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ISSN : 1226-9999(Print)
ISSN : 2287-7851(Online)
Korean J. Environ. Biol. Vol.38 No.2 pp.278-288
DOI : https://doi.org/10.11626/KJEB.2020.38.2.278

Ultrastructure of the flagellar apparatus in Rhodomonas salina (Cryptophyceae, Cryptophyta)

Seung Won Nam, Bok Yeon Jo, Woongghi Shin1,*
Nakdonggang National Institute of Biological Resources, Sangju 37242, Republic of Korea
1Department of Biology, Chungnam National University, Daejeon 34134, Republic of Korea
*Corresponding author Woongghi Shin Tel. 042-821-6409 E-mail. shinw@cnu.ac.kr
14/05/2020 05/06/2020 08/06/2020

Abstract


Rhodomonas salina is a phototrophic marine flagellate. We examined the ultrastructure of R. salina with particular attention to the flagellar apparatus by transmission electron microscopy and compared it with that of other cryptomonads reported previously. The major components of the flagellar apparatus in R. salina were a keeled rhizostyle (Rhs), a striated fibrous root (SR), a SR-associated microtubular root (SRm), a mitochondrion-associated lamella (ML), and three types of microtubular roots (9r, 4r, and 2r). The keeled Rhs originated near the proximal end of the dorsal basal body, passed near the nucleus and dissociated at the posterior end of the cell. The SR and SRm originated between two basal bodies and laterally extended to the right side of the cell. The ML originated between two basal bodies and extended to the left side of the cell. The 9r originated between the ventral basal body and the Rhs and extended toward the anterior dorsal lobe of the cell. The 4r originated near the 9r and extended toward the dorsal lobe with the 2r, which originated between two basal bodies. Here, the flagellar apparatus in R. salina is described, and the ultrastructure of the flagellar apparatus is compared among cryptomonad species.


cryptomonad , flagellar apparatus , rhizostyle , Rhodomonas , ultrastructure

초록

    National Research Foundation of Korea
    NRF-2016R1C1B100852
    NNIBR202001103

    INTRODUCTION

    Rhodomonas is distributed worldwide, and most of the species in this genus inhabit marine or brackish environments, while some are freshwater species ( Javornický 1976;Willén et al. 1980;Klaveness 1981;Erata and Chihara 1989;Hill and Wetherbee 1989). Since the first description of Rhodomonas, this genus has been revised continuously. Butcher (1967), who considered Rhodomonas to differ in color from Cryptomonas, rejected Rhodomonas and transferred its species to the genera Cryptomonas, Hillea, and Chroomonas (Hill and Wetherbee 1989). Santore (1984) revised the cryptomonad classification based on ultrastructural characteristics, recognized four pigmented genera, namely, Cryptomonas, Chroomonas, Hemiselmis, and Pyrenomonas, and abandoned the genus Rhodomonas. Later, Hill and Wetherbee (1989) emended the genus Rhodomonas and described Pyrenomonas as a junior synonym of Rhodomonas based on ultrastructural characteristics of cellular organization and periplast details.

    In previous molecular phylogenetic studies, the genus Rhodomonas formed a clade with the genera Rhinomonas and Storeatula. Moreover, the nuclear 18S rDNA sequences of Rhodomonas species are similar to those of species in Rhinomonas and Storeatula (Marin et al. 1998;Deane et al. 2002;Hoef-Emden et al. 2002). Therefore, Rhodomonas is a polyphyletic group, and the morphological and ultrastructural characteristics that distinguish these three genera are primitive (Deane et al. 2002;Hoef-Emden et al. 2002).

    One of the useful diagnostic features to infer the phylogenetic relationships of algal groups is the flagellar apparatus. In cryptomonads, available flagellar apparatus data are very limited (Mignot et al. 1968;Lucas 1970a, 1970b;Hibberd et al. 1971;Roberts et al. 1981;Santore 1982a, 1982b;Gillott and Gibbs 1983;Roberts 1984;Hill and Wetherbee 1986;Kim and Archibald 2013;Nam et al. 2013;Nam and Shin 2016), and very few absolute configurations of the cryptomonad flagellar apparatus allow for accurate taxonomic and phylogenetic conclusions (Mignot et al. 1968;Roberts et al. 1981;Gillott and Gibbs 1983;Roberts 1984;Hill and Wetherbee 1986;Kim and Archibald 2013;Nam et al. 2013;Nam and Shin 2016). Nonetheless, Nam and Shin (2016) revealed that characteristics of the flagellar apparatus are useful for inferring phylogenetic affinities and distinguishing closely related taxa.

    In this study, the ultrastructure of the flagellar apparatus in Rhodomonas salina was described and compared with that of other cryptomonad species, particularly Rhinomonas and Storeatula species.

