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Newly recorded species of the genus Synura (Synurophyceae) from Korea

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Abstract

Background

Species in the heterokont genus Synura are colonial and have silica scales whose ultrastructural characteristics are used for classification. We examined the ultrastructure of silica scales and molecular data (nuclear SSU rDNA and LSU rDNA, and plastid rbcL sequences) to better understand the taxonomy and phylogeny within the section Petersenianae of genus Synura. In addition, we report the first finding of newly recorded Synura species from Korea.

Results

We identified all species by examination of scale ultrastructure using scanning and transmission electron microscopy (SEM and TEM). Three newly recorded species from Korea, Synura americana, Synura conopea, and Synura truttae were described based on morphological characters, such as cell size, scale shape, scale size, keel shape, number of struts, distance between struts, degree of interconnections between struts, size of base plate pores, keel pores, base plate hole, and posterior rim. The scales of the newly recorded species, which belong to the section Petersenianae, have a well-developed keel and a characteristic number of struts on the base plate. We performed molecular phylogenetic analyses based on sequence data from three genes in 32 strains (including three outgroup species). The results provided strong statistical support that the section Petersenianae was monophyletic, and that all taxa within this section had well-developed keels and a defined number of struts on the base plate.

Conclusions

The phylogenetic tree based on sequence data of three genes was congruent with the data on scale ultrastructure. The resulting phylogenetic tree strongly supported the existence of the section Petersenianae. In addition, we propose newly recorded Synura species from Korea based on phylogenetic analyses and morphological characters: S. americana, S. conopea, and S. truttae.

Background

Ehrenberg established the genus Synura in 1834 (Ehrenber 1834), with S. uvella as the type species. Synura is the most common and widespread genus in many phytoplankton floras (Kristiansen & Preisig 2007). The species in this genus are colonial flagellates with two visible flagella and two chloroplasts, and are covered by imbricate silica scales. Several scale morphologies (apical scales, body scales, transition scales, and caudal scales) occur at different locations on the surface of the same cell. These body scales are the most important character for species identification (Kristiansen & Preisig 2007).

Early classification of Synura species using light microscopy (LM) was based largely on features such as cell size and shape, general outline of scales, and the spine or keel (Ehrenber 1834). Previous taxonomical studies of Synura have traditionally stressed the distinguishing features of these scales.

The classification of Synura species using electron microscopy (EM) is based on scale ultrastructure (Korshikov 1929; Petersen & Hansen 1956; Petersen & Hansen 1958; Fott & Ludvík 1957; Asmund 1968; Balonov & Kuzmin 1974; Péterfi & Momeu 1977; Takahashi 1967; Takahashi 1972; Takahashi 1973; Takahashi 1978; Cronberg 1989; Škaloud et al. 2012; Škaloud et al. 2013; Škaloud et al. 2014). In fact, examination of the ultrastructural features of the silica scales has revolutionized Synura taxonomy. The first classification scheme to consider scale ultrastructure suggested that the genus Synura is divided into two sections: Petersenianae and Uvellae (Petersen & Hansen 1956). Subsequent classification schemes have made additional subgeneric distinctions (Balonov & Kuzmin 1974; Péterfi & Momeu 1977; Takahashi 1967; Takahashi 1972; Takahashi 1973; Takahashi 1978; Cronberg 1989).

The first molecular analyses investigated the genetic variability in 15 individuals of Synura petersenii by comparison of nuclear internal transcribed spacer (ITS) sequences (Wee et al. 2001). Subsequent molecular analyses examined ITS sequences from 21 other individuals (Kynčlová et al. 2010). Also, phylogenetic analyses investigated about 100 S. petersenii using seven-protein gene and confirmed the high degree of cryptic, species-level diversity within this nominal species (Boo et al. 2010). A recent taxonomic assessment of observed cryptic diversity redefined the species concept within the S. petersenii morphotype and recognized six cryptic lineages as separate species: Synura americana, Synura conopea, Synura glabra, Synura macropora, Synura petersenii, and Synura truttae (Škaloud et al. 2012). Most recently, the classification of Synura described an additional four new species within the S petersenii species complex based on scale morphology and sequence data (ITS, rbcL, and cox1) (Škaloud et al. 2014).

Several researchers have studied the genus Synura from different regions in Korea by the use of EM (Kim 1997). These studies described nine species and provided very short descriptions based on scale ultrastructure (Kim 1997; Kristiansen 1990). Most recently, the first molecular multigene phylogeny of a large number of S. petersenii confirmed the high degree of cryptic, species-level diversity (Boo et al. 2010).

The purpose of the present study was to provide a better understanding of the taxonomy and molecular phylogeny within the section Petersenianae of genus Synura by analysis of the ultrastructure of the silica scales and molecular data (nuclear SSU rDNA and LSU rDNA, and plastid rbcL sequences) and to describe three species of Synura that are new to Korea.

