realDB: A Genome Database for Red Algae


Phylogeny

Figure 1. The evolutioanry place of red algae (Rhodophyta) in the green plant lineage.


Figure 2. Maximum likelihood (ML) phylogeny of the red algae using the combined plastid protein sequences of psaA and rbcL.
Reference: Seckbach J, Chapman DJ. Red algae in the genomic age: Cellular Origin, Life in Extreme Habitats and Astrobiology. 2010. Springer. ISBN-13: 978-9048137947.

Characteristics

Table 1. The seven classes and all recognized genera of the Rhodophyta (excluding Florideophyceae) and some of their diagnostic characters.

Class   Genus    Golgi association    Low-molecular-weight carbohydrate (LMWC)    Other characters
Cyanidiophyceae Cyanidium ER
Cyanidioschyzon
Galdieria ER
Bangiophyceae Bangia Floridoside, isofloridoside
Bangiadulcis
Dione
Minerva
Porphyra Floridoside, isofloridoside
Pseudobangia
Florideophyceae Hundreds of genera
Compsopogonophyceae  Compsopogon ER Floridoside
Boldia ER
Chlidophyllon
Erythrocladia Floridoside
Erythropeltis
Erythrotrichia Floridoside
Membranella
Porphyropsis Floridoside
Porphyrostromium
Pulvinaster ER Floridoside
Pyrophyllon
Rhodochate Floridoside, digeneaside
Sahlingia Floridoside
Smithora Floridoside, isofloridoside
Porphyridiophyceae Porphyridium ER/M Floridoside
Erythrolobus
Flintiella ER/M Floridoside Intron (1,219/psaA)
Rhodellophyceae Rhodella ER Mannitol Intron (91/psaA)
Dixoniella Nu Mannitol
Glaucosphaera Nu Mannitol
Stylonematophyceae Stylonema ER Sorbitol, digeneaside Intron (229/psaA)
Bangiopsis ER Sorbitol, digeneaside Intron (229/psaA)
Chroodactylon Sorbitol Intron (229/psaA)
Chroothece Intron (229/psaA)
Colacodictyon
Empselium
Goniotrichopsis
Kylinella
Neevea
Purpureofilum ER Sorbitol, digeneaside Intron (229/psaA)
Rhodaphanes ER Sorbitol, digeneaside, threhalose
Rhodosorus Sorbitol, digeneaside Intron (229/psaA)
Rhodospora Sorbitol, dulcitol Intron (229/psaA)
Rufusia Floridoside Intron (229/psaA)

ER = endoplasmic reticulum; ER/M = ER-mitochondrion association; Nu = nucleus.

Reference: Seckbach J, Chapman DJ. Red algae in the genomic age: Cellular Origin, Life in Extreme Habitats and Astrobiology. 2010. Springer. ISBN-13: 978-9048137947.


Table 2. Classes of Rhodophyta showing evolution of key characteristics.

Class    Unicellular (U) or multicellular (M)   Asexual spores   Sexual reproduction   Complex life histories   Pit plugs
Cyanidiophyceae U
Porphyridiophyceae U
Rhodellophyceae U
Compsopogonophyceae M Present Present
Stylonematophyceae M Present Present
Bangiophyceae M Present Present Present Present
Florideophyceae M Present Present Present Present

Reference: Seckbach J, Chapman DJ. Red algae in the genomic age: Cellular Origin, Life in Extreme Habitats and Astrobiology. 2010. Springer. ISBN-13: 978-9048137947.

Bangiophyceae

     Bangiophyceae is a group of red algae that has simple unbranched filaments or a leaf-shaped thallus.

     The monophyly of the Bangiophyceae is supported by most molecular phylogenetic studies (Oliveira and Bhattacharya, 2000; Müller et al., 2001; Broom et al., 2004; Yoon et al., 2006).

     The Bangiophyceae grows in both marine and freshwater habitats.

     A biphasic life cycle is common in the group that includes macroscopic gametophyte and microscopic conchocelis phases.

     The monophyly of the Bangiophyceae and Florideophyceae is supported by morphological as well as molecular data (see below). Bangiomorpha and Porphyra fossils are found in deposits of ages 1,200 Ma and 600 Ma, respectively (see above, Butterfield et al., 1988; Xiao et al., 1998; Butterfield, 2000).

