J. Phycol. 47, 627–637 (2011) Ó 2011 Phycological Society of America DOI: 10.1111/j.1529-8817.2011.00985.x MOLECULAR PHYLOGENY OF THE UPRIGHT ERYTHROPELTIDALES (COMPSOPOGONOPHYCEAE, RHODOPHYTA): MULTIPLE CRYPTIC LINEAGES OF ERYTHROTRICHIA CARNEA1 Giuseppe C. Zuccarello2 School of Biological Sciences, Victoria University of Wellington, P.O. Box 600, Wellington, New Zealand Hwan Su Yoon, HeeJeong Kim Bigelow Laboratory for Ocean Sciences, 180 McKown Point Road, West Boothbay Harbor, Maine 04575, USA Ling Sun School of Biological Sciences, Victoria University of Wellington, P.O. Box 600, Wellington, 6140 New Zealand Susan Loiseaux de Goe¨r 11 rue des Moguerou, 29680 Roscoff, France and John A. West School of Botany, University of Melbourne, Parkville, Victoria 3010, Australia The phylogeny of morphologically simple algae is Key index words: Compsopogonophyceae; Erythro- problematic due to insufficient morphological char- peltidales; Erythrotrichia; molecular phylogeny; acters to aid in distinguishing species and relation- Porphyrostromium; Rhodophyta; taxonomy ships. The problem is further compounded because multiple evolutionary lineages of morphologically similar species occur in most well-sampled biogeo- The Erythropeltidales are commonly encountered graphic locations; therefore, location cannot be epiphytes in marine environments. The most com- used as a proxy for species. The phylogeny of the mon genera are Erythrotrichia, Erythrocladia, and Sah- upright members of the Erythropeltidales is partially lingia; other genera are less well-known or are clarified by combining molecular data, unialgal cul- geographically restricted (e.g., Porphyrostromium, Smi- ture observations, and worldwide sampling. Our thora); and other genera have only been described results show that there are several well-supported recently (Pseudoerythrocladia, Madagascaria; Zucca- lineages within the Erythropeltidales with only two rello et al. 2010). The usually small stature of these morphologically recognizable taxa at present. The algae, and their frequent co-occurrence on sub- first is the genus Porphyrostromium, with a well-devel- strates, makes their isolation into unialgal culture oped basal crust, which includes two Erythrotrichia essential for accurate observations and molecular species (Porphyrostromium ligulatum comb. nov. and analysis. The ‘‘simple’’ morphology of these algae Porphyrostromium pulvinatum comb. nov.). The sec- led to their placement in one class, the Bangiophy- ond is the branched species Erythrotrichia welwitschii ceae, with other algae of simple morphology (e.g., (Rupr.) Batters. There are also six strongly sup- see van den Hoek et al. 1995). The advent of molec- ported Erythrotrichia carnea–like lineages. While not ular studies has led to the reclassification of the completely satisfactory, we propose that one lineage Bangiophyceae into six classes and a more natural (lineage 2) with samples close to the type locality be taxonomy (Yoon et al. 2006). designated as E. carnea with a specific isolate as an The Erythropeltidales are placed in the class epitype. The lack of morphology to differentiate the Compsopogonophyceae, along with the orders Com- other lineages leads to a taxonomy based solely on psopogonales and Rhodochaetales. In addition to gene sequencing and molecular phylogeny, with rbcL molecular data, this class is supported by some ultra- sequences differentiating the lineages proposed. We structural characters (see Zuccarello et al. 2000, hold off on proposing more species and genera West et al. 2007a,b, Scott et al. 2010). The Compso- until more data and samples can be gathered. pogonophyceae is further characterized by the pres- ence of the low-molecular-weight carbohydrate floridoside, which is also found in the Florideophy- 1Received 11 July 2010. Accepted 15 November 2010. ceae and Porphyridiophyceae (Karsten et al. 1999, 2Author for correspondence: e-mail [email protected]. 2003). 627 628 GIUSEPPE C. ZUCCARELLO ET AL. The defining features of the Erythropeltidales are in stature, Membranella nitens G. Hollenb. et I. A. Ab- as follows: most species and genera have cells con- bott, has been merged into synonymy with S. naiad- taining a central plastid with a pyrenoid; pit plugs um, again based mostly on molecular characters lacking in all studied species; production of mo- (West and Zuccarello 2009). nospores by the unequal (oblique) division of vege- The remaining two more ubiquitous upright tative cells, forming what is called a lenticular cell, genera in the Erythropeltidales are Erythrotrichia and and the release of this cell as a monospore. The first Porphyrostromium. While there has been much confu- two characters are shared with the Stylonematophy- sion around the application of the names