    MATERIALS AND METHODS

    Culture of R. salina was obtained from the National Center for Marine Algae and Microbiota, Bigelow Laboratory for Ocean Sciences, West Boothbay Harbor, Maine, 04575, U.S.A. (CCMP no. 1419), maintained in f/2 medium and exposed to a 14 : 10 h light:dark cycle at 20-22°C. For transmission electron microscopy, the cells were prefixed in a 1 : 1 mixture of 5% (V/V) glutaraldehyde in 0.2 M cacodylate at pH 7.4 and f/2 culture media for 1 h at 4°C. The glutaraldehyde-fixed cells were washed 3 times in cacodylate buffer and postfixed in 1% (W/V) OsO4 for 1 h at 4°C. After being rinsed in the same buffer, the cells were en-bloc stained with 3% (W/V) aqueous uranyl acetate for 1 h at room temperature. Dehydration, embedding and polymerization were performed following the methods of Nam et al. (2012). The polymerized blocks were thin-sectioned at a thickness of 70 nm using a PT-X instrument (RMC Products, Boeckeler Instruments, Tucson, AZ). Sections were collected onto slotted copper grids coated with 0.25% (w/ v) formvar, stained with 3% (w/v) uranyl acetate and Reynold’s lead citrate (Reynolds 1963), and examined and photographed using a JEM-1010 transmission electron microscope operated at 80 kV (JEOL, Tokyo, Japan). Images of the sections were recorded on Kodak EM Film 4489 (East-man Kodak Co., Rochester, NY) and scanned in tagged image file format using an Epson Perfection V700 Photo scanner (Epson Korea Co., Ltd., Seoul, Korea). Threedimensional reconstructions were generated via Catia V5R16 (Dassault-Aviation, Argenteuil, France).

    RESULTS

    1. General ultrastructure

    The significant organelles of R. salina are visible in Fig. 1A and B. R. salina had a single chloroplast (Fig. 1A, B). The pyrenoid was positioned slightly dorsally to the center, and thylakoids did not traverse the pyrenoidal matrix. The nucleomorph was located in an invagination of the periplastidial compartment into the pyrenoid (Fig. 1A, B). A Golgi body was positioned ventrally at the level of the gullet (Fig. 1B). R. salina possessed a fibrous plate (rim fiber) with specific cytoskeletal structures in the furrow-gullet system. The rim fiber showed a prominent striped pattern with parallel stripes (Fig. 1C, D).

    2. Ultrastructure of the flagellar apparatus

    The flagellar apparatus of R. salina was asymmetrical and extraordinarily complex and consisted of the following seven major components: rhizostyle (Rhs), striated fibrous root (SR), SR-associated microtubular root (SRm), mitochondrion- associated lamella (ML), nine-stranded microtubular root (9r), four-stranded microtubular root (4r) and two-stranded microtubular root (2r).

    The most prominent and conspicuous component of the flagellar apparatus was the Rhs. In the R. salina cell, the Rhs originated from the left side of the proximal dorsal basal body (Fig. 2A, E), passed through the ventral side of the nucleus (Fig. 2B), and finally ended at the posterior end of the nucleus (Fig. 2D). In cross-section, the Rhs comprised four microtubules with a wing-like lamellar projection (Fig. 2E, F). The wing-like lamellar projection of each rhizostylar microtubule was located on the outside of the curved Rhs (Fig. 2E, F). At the nucleus level, the outer rhizostylar microtubule did not exhibit a wing-like lamellar projection (Fig. 2F).

    The other major components of the flagellar apparatus were a SR and SRm. The SR originated between dorsal and ventral basal bodies and extended to the right (Figs. 2C, 3A, B, F, 5A). The SR was arranged perpendicular to the Rhs (Fig. 2C). The SRm originated on the left side of two basal bodies, extended to the right side between two basal bodies (Figs. 3C, D, G, 5B), and was parallel with the SR (Fig. 3D). In the longitudinal section of two basal bodies, the SRm consisted of three microtubules (Fig. 3E). At the origin point of the SRm, the SRm was connected to the ventral basal body by a distinctive striated fibrous structure (anchoring fiber (AF), Fig. 3C, G).

    An unusual component of the flagellar root system was the mitochondrion-associated lamellar root. The lamellar root originated between two basal bodies near the SR root, extended to the left side of the basal bodies at the SR level, and connected a mitochondrion and basal bodies (Fig. 3B, F). The end part of the lamellar root extended in three different directions (Fig. 3H).

    In the flagellar apparatus of R. salina, the microtubular roots were well developed and composed of three types without the Rhs and SRm: the nine-stranded microtubular root (9r), the four-stranded microtubular root (4r), and the two-stranded microtubular root (2r). The 9r originated from the ventral basal body (Fig. 4A). At this level, the 9r consisted of six microtubules (Fig. 4B), added two or three more microtubules, and quickly acquired eight (Fig. 5D) to nine microtubules (Fig. 2E). At the level of the basal body, the 9r overlapped with the Rhs (Figs. 2E, 3D, 4A, B). The 9r extended toward the dorsal side and the anterior lobe of the cell (Fig. 4C). The 4r originated on the dorsal side of the dorsal basal body on the upper side of the origin of the Rhs and formed a C shape with the 9r around the dorsal basal body (Fig. 5D). The 4r moved toward the 2r (Fig. 5D, F, G) and extended to the dorsal right side with the 2r (Fig. 5C). The 2r originated between two basal bodies (Figs. 3C, D, 5A), extended to the dorsal-right side under the gullet (Fig. 5A, B) and joined the 4r (Fig. 5C).