Methods

Strains and cultures

The information and accession numbers for the 32 strains (including three outgroup species) examined in this study are in Table 1. Strains were either obtained from culture collections or collected with a 20-μm mesh plankton net (Bokyeong Co., Pusan, Korea) from small ponds in Korea. The details of the culture methods were previously published (Jo et al. 2011; Jo et al. 2013).

Table 1 List of strains used in the molecular study and GenBank accession number

Morphological investigations

For field emission scanning electron microscopy (SEM), cells were filtered using nylon membrane filters (Whatman Ltd., Maidstone, UK), rinsed in distilled water, fixed in 1% OsO4, dehydrated, and then prepared and viewed as described previously (Jo et al. 2011). Voucher specimens were stored at the Kyungpook National University Herbarium. For field emission transmission electron microscopy (TEM), cells were prepared by air drying onto formvar coated copper grids. The grids were viewed in a JEM 1010 TEM (JEOL Ltd., Tokyo, Japan) at 80 kV. Images were recorded on Kodak EM Film 4489 (Eastman Kodak Co., Rochester, NY, USA) and scanned to digital format using an Epson Perfection V700 Photo scanner (Epson Korea Co., Ltd, Seoul, Korea). The terminology used to describe scale ultrastructure follows a previous method (Škaloud et al. 2012).

DNA extraction, amplification, sequence alignment, and phylogenetic analyses

DNA extraction, PCR amplification, PCR product purification, and sequence alignment were conducted as previously described (Jo et al. 2011; Jo et al. 2013). Phylogenetic analyses were performed using a combined dataset of 5011 characters (nr SSU rDNA = 1638, nr LSU rDNA = 2548, and pt rbcL = 825) by maximum likelihood (ML) and Bayesian inference (BI). Although nuclear ITS1 and ITS2 sequences were also determined, these sequences were used to examine groups of genetically identical strains and as a barcode to identify species. The sequences of three species of Chrysophyceae (Chromulina sp., Ochromonas danica, and Ochromonas sp.) were used as outgroups to root the tree. Primer regions and ambiguously aligned regions were removed prior to phylogenetic analyses. Prior to ML analysis, the best-fit model for individual and concatenated data sets was traced under Bayesian information criterion (BIC) using Modeltest 3.7 (Posada & Crandall 1998). GTR + I + G model for all the individual and concatenated data sets was selected. We used the GTR + I + G nucleotide model as implemented in RAxML v8 (Stamatakis 2014). Bayesian analyses were run using MrBayes 3.2 (Ronquist et al. 2012) with a random starting tree and ran for 2 × 106 generations, keeping on tree every 1000 generations. The burn-in point was identified graphically by tracking the likelihoods in Tracer v.1.6 (Rambaut et al. 2013). Trees were visualized using the FigTree v.1.4.2 program (Rambaut A. FigTree v1.4.2 2014). Each analysis was conducted as previously described (Jo et al. 2011; Jo et al. 2013).

Results and discussion

Morphological characteristics

We identified all species based on scale ultrastructure from SEM and TEM. This analysis led to identification of three species that are new to Korea: S. americana, S. conopea, and S. truttae (Figs. 1, 2 and 3 and Table 2). The scales of the newly recorded species, all in the section Petersenianae, have well-developed keels and a number of struts on the base plate. The terminology used to describe the ultrastructure of these scales follows a previous method (Škaloud et al. 2012). Other studies have described newly recorded species of Synura from Korea based on morphological characters, such as cell size, scale shape, scale size, keel shape, number of struts, distance between struts, degree of interconnections between struts, size of the base plate pores, keel pores, base plate hole, and posterior rim (Škaloud et al. 2012). Two of our species (S. americana and S. conopea) are morphologically similar to S. petersenii, suggesting a close relationship. S. conopea was most similar to S. petersenii in terms of cell shape and transverse folds, although these species differ in keel reticulation. S. conopea is distinguished by its smaller scales and its large and closely arranged keel pores. S. americana is characterized by rounded scales, a near absence of transverse folds, an occasionally triangular keel, and long rear scales. S. truttae is characterized by small scale size, keel tips, large base plate hole, and short distance between struts.

Fig. 1
figure1

Morphology of the colony and scales of Synura americana (ac: SEM, d: TEM). All scale bars, 1 μm. a SEM image of colony forming cells. b Top surface of a body scale. c Bottom surface of a body scale. d TEM image of body scale

Fig. 2
figure2

Morphology of the colony and scales of Synura conopea (ac: SEM, d: TEM). All scale bars, 1 μm. a SEM image of colony forming cells. b Top surface of a body scale. c Bottom surface of a body scale. d TEM image of a body scale

Fig. 3
figure3

Morphology of the colony and scales of Synura truttae (ac: SEM, d: TEM). All scale bars, 1 μm. a SEM image of colony forming cells. b Top surface of a body scale. c Bottom surface of a body scale. d TEM image of a body scale

Table 2 Summary of the major characteristic features observable with EM used in this study to distinguish between taxa of the section Petersenianae

Taxonomic description S. americana Kynčlová and Škaloud 2012 (Fig. 1)

Reference: Škaloud et al. 2012, p. 320, Figs. 62–69.

