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Molecular Phylogeny of Selected Members of the Order Thalassiosirales (Bacillariophyta) and Evolution of the Fultoportula1

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Molecular Phylogeny of Selected Members of the Order Thalassiosirales (Bacillariophyta) and Evolution of the Fultoportula1 J. Phycol. 42, 121–138 (2005) r 2005 Phycological Society of America DOI: 10.1111/j.1529-8817.2005.00161.x MOLECULAR PHYLOGENY OF SELECTED MEMBERS OF THE ORDER THALASSIOSIRALES (BACILLARIOPHYTA) AND EVOLUTION OF THE FULTOPORTULA1 Irena Kaczmarska2, Margaret Beaton and Anita C. Benoit Biology Department, Mount Allison University, 63B York Street, Sackville, New Brunswick, Canada E4L 1G7 and Linda K. Medlin Alfred Wegener Institute, Am Handelshafen 12, D-27570 Bremerhaven, Germany Recent phylogenetic studies of the diatoms indi- Key index words: development; fultoportula; cate that members of the order Thalassiosirales Lithodesmiales; molecular phylogeny; morpholo- occupy an interesting position in the diatom evolu- gy; Thalassiosirales tionary tree. Despite their radial morphology and scaly auxospores, they are consistently recovered in Abbreviations: AWI, Alfred–Wegener Institute; BI, molecular analyses as a member of subdivision Ba- Bayesian Inference; BT, bootstraps; ML, Maximum cillariophytina and a sister clade to non-fultoportu- Likelihood; MP, Maximum Parsimony; MTA, late and non-radial lithodesmioids. This study Mount Allison University; NJ, Neighbor Joining; included 46 species from nine traditionally accept- PP, posterior probabilities ed extant genera, and analyzed 43 nuclear small subunit (SSU) rRNA sequences in parallel with a survey of the variation in fultoportula structure. Despite their relatively recent origins (Rothpletz Three possible scenarios leading to the evolution 1896, Kooistra and Medlin 1996), the Bacillariophyta of the fultoportula are discussed in the context of are a successful, abundant, and diverse algal group molecular and morphological similarities between found in most aquatic ecosystems. Diatoms are of great the examined Thalassiosirales and their SSU rRNA ecological importance, especially as a key contributor sister clade Lithodesmiales. We speculate that the to global carbon and silica cycling (Treguer et al. 1995, fultoportula might be derived by a modification of Mann 1999). The classical view of diatom systematics, either a cribrum in an areola (fultoportula within an inferred mainly from morphological characteristics of areola), or structures similar to marginal ridges now their siliceous cell walls, places species into one of two seen in lithodesmioids around a cluster of poroids or three classes: centric diatoms (radial and non-radial) (fultoportula in a tube), or finally, that the central and pennates (araphid or raphid) (Simonsen 1972, fultoportula may have an origin different from the 1979, Round et al. 1990). Recent molecular analyses, marginal fultoportulae. Our data confirm that ful- however, have suggested extensive reorganization of toportula-bearing diatoms constitute a natural the diatom classification system into different clades phylogenetic group. The families Thalassiosira- (Medlin and Kaczmarska 2004, Fig. 1). The first clade, ceae, Skeletonemaceae, and Stephanodiscaceae based on nuclear small subunit (SSU) rRNA, includes and the genus Thalassiosira Cleve were unexpect- only radial centric diatoms, whereas the second clade edly found to be paraphyletic. Further, Cyclotella contains two distinct subclades: bipolar centrics plus Kutz. and Stephanodiscus Ehr. may not be closely the radial Thalassiosirales and all pennate forms (Med- related and some species of these genera are more lin et al. 1993, 1996a, b). This segregation of diatom closely allied to other species of Thalassiosira. The types is supported by analyses using several genes: nu- generitype, T. nordenskioeldii, is embedded within a clear SSU rRNA (Medlin et al. 1993, 1996a, b, 2000, large poorly structured cluster of species that in- Sinninghe Damste´ et al. 2004), nuclear large subunit cludes several members of Thalassiosira, Planktoni- rRNA (So¨rhannus et al. 1995), plastid rbcLandtufA ella sol, Minidiscus trioculatus, and two members (D. G. Mann, unpublished data, Medlin et al. 1997, of Stephanodiscus. An emendment of the order respectively), mitochondrial cytochrome c oxidase I, Lithodesmiales and the family Lauderiaceae are and rpoA (Ehara et al. 2000, Fox and So¨rhannus 2003, proposed. respectively). This segregation has been recently formalized, and two new subdivisions have been proposed for these 1Received 24 October 2003. Accepted 29 September 2005. clades: Coscinodiscophytina (Clade 1) and Bacillario- 2Author for correspondence: email [email protected]. phytina (Clade 2, Medlin and Kaczmarska 2004). Cos- 121 122 I. KACZMARSKA ET AL. group’s ecological importance and rich morphology. Thalassiosira, with about 180 described marine species and