     The Bangiophyceae includes one order Bangiales, one family Bangiaceae, and six genera Bangia, Bangiadulcis, Dione, Minerva, Porphyra, and Pseudobangia. Around 130 species are reported from the six genera, but the majority of species belong to Bangia (10 sp.) and Porphyra (117 sp.; http://www.algaebase.org/). Broom et al. (2004) collected 123 samples of Bangia, which had been recognized as ten species and reported significant hidden genetic diversity within this genus. Continuing efforts have erected the monotypic genera Bangiadulcis, Dione, Minerva, and Pseudobangia (Müller et al., 2005; Nelson et al., 2005; Nelson, 2007). However, it is obvious that a comprehensive taxonomic study is required for this group as well to uncover their “real” diversity.

Reference Publication(s)

     Seckbach J, Chapman DJ. Red algae in the genomic age: Cellular Origin, Life in Extreme Habitats and Astrobiology. 2010. Springer. ISBN-13: 978-9048137947

The sequenced species in this class:

1. Pyropia yezoensis

2. Porphyra umbilicalis

3. Porphyra purpurea

4. Calliarthron tuberculosum

Compsopogonophyceae

     The Compsopogonophyceae consists of one freshwater order Compsopogonales with two families Boldiaceae and Compsopogonaceae, and two marine orders Erythropeltidales and Rhodochaetales. Fourteen genera have been reported in this class (Compsopogon,Boldia, Chlidophyllon, Erythrocladia, Erythropeltis, Erythrotrichia, Membranella, Porphyropsis, Porphyrostromium, Pulvinaster, Pyrophyllon, Rhodochaete, Sahlingia,Smithora).

     All of these species are multicellular; Erythrotrichia is filamentous, Smithora and Chlidophyllon are parenchymatous blades, and Boldia is a single-cell-thick tubular form that is 20–75 cm in length.

     The monophyly of this group is supported by nuclear SSU rDNA and a plastid multigene analysis that show a sister relationship of Erythropeltidales and Rhodochaetales (Rintoul et al., 1999; Zuccarello et al., 2000; Müller, et al., 2001; Yoon et al., 2002b, 2006). This recently established class (Saunders and Hommersand, 2004) is characterized by having a Golgi–ER association, and floridoside as the low-molecular-weight carbohydrates (LMWC); Broadwater and Scott, 1994; Karsten et al., 2003). This class is also the only group outside the Bangiophyceae and Florideophyceae in which sex (a complete life cycle or putative sexual structures) has been well documented (Magne, 1960, 1990) or proposed (Hawkes, 1988; Nelson et al.,2003). The divergence of this class parallel to the Bangiophyceae/ Florideophyceae clade indicates that sex was established in the Rhodophyta before the putative fossil evidence provided by Bangiomorpha.

Reference Publication(s)

     Seckbach J, Chapman DJ. Red algae in the genomic age: Cellular Origin, Life in Extreme Habitats and Astrobiology. 2010. Springer. ISBN-13: 978-9048137947

The sequenced species in this class:

1. Compsopogon coeruleus

2. Madagascaria erythrocladiodes

Cyanidiophyceae

     The Cyanidiophyceae is an asexual, unicellular red algal class that belongs to the subphylum Cyanidiophytina.

     These taxa thrive in acidic and high temperature conditions around hot springs or acidic sulfur fumes (Pinto et al., 2003).

     The Golgi apparatus in these species associates with the ER.

     The Cyanidiophyceae is a well-supported monophyletic group that diverged earliest within red algae around 1,370 Ma prior to the chromalveolate red algal secondary endosymbiosis (i.e., according to Yoon et al., 2004).