Specimens examined: KNUJO-CM20151226.

Description: Colonies globular and 22–51 μm in diameter (Fig. 1a). Cells pyriform (22–28 × 8–12 μm) and entirely covered by rounded scales (Fig. 1a). Body scales 3.0–4.2 × 1.7–2.3 μm (Fig. 1bd). The keel often terminates at an acute tip (Fig. 1b) and is ornamented by medium-sized pores (Fig. 1d). In some cases, the keel is wider in the anterior region, giving it a triangular shape (Fig. 1b). The basal plate, ornamented by numerous small pores, is anteriorly perforated by a rounded base plate hole that is 0.08–0.27 μm in diameter (Fig. 1bd). Numerous struts (21–24) extend regularly from the keel to the edge of the scale but almost never interconnect the transverse folds (Fig. 1b and d). The spacing between struts is 0.27–0.30 μm (Fig. 1b and d).

Site of collection: Chimu, Daesan-myeon, Haman-gun, Gyeongsangnam-do, Korea (35°20′21"N, 128°25′47"E).

Date of collection: 26 Dec 2015.

Distribution: Widely distributed. Canada (Wee et al. 2001), Colombia (Cronberg 1989), Czech Republic (Škaloud et al. 2012; Kynčlová et al. 2010), Denmark (Kristiansen 1988), Germany (Kies & Berndt 1984), Korea (Boo et al. 2010, this study), North America (Kling & Kristiansen 1983; Kristiansen 1975; Wee 1981), and USA (Wee et al. 2001; Boo et al. 2010).

S. conopea Kynčlová and Škaloud 2012 (Fig. 2)

Reference: Škaloud et al. 2012, p. 324, Figs. 78–85.

Specimens examined: KNUJO-YG20160117, NIBRFL0000131748, and NIBRFL0000131749.

Description: Colonies globular and 25–47 μm in diameter (Fig. 2a). Cells pyriform (20–28 × 8–12 μm) and entirely covered by lanceolate scales (Fig. 2a). Body scales 3.3–4.1 × 1.4–1.9 μm (Fig. 2bd). The keel terminates at an acute tip (Fig. 2b) and is usually broadened apically and ornamented by medium to large-sized pores (Fig. 2d). The basal plate, ornamented by numerous medium-sized pores, is anteriorly perforated by a round to oblong base plate hole that is 0.19–0.32 μm in diameter (Fig. 2bd). Numerous struts (24–30) extend regularly from the keel to the edge of the scale but are usually not interconnected by transverse folds (Fig. 2b and d). The spacing between struts is 0.23–0.26 μm (Fig. 2b and d).

Site of collection: Yongji, Yongchon-ri, Toseong-myeon, Goseong-gun, Gangwon-do, Korea (38°13′43"N, 128°33′49"E).

Date of collection: 17 Jan 2016.

Distribution: Widely distributed. Argentina (Vigna & Munari 2001), Brazil (Couté & Franceschini 1988), Czech Republic (Škaloud et al. 2012; Kynčlová et al. 2010), Greenland (Jacobsen 1985), Ireland (Řezáčová & Škaloud 2005), Japan (Boo et al. 2010), and Korea (Boo et al. 2010, this study).

S. truttae (Siver 1987) Škaloud and Kynčlová 2012 (Fig. 3)

Basionym: S. petersenii f. truttae (Siver 1987), p. 111, Figs. 12–14.

Reference: Škaloud et al. 2012, p. 318, Figs. 52–61.

Specimens examined: KNUJO-HJ20151222.

Description: Colonies globular and 35–48 μm in diameter (Fig. 3a). Cells pyriform (22–31 × 11–13 μm) and entirely covered by lanceolate scales (Fig. 3a). Body scales elongated and 3.3–3.8 × 1.5–1.8 μm (Fig. 3ad). The keel of the body scales has no apparent tip or a much reduced tip and is ornamented by small pores (Fig. 3b). The keel tip frequently has several (two to four) very short teeth on its top (Fig. 3d) and is covered by a number of small bumps. The basal plate, ornamented by numerous small pores, is anteriorly perforated by a large, round to oblong base plate hole that is 0.32–0.56 μm in diameter (Fig. 3bd). Numerous struts (27–33), which are often interconnected, regularly extend from the keel to the edge of the scale (Fig. 3b and d). Scales with nearly absent transverse folds (Fig. 3bd). The spacing between struts is 0.19–0.24 μm (Fig. 3b and d).