at least 12 reported freshwater species (Round et al. 1990, Silva and Hasle 1994), is one of the most speciose genera within the order. The genus is recog- nized by a combination of characters rather than spe- cific diagnostic characteristics (Hasle 1972, 1973a, FIG. 1. Schematic representations of the molecular phylo- Makarova 1981, 1994), which typically include locu- geny from Medlin and Kaczmarska (2004) showing the relation- ship between the major lineages within the diatoms and their late areolae with external foramina and internal cribra, common names. marginal and central strutted processes (fultoportulae, Hasle 1972, Hasle 1973a), and the peripheral labiate processes (rimoportulae). In addition, a number of cinodiscophytina contains one class (Clade 1, radial girdle and valve face characteristics identified with centrics, except Thalassiosirales), whereas Bacillar- light microscopy (LM) and SEM may be used to cir- iophytina has been further separated into two subcla- cumscribe species within the genus (Fryxell and Hasle des: Clade 2a containing the bi(multi)polar centrics 1972, 1979a, Hasle and Fryxell 1977a, Hasle 1980, plus the radial Thalassiosirales, and Clade 2b retaining 1983). the raphid and araphid pennate diatoms (Fig. 1, and Despite the extensive volume of literature devoted Medlin et al. 1993, 1996a, b, 2000). Thus, the diatoms to many aspects of Thalassiosira biology, fultoportulae are now divided into two subdivisions (Coscino- have not been well investigated within the genus. To discophytina and Bacillariophytina) and three classes: the best of our knowledge, there has been no system- Coscinodiscophyceae, Mediophyceae, and Bacillar- atic research on the types of fultoportulae since the iophyceae (Medlin and Kaczmarska 2004). work on Lauderia annulata by Syvertsen and Hasle Members of the order Thalassiosirales, a morpho- (1982). Even the number of pores subtending this logically radial centric group, do not belong to the SSU portula has not been consistently reported in recent rRNA Clade 1 of radial centrics as might be anticipated accounts. Although there are serious logistical reasons from their valve morphology (Round et al. 1990, Med- for the lack of such knowledge, the absence of system- lin et al. 1993). Instead, members of this order have atic attention to fultoportulae is quite surprising given been consistently placed within Clade 2 together with the widespread consensus that it is a lineage-defining bi(multi)-polar centrics and pennates (Fig. 1). Within characteristic. As such, it should be considered a prime this clade, the Thalassiosirales and its sister groups the candidate for studies of the evolutionary history of Lithodesmiales and Hemiaulales (sensu Round et al. these diatoms, as suggested a decade ago (Theriot and 1990, in part) appear to be among the earliest diver- Serieyssol 1994). gences. Whereas molecular evidence strongly supports The goals of our study were twofold. First, we re- the inclusion of the Thalassiosirales with bi(multi)polar examine the phylogenetic position of Thalassiosirales diatoms, the cellular evidence is less consistent. Some within the diatoms, specifically in terms of the internal aspects of protoplast ultrastructure (e.g. arrangement architecture of the fultoportula and its relationship of the Golgi bodies) support the inclusion of Thalassio- with the valve face structures in the non-fultoportulate sirales with the non-radial centrics in Clade 2 (Schmid species from its SSU rRNA sister clade, Lithodesmi- 1987, 1989, Medlin et al. 2000). In contrast, the circu- ales–Hemiaulales. We then hypothesize about the lar shape, radially symmetric valve perforation pattern, evolutionary roots of the fultoportula in the context scaly structure, and isometric architecture of the au- of the molecular relatedness between the two sister xospores of this group are more similar to the radial lineages. Second, we investigate interspecific relation- than to the bi(multi)polar centric diatoms (von Stosch ships within selected members of Thalassiosirales. Ma- 1982, Kaczmarska et al. 2000, 2001). rine species of the genus Thalassiosira, emended by With the advent of SEM, the distinctiveness of taxa Hasle (1973a), constitute the majority of the diatoms that possess strutted processes, or fultoportulae, quick- investigated in this study. Additional strains, represent- ly became apparent (Ross and Sims 1972, Hasle ing traditionally accepted genera from the order, were 1973b). A conspicuous feature of the order Thalassio- included to recover the major lineages among the sirales (Gleser and Makarova 1986, Gleser et al. 1988), fultoportulate species and to compare them with cur- this character was used as the criterion for emending rently accepted taxonomies. Members of Stephanodiscus the family Thalassiosiraceae (Hasle 1973a, b). Present- and Cyclotella (predominantly freshwater lineages) are ly, more than 30 genera are
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