprehensive analysis using a broad sampling oftaxa and sufficient phylogenetic information toclearly define the major lineages. In this study, wedetermined 48 sequences of the PSI P700 chl aapoprotein A1 (psaA) and rbcL coding regions andestablished a robust red algal phylogeny to identifythe major clades. The tree included most of the lin-eages of the Bangiophyceae (25 genera, 48 taxa).Seven well-supported lineages were identified withthis analysis with the Cyanidiales having the earliestdivergence and being distinct from the remainingtaxa; i.e. the Porphyridiales 1–3, Bangiales, Flori-deophyceae, and Compsopogonales. We also analy-zed data sets with fewer taxa but using seven pro-teins or the DNA sequence from nine genes toresolve inter-clade relationships. Based on all ofthese analyses, we propose that the Rhodophytacontains two new subphyla, the Cyanidiophytinawith a single class, the Cyanidiophyceae, and theRhodophytina with six classes, the Bangiophyceae,Compsopogonophyceae, Florideophyceae, Por-phyridiophyceae classis nov. (which contains Por-phyridium, Flintiella, and Erythrolobus), Rhod-ellophyceae, and Stylonematophyceae classis nov.(which contains Stylonema, Bangiopsis, Chroodacty-lon, Chroothece, Purpureofilum, Rhodosorus, Rho-

dospora, and Rufusia). We also describe a neworder, Rhodellales, and a new family, Rhodellaceae(with Rhodella, Dixoniella, and Glaucosphaera).

Key index words: Bangiophyceae; Compsopogono-phyceae; Cyanidiophyceae; Florideophyceae;Porphyridiophycae; red algal lineages; Rhod-ellophyceae; Rhodophyta; Stylonematophyceae

Abbreviations: BPP, Bayesian posterior probabili-ties; ML, maximum likelihood; MP, maximum par-simony; PsaA, PSI P700 chlorophyll a apoproteinA1; PsaB, PSI P700 chlorophyll a apoprotein A2;PsbA, PSII reaction center protein D1; PsbC, PSII44 KD apoprotein; PsbD, PSII D2 reaction centerprotein; TBR, tree bisection-reconnection

The red algae (Rhodophyta) are a distinct eukaryoticlineage whose members are united in phylogenetic anal-yses of nuclear, plastid, and mitochondrial genes (Fresh-water et al. 1994, Ragan et al. 1994, Van de Peer and DeWachter 1997, Burger et al. 1999, Yoon et al. 2002b,2004). Rhodophytes lack chl b and c but contain all-ophycocyanin, phycocyanin, and phycoerythrin in theform of phycobilisomes on unstacked thylakoids. Theplastid in these taxa is bound by two membranes andproduces floridean starch that is deposited in the cyto-plasm. All members of this group lack flagella and cent-rioles in all stages of the life history (Gabrielson et al.1990, Graham and Wilcox 2000). It is believed that thered algal plastid originated from a cyanobacterial pri-mary endosymbiosis and this organelle shares a com-mon ancestry with green and glaucophyte algae

1Received 13 September 2005. Accepted 27 December 2005.2Author for correspondence: e-mail debashi-bhattacharya@

uiowa.edu.

482

J. Phycol. 42, 482–492 (2006)r 2006 Phycological Society of AmericaDOI: 10.1111/j.1529-8817.2006.00210.x

(Bhattacharya and Medlin 1995, Delwiche et al. 1995,Cavalier-Smith 1998, McFadden 1999, Bhattacharyaet al. 2004, Rodrıguez-Ezpeleta et al. 2005). These three‘‘primary’’ plastid-containing groups are considered tobe taxonomically united in the kingdom Plantae (Cava-lier-Smith 1998) or Archaeplastida (Adl et al. 2005).