     Traditionally, the Cyanidiophyceae was classified into one order Cyanidiales, two families Cyanidiaceae and Galdieriaceae, and three genera Cyanidium (1 sp.), Cyanidioschyzon (1 sp.), and Galdieria (5 spp.). Because of their simple morphology, only seven species are recognized to date (Merola et al., 1981; Sentsova, 1991; Ott and Seckbach, 1994; Albertano et al., 2000; Pinto et al., 2003, 2007). It is, however, now clear that the diversity of the Cyanidiophyceae was underestimated. Ciniglia et al. (2004) used an environ- mental PCR survey to find the hidden biodiversity among Cyanidiophyceae and suggested six putative family-level taxa within the cyanidiophycean lineage; the Galdieria lineage (as Galdieria-A), the endolithic Galdieria (Galdieria-B), the meso- philic Cyanidium lineage, the Cyanidium lineage, the Cyanidioschyzon lineage, and the G. maxima lineage (Fig. 2), which is essentially consistent with other molecular phylogenetic studies (Gross et al. 2001; Yoon et al., 2002a, 2006; Pinto et al., 2003). For example, the endolithic Galdieria-B was recently established as the new species Galdieria phlegrea by Pinto et al. (2007). On the basis of molecular phylogenetic analyses (Ciniglia et al., 2004), they conducted additional ecophysiological studies to characterize this new species. G. maxima and Cyanidioschyzon merolae showed a close sister group relationship; however, G. maxima is very different from C. merolae with regard to many morphological features (e.g., spherical vs. ellipsoidal cell shape, thick cell wall vs. lack of cell wall, facultative heterotroph vs. obligate autotroph, endospore vs. binary fission).

     It is clear that the current taxonomic scheme does not reflect the underlying phylogenetic relationships. Therefore, there needs to be a thorough revision of the classification system of the Cyanidiophyceae at the higher level (i.e., family level) as well as a comprehensive sampling of potentially new taxa (e.g., environmental PCR survey) to characterize the hidden biodiversity in this group.

Reference Publication(s)

     Seckbach J, Chapman DJ. Red algae in the genomic age: Cellular Origin, Life in Extreme Habitats and Astrobiology. 2010. Springer. ISBN-13: 978-9048137947

The sequenced species in this class:

1. Cyanidioschyzon merolae

2. Galdieria sulphuraria

3. Galdieria phlegrea

Florideophyceae

     The monophyly of the Bangiophyceae and Florideophyceae is supported not only by molecular analyses but also by features of the reproductive cells, the association of the Golgi apparatus with ER/mitochondria, the presence of pit connections, and the presence of group I introns (Gabrielson et al., 1985, 1990; Freshwater et al., 1994; Ragan et al., 1994; Oliveira and Bhattacharya, 2000; Müller et al., 2001; Yoon et al., 2002b, 2004, 2006).

     Regarding, the close relationship between Bangiophyceae and Florideophyceae, Saunders and Hommersand (2004) suggested the subphylum Eurhodophytina to include these taxa.

     The class Floridiophyceae appears to have diverged from an ancestor of bangiophycean and florideophycean alga around 800 Ma (Yoon et al., 2004) and is the most taxonomically diverse of all red algal groups, including around 5,800 species.

     The Florideophyceae is one of the most successful algal groups in marine environments, perhaps because of their specialized life cycles (e.g., triphasic life cycle; gametophyte, carposporophyte, and tetrasporophyte phases).

     These red algae possess unique and distinctive female reproductive structures that are often used as taxonomic markers with respect to postzygotic development.

     On the basis of morphological and molecular phylogenetic data (Pueschel and Cole, 1982; Maggs and Pueschel, 1989; Harper and Saunders, 2002; Huisman et al., 2003; Saunders et al., 2004), the Florideophyceae is classified into four subclasses Hildenbrandiophycidae, Nemaliophycidae, Ahnfeltiophycidae, and Rhodymeniophycidae. Although internal relationships within these groups are still unclear, the four subclass system provides an overall view of florideophycean classification. For a detailed review of the Florideophyceae, see Saunders and Hommersand (2004).

Reference Publication(s)

     Seckbach J, Chapman DJ. Red algae in the genomic age: Cellular Origin, Life in Extreme Habitats and Astrobiology. 2010. Springer. ISBN-13: 978-9048137947

The sequenced species in this class:

1. Chondrus crispus

2. Gracilaria lemaneiformis

3. Ceramium kondoi

4. Heterosiphonia pulchra

5. Symphyocladia latiuscul

6. Neosiphonia japonica

7. Dumontia simplex

8. Mazzaella japonica

9. Ahnfeltiopsis flabelliformis

10. Eucheuma denticulatum

11. Betaphycus philippinensis

12. Kappaphycus alvarezii

13. Gracilaria vermiculophylla

14. Gracilaria chouae

15. Gracilaria blodgettii

16. Grateloupia livida

17. Grateloupia turuturu

18. Grateloupia catenata

19. Grateloupia filicina

20. Gloiopeltis furcata

Porphyridiophyceae

     The Porphyridiophyceae includes one order Porphyridiales, one family Porphyridiaceae, and three unicellular genera, Erythrolobus, Flintiella, and Porphyridium.