Site of collection: Hanjeong, Girin-ri, Soseong-myeon, Jeongeup-si, Jeollabuk-do, Korea (35°33′55"N, 126°46′30"E).

Date of collection: 22 Dec 2015.

Distribution: Widely distributed. Czech Republic (Škaloud et al. 2012; Kynčlová et al. 2010), Korea (This study), and USA (Siver 1987; Siver & Wujek 1993; Siver & Lott 2004).

Molecular data

The 5011 nucleotides of the combined data set (nuclear SSU and LSU rDNA, and plastid rbcL) were determined for 32 strains (Table 1). Although the nuclear ITS1, 5.8S, and ITS2 sequences were also determined, these sequences were only used for to confirm identification, not to assess phylogenetic relationships. The combined sequences had 5011 nucleotides, 4039 variable sites, and 725 parsimoniously informative sites. The molecular data contained 12 new sequences (3 new nr SSU rDNA sequences, 3 new nr LSU rDNA sequences, 3 new nr ITS sequences, and 3 new pt rbcL sequences) and 102 published sequences (29 nr SSU rDNA sequences, 20 nr LSU rDNA sequences, 25 nr ITS sequences, and 28 pt rbcL sequences).

Phylogenetic analyses

We analyzed nr SSU and LSU rDNA, and pt rbcL sequences from 32 strains (including three outgroup species). The phylogenetic tree based on the Bayesian analysis was rooted with three species of Chromulinaceae serving as outgroups. The Bayesian and ML analyses recovered a tree with identical topologies (Fig. 4). The phylogenetic tree consisted of species of the section Petersenianae, each of which has a well-developed keel and a number of struts on the base plate. The section Petersenianae formed a strongly supported monophyletic lineage (pp = 1.00 and ML = 100). The single strain of Synura macracantha diverged at the base of the tree, followed by Synura bjoerkii and Synura asmundiae. The single strain of S. bjoerkii was closely related to S. asmundiae, which included two strains (pp = 1.00 and ML = 100). Synura glabra formed a sister group with S. americana, S. conopea, S. petersenii, and S. truttae (pp = 1.00 and ML = 100), and S. americana and S. petersenii diverged at the next S. glabra. The five strains of S. petersenii formed a strongly supported monophyletic lineage (pp = 1.00 and ML = 100) and was a sister group to the five strains of S. americana, which included KNUJO-CM20151226 (pp = 1.00 and ML = 92). The five strains of S. americana were monophyletic group (pp = 1.00 and ML = 95), and the intraspecific similarity based on nuclear ITS rDNA sequence data ranged from 99.9% to 100.0%. The five strains of S. truttae (including KNUJO-HJ20151222) were a sister group to the five strains of S. conopea, which included KNUJO-YG20160117 (pp = 1.00 and ML = 94). The five strains of S. conopea formed a monophyletic lineage with strong support values (pp = 1.00 and ML = 100), and the intraspecific similarity based on nuclear ITS rDNA sequence data ranged from 98.5% to 100.0%. The five strains of S. truttae formed a monophyletic lineage with strong support values (pp = 1.00 and ML = 100), and the intraspecific similarity based on nuclear ITS rDNA sequence data was 100.0%.

Fig. 4
figure4

Consensus Bayesian tree of the genus Synura based on a combined nuclear SSU and LSU rDNA, and plastid rbcL sequences data. Bayesian posterior probability (pp) and maximum-likelihood (ML) bootstrap values are shown above or below the branches. The bold branches indicate strongly supported values (pp = 1.00 and ML = 100). Scale bar, 0.01 substitutions/site

Conclusions

In summary, we used molecular analysis of three genes and data on the scale ultrastructure to investigate the phylogenetic relationships within Synura, with a focus on the section Petersenianae. The phylogenetic tree based on a combined dataset was well congruent with the ultrastructural characteristics of scales. The phylogenetic tree was comprised of members of the section Petersenianae. The section Petersenianae was monophyletic with strong support values and characterized by a well-developed keel and a number of struts on the base plate. In addition, our morphological observations and molecular analyses confirmed unambiguously that this is the first report of S. americana, S. conopea, and S. truttae in Korea.

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Funding

This work was supported by a grant from the National Institute of Biological Resources (NIBR) funded by the Ministry of Environment (MOE) of the Republic of Korea (NIBR201501209).

Availability of data and materials

The sequence data from this study were deposited in GenBank with the accession codes KX610938-KX610949.

Authors’ contributions

Both authors read and approved the final manuscript.

Competing interests

The authors declare that they have no competing interests.

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Correspondence to Han Soon Kim.

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Keywords

  • Synura americana
  • S. conopea
  • S. truttae
  • Morphology
  • Ultrastructure
  • Scale
  • Molecular phylogeny
  • Taxonomy