Traditionally, the phylum Rhodophyta has been di-vided into two classes (or subclasses), Bangiophyceae(Bangiophycidae) and Florideophyceae (Florideo-phycidae) (Garbary and Gabrielson 1990). However,recent studies have concluded that the Florideo-phyceae form a monophyletic group with the orderBangiales (Oliveira and Bhattacharya 2000, Mulleret al. 2001, Yoon et al. 2002b, Saunders and Hommer-sand 2004). The Bangiophyceae, which has in the pastbeen divided into six orders (Bangiales, Cyanidiales,Compsopogonales, Erythropeltidales, Porphyridiales,and Rhodochaetales), is now considered to form a se-ries of radiations that define the ancestral lineages ofthe red algae (Gabrielson et al. 1985, Freshwater et al.1994, Ragan et al. 1994). Comprehensive phylogeneticstudies of the Bangiophyceae (Oliveira and Bhatta-charya 2000, Muller et al. 2001, 2003, West et al. 2005)using the plastid and nucleus-encoded small subunit(SSU) rDNA and plastid rbcL show furthermore thatthe Porphyridiales are paraphyletic and comprise atleast three independent lineages. This result is gener-ally consistent with previous morphological studiesthat show great differences in plastid ultrastructureand variable vegetative and reproductive anatomy(Gabrielson et al. 1985, 1990, Garbary and Gabrielson1990, Muller et al. 2001). However, all of these previ-ous studies are characterized either by broad taxonsampling with a single gene (Muller et al. 2001) ornarrow sampling with multiple genes (Yoon et al.2002b, 2004). For this reason, whereas the identity ofthe major red algal lineages has been relatively firmlyestablished, their interrelationships remain unclear.Recently, Saunders and Hommersand (2004) pro-posed a new red algal taxonomic scheme based onprevious molecular phylogenies and ultrastructuralcharacters (e.g. Golgi–ER association). Their taxo-nomic system is a large step forward but still containsthe paraphyletic class Rhodellophyceae that includesboth unicellular and pseudofilamentous forms (i.e.Porphyridiales Kylin ex Skuja 1939, StylonematalesK. Drew 1956, and ‘‘Porphyridiales 1’’ sensu Mulleret al. 2001).

In this study, we determined 48 sequences from thePSI P700 chl a apoprotein A1 (psaA) and rbcL codingregions with broad taxonomic sampling. We includedmost of the lineages of Bangiophyceae (25 genera, 48taxa) in the analyses because these taxa represent theancestral pool of red algae. In addition, we analyzeddata sets with fewer taxa but using seven proteins orDNA sequence from nine genes to resolve inter-claderelationships. The combination of all of these phylo-genetic studies was then used to advance our under-standing of the higher-level taxonomic relationshipswithin the red algae.

MATERIALS AND METHODS

Taxon sampling and sequencing. Forty-eight red algal taxawere used to infer the phylogeny of the Bangiophyceae (Ta-ble 1). The data set included all bangiophycean orders and25 genera from the different phylogenetic lineages (Garbaryand Gabrielson 1990, Muller et al. 2001). Our alignment alsoincluded 10 green algae, two glaucophytes, and three cyano-bacteria as the outgroup (Bhattacharya and Medlin 1995,Moreira et al. 2000). We obtained algal cultures from theCulture Collection of Algae & Protozoa (CCAP), Provasoli-Guillard National Center for Culture of Marine Phytoplank-ton (CCMP), the Dipartimento di Biologia Vegetale (DBV)culture collection at the University of Naples, the Sammlungvon Algenkulturen (SAG) at the University of Gottingen, andthe Culture Collection of Algae at the University of Texas atAustin (UTEX). Some of the bangiophytes were collected inthe field and/or maintained in the private collection of F. D. Ott.

The algal cells were frozen in liquid nitrogen and groundwith glass beads using a glass rod and/or Mini-BeadBeatert(Biospec Products Inc., Bartlesville, OK, USA). Total genomicDNA was extracted using the DNeasy Plant Mini Kit (Qiagen,Santa Clarita, CA, USA). PCR were carried out using specificprimers for each plastid gene (Yoon et al. 2002a). Because in-trons were found in the psaA gene of some red algae, the RT-PCR method was used to isolate cDNA for these coding regions(H. S. Yoon et al. unpublished data). The PCR products werepurified using the QIAquick PCR Purification Kit (Qiagen),and were used for direct sequencing using the BigDyet Ter-minator Cycle Sequencing Kit (PE-Applied Biosystems, Nor-walk, CT, USA), and an ABI-3700 at the Roy J. Carver Centerfor Comparative Genomics at the University of Iowa. SomePCR products were cloned into the pGEM-T vector (Promega,Madison, WI, USA) before sequencing.