     This unicellular red algal group contains a single branched or stellate plastid with the presence of a group II intron (genic position 1219) in the plastid-encoded psaA gene from Flintiella.

     It was reported that Flintiella and Porphyridium have a Golgi association with ER/mitochondria (Scott et al., 1992) and possess floridoside as a LMWC (Karsten et al., 2003).

Reference Publication(s)

     Seckbach J, Chapman DJ. Red algae in the genomic age: Cellular Origin, Life in Extreme Habitats and Astrobiology. 2010. Springer. ISBN-13: 978-9048137947

The sequenced species in this class:

1. Porphyridium cruentum

2. Porphyridium purpureum

3. Porphyridium aerugineum

4. Timspurckia oligopyrenoides

5. Erythrolobus australicus

6. Erythrolobus madagascarensis

Rhodellophyceae

     The class Rhodellophyceae was proposed by Cavalier-Smith (1998) and modified/ retained by Saunders and Hommersand (2004); however, both definitions were not natural. Yoon et al. (2006) have revised the class as a group that includes unicellular red algae, Dixoniella grisea, Glaucosphaera vacuolata, Rhodella violacea, and R. maculata.

     The monophyly of the Rhodellophyceae is supported by multigene (Yoon et al., 2006) and 18S rDNA trees (Müller et al., 2001). This group contains mannitol as a LMWC (Karsten et al., 2003).

     Within the lineage, D. grisea and G. vacuolata are separated from two Rhodella species.

     Ultrastructural characters support the relationship between Dixoniella and Glaucosphaera, which have a Golgi-Nuclear association with the presence of peripheral thylakoids, whereas Rhodella has a Golgi–ER association with the absence of peripheral thylakoids (Scott et al., 1992). Furthermore, group II introns were found at genic position 91 in the psaA gene only in two Rhodella species (R. violacea, R. maculata). Therefore, it may be possible to classify the two groups into separate orders or families. Additional work may show that more genera or families need to be established to encompass this diversity.

Reference Publication(s)

     Seckbach J, Chapman DJ. Red algae in the genomic age: Cellular Origin, Life in Extreme Habitats and Astrobiology. 2010. Springer. ISBN-13: 978-9048137947

The sequenced species in this class:

Rhodella maculata

Stylonematophyceae

      The Stylonematophyceae was proposed by Yoon et al. (2006) based on multigene phylogenetic analyses. This class includes pseudofilamentous or unicelluar taxa with thick mucilaginous walls and cells lacking pit plugs.

      With the single order Stylonematales, the single family Stylonemataceae contains 14 genera (Bangiopsis, Chroodactylon, Chroothece, Colacodictyon, Empselium, Goniotrichopsis, Kylinella, Neevea, Purpureofilum, Rhodaphanes, Rhodosorus, Rhodospora, Rufusia, and Stylonema) that have been reported mostly from marine habitats.

      Most genera have cells with a single stellate plastid with a pyrenoid. A Golgi–ER association with digeneaside and sorbitol as a LMWCs are diagnostic characters for this group (Broadwater and Scott, 1994; Karsten et al., 2003), although digeneaside is missing in Chroodactylon and dulcitol is present in Rhodospora. A group II intron was found at genic position 229 in the psaA gene from most of the species. Recently, West and colleagues isolated two new genera Rhodaphanes and Purpureofilum belonging to this class (West et al., 2005, 2007).

     Most of the pseudofilamentous species in this group are found as epiphytes, and it is expected that new taxa will continue to be discovered.

Reference Publication(s)

     Seckbach J, Chapman DJ. Red algae in the genomic age: Cellular Origin, Life in Extreme Habitats and Astrobiology. 2010. Springer. ISBN-13: 978-9048137947

The sequenced species in this class:

Rhodosorus marinus