Erythrotrichia, ceae (Zuccarello et al. 2010). Even with this lack of Erythropeltis, Erythrotrichopeltis, and Porphyrostromium many defining characters, the order is well sup- (Wynne 1986, Silva et al. 1996), it appears that the ported by molecular data (Mu¨ller et al. 2001, Yoon correct names presently are Erythrotrichia and et al. 2006). Porphyrostromium. The status of the filamentous genus A sexual cycle, or some features of a sexual cycle, Porphyrostromium Trevis. is not fully resolved, with have been reported in the Compsopogonophyceae. Heerebout (1968) subsuming it into Erythrotrichia Reports of sex are unusual outside the Bangiophy- Aresch. and others not (Kornmann 1984, 1989, ceae (i.e., Bangiales) and Florideophyceae. The Brodie and Irvine 2003, Kikuchi and Shin 2011). At Rhodochaetales was first described as having an present, Porphyrostromium is considered to encompass unusual sexual cycle [in Rhodochaete pulchella Thur. several species with a crustose base (Kornmann 1984, ex Bornet (Magne 1960), as Rhodochaete parvula], 1987), while Erythrotrichia species have a more unicel- although another isolate of R. pulchella is not sexual, lular rhizoidal or discoidal holdfast. Species distinc- but only reproduces by monospores (Zuccarello tions within these two genera have also been et al. 2000). Other reports on sexuality in the controversial, with many species names considered Compsopogonophyceae are few, and evidence of a synonyms. Most characters used to distinguish the sexual cycle is often incomplete (Heerebout 1968, species have been based on substrate, width of the fil- Murray et al. 1972, Kornmann 1984, 1987, Hawkes ament (uni- vs. bi- vs. multiseriate), and attachment 1988, Magne 1990, Nelson 1993, Nelson et al. 2003, structure. Some of these species names (e.g., Erythro- Kikuchi and Shin 2011). trichia australis Levring) have been sunk into a poly- The taxonomy of the crustose members of the typic species E. carnea (Dillwyn) J. Agardh (Guiry and Erythropeltidales was recently investigated using cul- Guiry 2010). Still, little is known about the variability tured isolates and multiple molecular markers and of any of these characters in distinguishing species, wide-range sampling (Zuccarello et al. 2010). This and there has been little comparison of multiple iso- work showed that the diversity of the crustose mem- lates in controlled laboratory conditions. bers is greater than previously suspected. Crustose The Erythropeltidales, while often overlooked in members resembling the genus Erythrocladia were floras due to their small size, are found throughout found in several quite distinct molecular groups that the world. The genera Erythrocladia, Sahlingia, and warranted generic designation. Pseudoerythrocladia Erythrotrichia are especially common and often occur kornmannii J. A. West et Zuccarello was morphologi- as epiphytes on other algae. Worldwide presence of cally distinguishable from Erythrocladia irregularis small organisms may not be due to recent human- Rosenv. by its lack of pyrenoids (Scott et al. 2010), influenced dispersal events, but a characteristic of while the morphology of the genus Madagascaria their small size (e.g., large population sizes, rarity of erythrocladioides J. A. West et N. Kikuchi, a sister group extinction, high probability of dispersal) as stated by to all the other Erythropeltidales, is not easily distin- Bass-Becking (1934, p. 15) and de Wit and Bouvier guished from E. irregularis. The data also showed that (2006, p. 756), ‘‘everything is everywhere but the Porphyropsis coccinea (J. Agardh ex Aresch.) Rosenv. environment selects,’’ and recently expanded by (erect blades without pyrenoids) grouped with others especially for eukaryotes (Fenchel and Finlay the crust P. kornmannii. The data also supported the 2004, Finlay et al. 2004). In the red alga Stylonema genus Sahlingia with bifurcate marginal cells, and this alsidii (Zanardini) K. M. Drew, molecular data indi- genus seemed to be most closely related to the cate that many lineages have worldwide distribu- remaining upright genera (Zuccarello et al. 2010). tions, with some lineages hypothesized to result The upright members of the Erythropeltidales, from recent dispersals (Zuccarello et al. 2008). Also, besides Porphyropsis, have a complex taxonomic his- in E. irregularis, little genetic variation was found in tory. Several large, wide-bladed members in New samples collected from widely dispersed locations Zealand were considered species of Porphyra until (France, the Netherlands, Australia, New Zealand) molecular studies were initiated (Pyrophyllon, Chlido- (Zuccarello et al. 2010). The cause of this wide dis- phyllon; Nelson 1993, Nelson et al. 2003). Others tribution is unknown, but these data suggest that have been known