Phylogenetic analyses. We primarily used amino acid se-quences in the phylogenetic analysis in order to minimizepotentially misleading phylogenetic signal because of DNAmutation bias at the third positions of codons (Sandersonet al. 2000, Pinto et al. 2003) or because of heterogeneouscodon usage (Inagaki et al. 2004). The protein sequenceswere manually aligned using SeqPup (Gilbert 1995). Twodata sets were used in the phylogenetic analyses and thealignments are available from D. Bhattacharya. In the firstdata set, we generated a concatenated alignment of sevenplastid-encoded proteins (7PEP; a total of 2564 aa): PsaA(465 aa), PSI P700 chlorophyll a apoprotein A2 (PsaB, 422aa), PSII reaction center protein D1 (PsbA, 319 aa), PSII 44KD apoprotein (PsbC, 334 aa), PSII D2 reaction center pro-tein (PsbD, 296 aa), RbcL (405 aa), and TufA (323 aa), from16 bangiophytes, and from 15 outgroup taxa including greenand glaucophyte algae and cyanobacteria. Because the rbcLgene of the green and glaucophyte algae are of a cyanobac-terial origin, whereas those in the red algae and red algal-derived plastids are of proteobacterial origin (Valentin andZetsche 1990, Delwiche and Palmer 1996), the evolutionarilydistantly related green and glaucophyte rbcL sequences werecoded as missing data in the phylogenetic analyses. In thesecond amino acid data set, we combined only PsaA and RbcL(2PEP), and added 33 more bangiophytes to the alignment(now a total of 49 bangiophytes). The Cyanidiales, which isthe earliest diverging clade of red algae (Yoon et al. 2002b,2004), was used as the outgroup for this data set. In additionto the amino acid data, we generated a DNA alignment thatincluded nuclear SSU rDNA (18S; 1486 bp) and plastid SSUrDNA (16S; 1285 bp) sequences resulting in a nine-geneDNA sequence data set (9GDS; 10,463 bp) that excludedthe green and glaucophyte algae. Three additional Cyanidi-ales species were included in the DNA alignment and used asthe outgroup for this data set.

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All protein phylogenies were reconstructed under maxi-mum likelihood (ML) using proml in the PHYLIP V3.6b pro-gram package (Felsenstein 2002). The trees were inferred withthe JTTþG evolutionary model and global rearrangementswith four random addition replicates (Jones et al. 1992). The avalues for the g distribution for the different data sets werecalculated using TREE-PUZZLE V5.2 (Schmidt et al. 2002). Toassess the stability of monophyletic groups in the ML trees, wecalculated bootstrap support values using PHYML V2.4.3(Guindon and Gascuel 2003) and unweighted maximum par-simony (MP) using PAUP*V4.0b10 (Swofford 2004). We alsocalculated Bayesian posterior probabilities (BPP) usingMrBayes (V3.0b4, Huelsenbeck and Ronquist 2001). In theBayesian inference of the amino acid data, we used theWAGþG model with Metropolis-coupled Markov chain Mon-te Carlo from a random starting tree. These analyses were runfor 1,000,000 generations with trees sampled each 200 cycles.Four chains were run simultaneously of which three wereheated and one was cold, with the initial 20,000 cycles (200trees) being discarded as the ‘‘burn in.’’ A consensus tree wasmade with the remaining 1800 phylogenies to determine theposterior probabilities at the different nodes. In the MP anal-yses, 1000 bootstrap replicates were analyzed (Felsenstein1985) with 10 heuristic searches with random-addition-se-quence starting trees and tree bisection-reconnection (TBR)branch rearrangements. For the ML bootstrap analysis (500replicates), we used the JTTþG evolutionary model.

For the DNA data set, we used ML and BPP approaches.We used a site-specific GTR model to incorporate differentrates in the genes at the three codon positions. This approachappears to be superior to using a single set of rate parametersfor protein-coding DNA sequences (Shapiro et al. 2005). Fivedifferent rates were used to account for among-site rate var-iation (0.50931, 18S; 0.43367, 16S; 0.60518, 1st codon;0.16149, 2nd codon; 2.80154, 3rd codon). For the ML analy-sis, global rearrangements and random sequence addition rep-licates (five rounds) were used with TBR branch swapping.The unweighted MP analysis was performed as describedabove.

RESULTS AND DISCUSSION

The seven major lineages of red algae. Seven well-supported lineages were identified within the red al-gae (Figs. 1 and 2). The Cyanidiales was the earliestdivergence in the plastid protein tree and was distinctfrom the remaining red algal lineages (i.e. the Por-phyridiales-(1), Porphyridiales-(2), Porphyridiales-(3), Bangiales, Florideophyceae, and Compsopogon-ales). The Porphyridiales-(2) and the Compsopogon-ales were united in a clade (495% BPP, 55% MP; Fig.2), whereas the Porphyridiales-(1) grouped togetherwith the monophyletic clade of BangialesþFlorid-eophyceae (495% BPP, 76% ML; Fig. 1). The exist-ence of these seven red algal lineages in the plastidtrees is consistent with analyses of nuclear SSU rDNA(Muller et al. 2001), plastid SSU rDNA (Oliveira andBhattacharya 2000), and multi-gene plastid data set(Yoon et al. 2002b, 2004).

Although we used an extensive concatenated dataset of 7PEP (2564 aa) in our analyses, the lineage re-lationships were weakly supported except for the earlydivergence point of the Cyanidiales and the Bangi-alesþFlorideophyceae sister group relationship. Wethen added 18S and 16S rDNA sequences to the seven-T

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gene DNA sequence data set (9GDS; total 10,463 bp) inan attempt to increase the phylogenetic resolution.Three additional Cyanidiales species were added totest the interrelationship of these taxa and this cladewas used to root the tree. The ML phylogeny tree in-ferred from these data using the site-specific GTRmodel was similar to the 7PEP tree, except for the po-sition of the Porphyridiales-(3) lineage (Fig. 2). Similarto the 7PEP phylogeny, the Compsopogonales andPorphyridiales-(2) grouped together (55% ML) andthe Porphyridiales-(1) showed a weak sister group re-lationship (495% BPP, 53% ML) to the Bangiales andFlorideophyceae. Our analyses highlight the inherentdifficulties in resolving the intra-lineage relationshipsof the red algae (except for the position of the Cya-nidiales and the monophyly of the BangialesþFlorid-eophyceae). This may reflect a rapid radiation of thered algal lineages or poor resolving power of plastidsequences.

There are two important fossils to interpret theevolutionary history of the red algae. One is the well-preserved Bangia-like multicellular filamentous fossil,Bangiomorpha pubescens (Butterfield 2000). This fossilwas found from the approximately 1200 million yearold (Ma) Hunting Formation in Somerset Island, Can-ada, and contains putative spores that indicate sexualdifferentiation. The second fossil is of Corallinales(florideophytes) that contain typical reproductivestructures from the 599 Ma Doushantuo Formation,China (Xiao et al. 1998, 2004). Xiao et al. (2004) sug-gested the florideophyte—bangiophyte divergence tohave occurred in the Neoproterozoic or earlier. Based

on these fossils and our phylogeny, we postulate thatafter the divergence of the Cyanidiales, the five majorred algal lineages radiated around 1200 Ma, likely overa relatively short evolutionary time period. Thereafter,

FIG. 1. Bangiophycean red algal phylo-geny inferred using the maximum likeli-hood (ML) method and the combinedplastid protein sequences of PSI P700chlorophyll a apoprotein A1, PSI P700chlorophyll a apoprotein A2, PSII reactioncenter protein D1, PSII 44 KD apoprotein,PSII D2 reaction center protein, RbcL,and TufA. The results of a ML bootstrapanalysis are shown above the branches,whereas the values below the branches re-sult from a maximum parsimony bootstrapanalysis. The thick branches represent495% Bayesian posterior probability.

FIG. 2. Bangiophycean red algal phylogeny inferred usingthe maximum likelihood (ML) method and the combined DNAsequences of 18S rDNA, 16S rDNA, PSI P700 chlorophyll aapoprotein A1, PSI P700 chlorophyll a apoprotein A2, PSIIreaction center protein D1, PSII 44 KD apoprotein, PSII D2reaction center protein, rbcL, and tufA. The results of a MLbootstrap analysis are shown above the branches, whereas thevalues below the branches result from a maximum parsimonybootstrap analysis. The thick branches represent 495% Bayesianposterior probability.


the Florideophyceae diverged from the ancestor of theBangiales before 599 Ma when the coralline algae di-verged from the stem of florideophytes. Yoon et al.(2004) estimated divergence times using molecularclock methods and proposed the following dates forthe split of the red algae (1449–1513 Ma), Cyanidiales(1350–1416 Ma), and florideophytes (around 800 Ma,see Fig. 3 in Yoon et al. 2004).

Novel findings of our study. Porphyridiales-(2): Por-phyridiales-(2) is comprised of mostly pseudo-filamentous, filamentous, or colonial multicellulartaxa (Bangiopsis, Chroodactylon, Chroothece, Kyliniella,Purpureofilum, and Stylonema), but also includes uni-cellular forms such as Rhodosorus, Rhodospora, andRufusia (Fig. 3). Most members of this lineage con-tain sorbitol/digeneaside or only sorbitol as a low mo-lecular weight carbohydrate (Karsten et al. 2003,West et al. 2005). In addition all species of Porphy-ridiales-(2) contain putative group II introns in thepsaA gene at conserved positions (H. S. Yoon et al.unpublished data). These ribozymes are unique andare potentially a diagnostic character for this lineage.Group II introns are common in the green algaeand in green algal-derived plastids [e.g. Euglena andChlamydomonas (Odom et al. 2004, Perron et al. 2004,Sheveleva and Hallick 2004)] but apparently are rarein the red algae. Our preliminary phylogenetic analy-ses of the Pophyridiales-(2) group II introns show thatsequences at the homologous genic site 229 in psaAdiffer significantly in sequence from other intronspresent in Flintiella [position 219, Porphyridiales-(3)]and Rhodella [position 91, Porphyridiales-(1)]. It is like-ly that the introns at position 229 share a single origin(H. S. Yoon et al. unpublished data). This finding sug-gests that these mobile elements invaded the psaA gene(and potentially other sequences) in the plastid gen-ome of the common ancestor of Porphyridiales-(2) andhave been maintained in some taxa.

Rufusia pilicola diverges first in the Porphyridiales-(2). This poorly studied species was isolated fromsloth’s hair by one of the authors (F. D. Ott). The ma-terial came from the coastal city of Limon, Costa Rica(provided by Dr. Arroyo). The other species of Por-phyridiales-(2) occur in a variety of habitats, includingmarine, freshwater, and in caves. Bangiopsis and Kylini-ella make a well-supported monophyletic group withPurpureofilum that is sister to two Stylonema strains. TheSAG stain of S. alsidii formed a well supported a cladewith the UTEX strain. The S. alsidii UTEX strain hadbeen recognized as Goniotrichum elegans (Chauvin) V.May 1965, whereas the SAG strain was renamed fromGoniotrichum alsidii. Because these two S. alsidii strainsshow a high sequence divergence (79 substitutionsamong 2610 bp) in the psaA and rbcL genes, a moredetailed monographic study of Stylonema, including ex-amination of type specimens is required to verify thespecies delimitation.

Porphyridiales-(3): The Porphyridiales-(3) lineageincludes the three unicellular genera Erythrolobus,Flintiella, and Porphyridium. The three species of

Porphyridium are phylogenetically distinct from theFlintiella and Erythrolobus clade. It was previously re-ported that Flintiella and Porphyridium share the asso-ciation of the golgi with the mitochondria and ER(Scott et al. 1992) and floridoside as a low molecularweight carbohydrate (Karsten et al. 2003).

Compsopogonales: This lineage consists of onefreshwater order Compsopogonales and two marineorders Erythropeltidales and Rhodochaetales. Sah-lingia, Chlidophyllon, and Pyrophyllon are included inthis lineages (Kornmann 1989, Nelson et al. 2003).All of these species are multicellular, though withvaried morphologies. Although our two-gene phylo-geny (Fig. 3) did not support the monophyly ofCompsopogon spp. with Boldia erythrosiphon (as wouldbe expected; Rintoul et al. 1999, Muller et al. 2001),the nuclear SSU rDNA and the plastid multi-geneanalyses show a sister group relationship of the Er-ythropeltidales and Rhodochaetales (Zuccarello et al.2000, Muller et al. 2001, Yoon et al. 2002b) with theCompsopogonales and B. erythrosiphon. We were,however unable to isolate the psaA coding regionfrom B. erythrosiphon and only used the rbcL sequencein this analysis. Rintoul et al. (1999) suggested thatComposopogon coeruleus and Compsopogoniopsis le-ptocladus should be recognized as the single species,

FIG. 3. Bangiophycean red algal phylogeny inferred usingthe maximum likelihood (ML) method and the combined plastidprotein sequences of PSI P700 chlorophyll a apoprotein A1 andRbcL. The results of a ML bootstrap analysis are shown abovethe branches, whereas the values below the branches result froma maximum parsimony bootstrap analysis. The thick branchesrepresent 495% Bayesian posterior probability.


C. coeruleus, based on the identity in the sequence ofSSU rDNA and rbcL.

Taxonomic conclusions. A classification system for agroup of organisms should reflect its phylogeny. Areliable phylogeny ideally uses both broad taxonsampling and sufficient phylogenetic information.This study used analyses of seven- and nine-genedata sets with selected taxa, and a two-gene data setthat encompassed most of the bangiophycean genera.Although many clade interrelationships are still un-resolved, we clearly identified seven red algal lineag-es that should be recognized at the class-level. TheCyanidiophyceae diverged first in red algal evolutionand is separated from the remainder of the red algallineages. Hence, we propose the creation of two newsubphyla, Cyanidiophytina, for this grouping, andRhodophytina that encompasses the rest of the class-es. Saunders and Hommersand (2004) treated theCyanidiophyceae as the phylum Cyanidiophyta withanother phylum Rhodophyta under the subkingdomRhodoplantae. However, we believe that it is not ne-cessary to divide the red algae into two phyla becausethis group, including the cyanidiophytes, is phylo-genetically distinct in eukaryotic trees (Rodrıguez-Ezpeleta et al. 2005) and they share important bio-chemical features with other red algae such as thebiosynthesis of floridean starch in the cytoplasm(Barbier et al. 2005). In addition, all rhodophytesshare an important synapomorphy, a plastid boundby two membranes that lacks chl b or c. Rather, ourdata indicate that it is appropriate to divide therhodophytes into two subphyla, maintaining thetraditional characteristics of the phylum as a whole(Fig. 4). Under this taxonomic scheme the subphy-lum Rhodophytina contains six classes: Bangio-phyceae, Compsopogonophyceae, Florideophyceae,Porphyridiophyceae, Rhodellophyceae, and Stylo-nematophyceae. The interrelationships among theclasses of the subphylum Rhodophytina are unclearexcept for the monophyly of the Bangiophyceae and

the Florideophyceae. We did not find any phylo-genetic evidence to unite the Porphyridiales into asingle clade (as suggested by Saunders and Hommer-sand 2004). This (negative) evidence does not dis-prove Porphyridiales monophyly. However, itsuggests that if all three or a subset of the lineagesshare a monophyletic origin, the branch that unitesthem may prove difficult to establish unless a greatdeal more (or with higher phylogenetic resolution)sequence data is brought to bear on this issue. Ourtrees do, however, demonstrate an ancient split oftaxa formerly classified in the Porphyridiales. Forthese reasons, we chose to recognize this group asthree independent clades within the Rhodophytina.

Phylum Rhodophyta Wettstein 1901Subphylum 1: Cyanidiophytina H. S. Yoon, K. M.

Muller, R. G. Sheath, F. D. Ott et D. Bhattacharya,subphylum nov.

Rhodophyta unicellularis, forma globosa vel el-liptica; habitatio thermae acidae; cum pariescrassus vel paries absens; heterotrophicus vel au-totophicus; cellulae divisionem vel endospora.Unicellular red algae, spherical or elliptical inshape, inhabiting in acidic and high temperatureenvironment; thick cell wall or lack of cell wall;facultative heterotrophs or obligate photo-autotrophs; cell division or endospore form-ation.

Class Cyanidiophyceae Merola, Castaldo, DeLuca, Gambardella, Musacchio et Taddei 1981

Order Cyanidiales Christensen 1962Family 1 Cyanidiaceae Geitler 1935Genera Cyanidium, CyanidioschyzonFamily 2 Galdieriaceae Merola, Castaldo, DeLuca, Gambardella, Musacchio et Taddei 1981Genus Galdieria

FIG. 4. Red algal phylogeny and alterna-tive taxonomic schemes.


Subphylum 2: Rhodophytina

Unicellular, pseudofilamentous or multicellularred algae; various plastid morphologies and or-ganellar associations; life histories unknown orwhere known biphasic or triphasic.

Class 1: Bangiophyceae Wettstein 1901

Order Bangiales Nageli 1847Family Bangiaceae Engler 1892Genera Bangia, Dione, Minerva, Porphyra, Pseudo-bangia

Class 2: Compsopogonophyceae G. W. Saunders etHommersand 2004

Order 1 Compsopogonales Skuja 1939Family 1 Boldiaceae Herndon 1964Genus BoldiaFamily 2 Compsopogonaceae Schmitz in Engleret Prantl 1896Genus CompsopogonOrder 2 Erythropeltidales Garbary, Hansen etScagel 1980Family Erythrotrichiaceae G. M. Smith 1933Genera Erythrotrichia, Chlidophyllon, Erythrocladia,

Pyrophyllon, SahlingiaOrder 3 Rhodochaetales Bessey 1907Family Rhodochaetaceae Schmitz in Engler etPrantl 1896Genus Rhodochaete

Class 3: Florideophyceae Cronquist 1960Multiple orders.Class 4: Porphyridiophyceae H. S. Yoon, K. M.

Muller, R. G. Sheath, F. D. Ott et D. Bhattacharya,class nov.

Rhodophyta unicellularis; chloroplasti singulariset ramosi vel stellaris cum pyrenoides; Golgi cumreticulo endoplasmatico et mitochondrion conso-ciatus; cellulae cum floridoside; reproductio adivisio cellulosa.Unicellular red algae with a single branched orstellate plastid with or without pyrenoid; Golgiassociation with mitochondria and ER; cells withfloridoside as a low molecular weight carbohy-drate; reproduction by cell division.Order Porphyridiales Kylin ex Skuja 1939Family Porphyridiaceae Skuja 1939Genera Porphyridium, Erythrolobus, Flintiella

Class 5: Rhodellophyceae Cavalier-Smith 1998

Order Rhodellales ord. nov. H. S. Yoon, K. M.Muller, R. G. Sheath, F. D. Ott et D. Bhattacharya,order nov.Rhodophyta unicelluaris; chloroplasti singulariset lobati cum pyrenoides in centro vel a centro;Golgi cum reticulo endoplasmatico et nucleusconsociatus; cum mannitol; reproductio a divisiocellulosa.

Unicellular red algae; a single highly lobed plastidwith eccentric or centric pyrenoid, Golgi associa-tion with nucleus and ER; contains mannitol; re-production by cell division.Family Rhodellaceae fam. nov. H. S. Yoon, K. M.Muller, R. G. Sheath, F. D. Ott et D. Bhattacharya,fam. nov.Characters as for orderGenera Rhodella, Dixoniella, Glaucosphaera

Class 6: Stylonematophyceae H.S. Yoon, K.M.Muller, R.G. Sheath, F.D. Ott et D. Bhattacharya,classis nov.

Rhodophyta unicelluaris, pseudofilamentosis velfilamentosis; chloroplasti cum morphologiaevariabilis et cum vel sine pyrenoides; Golgi cumreticulo endoplasmatico et mitochondrion conso-ciatus; reproductio a division cellulosa vel mono-spora.Unicellular or pseudofilamentous or filamentousred algae; various plastid morphologies with orwithout pyrenoid; Golgi association with mito-chondria and ER; reproduction by cell divisionor monospores.Order Stylonematales Drew 1956Family Stylonemataceae Drew 1956Genera Stylonema, Bangiopsis, Chroodactylon,Chroothece, Purpureofilum, Rhodosorus, Rhodospora,Rufusia

This work was supported by grants from the National ScienceFoundation awarded to D. B., K. M. M., and R. G. S. (DEB01-07754) and to D. B. (MCB 02-36631).

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DEFINING THE MAJOR LINEAGES OF RED ALGAE (RHODOPHYTA)1

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