    Two accessory connective structures were observed between the basal bodies. One (C1) exhibited a striated pattern and was positioned diagonally between triplets of each basal body (Figs. 3A, F, 4E). The other connective structure (C2) was an electron-dense layer located on the left side of the two basal bodies (Fig. 3C, G).

    The diagrammatic reconstruction of R. salina is intended to provide an accurate reconstruction of the flagellar apparatus. However, this representation is not to scale (Fig. 6).

    DISCUSSION

    1. General ultrastructure

    The general ultrastructure of R. salina in this study was very similar to that of Rhodomonas, Rhinomonas, and Storeatula species in terms of the bilobed chloroplast, inwardly projecting pyrenoid and nucleomorph embedded in the pyrenoid (Santore 1982a;Hill and Wetherbee 1988;Kugrens et al. 1999;Nam et al. 2013). A molecular phylogeny based on nuclear and nucleomorph small subunit (SSU) rDNA sequence data suggested that Rhodomonas was grouped with Rhinomonas and Storeatula and was a polyphyletic group (Cavalier-Smith et al. 1996;Deane et al. 2002;Hoef-Emden et al. 2002;von der Heyden et al. 2004;Tanifuji et al. 2010). Therefore, the general ultrastructural characteristics of intercellular organization are not useful for distinguishing closely related genera.

    2. Ultrastructure of the flagellar apparatus

    The largest microtubular root in cryptomonad cells is the Rhs. In R. salina, the Rhs is long and keeled. A long and keeled Rhs was reported in campylomorphs of Cryptomonas paramecium (Roberts et al. 1981) and Cryptomonas pyrenoidifera (Hill 1991), Hanusia phi (Gillott and Gibbs 1983), diplomorph cells of Proteomonas sulcata (Hill and Wetherbee 1986) and Urgorri complanatus (Laza-Martínez 2012). In contrast, cryptomorphs of Cryptomonas curvata (Nam and Shin 2016) and C. pyrenoidifera (Roberts 1984;Perasso et al. 1992), Rhinomonas reticulata var. atrorosea (Nam et al. 2013), and haplomorph cells of P. sulcata (Hill and Wetherbee 1986) have a short and nonkeeled Rhs. Mignot et al. (1968) and Hill (1991) mentioned that the genera Rhodomonas and Storeatula have a keeled Rhs. These results are consistent with the results of this study. Therefore, the Rhs is an important feature that distinguishes Rhodomonas and Storeatula from Rhinomonas.

    Another conspicuous component was the SR, which was the most significant fibrous component. In most cryptomonad species, the SR always has striation patterns and exists with SRm. The striation periodicity of the SR ranges from 17 to 80 nm (35-65 nm in cryptomorphs of C. pyrenoidifera, 37-45 nm in cryptomorphs of C. curvata, 45 nm in campylomorphs of Cryptomonas paramecium, 60-80 nm in H. phi, 45-50 nm in the haplomorphs of P. sulcata, 42-46 nm in Rh. reticulata var. atrorosea and 17- 30 nm in Goniomonas avonlea) (Roberts et al. 1981;Gillott and Gibbs 1983;Roberts 1984;Hill and Wetherbee 1986;Kim and Archibald 2013;Nam et al. 2013;Nam and Shin 2016). The striation periodicity of SR in R. salina was measured as 22-30 nm. This periodicity is similar to that of a phagotrophic species, G. avonlea, and shorter than that of other phototrophic cryptomonad species. In previously reported species, the SRm consisted of three microtubules at the origin point (Nam and Shin 2016). However, the number of SR-associated microtubules increased to four or five in cryptomorphs of C. curvata and C. pyrenoidifera, G. avonlea, and Rh. reticulata var. atrorosea (Nam and Shin 2016). In R. salina, the SRm was composed of three microtubules without expansion, which was consistent with the results of Oakley and Dodge (1976). The SRm was connected to the ventral basal body by two AFs. These fibers are distinctive and unusual striated fibrous structures found only in cryptomorphs of C. curvata. However, C. curvata has only one AF (Nam and Shin 2016).

    A distinctive structure of the flagellar apparatus was the mitochondrion-associated lamellar root. Although the lamellar root is an unusual structure for phytoflagellates (Roberts et al. 1981), this root has been found in two phototrophic genera, Cryptomonas and Rhinomonas, as well as the phagotrophic genus Goniomonas. The ML of C. curvata, C. pyrenoidifera, and Rh. reticulata var. atrorosea displayed striation patterns. In R. salina, the ML was electron dense without striation patterns. One of the most remark-able features is the ML in R. salina, which is divided into three directions at the end.

    The microtubular roots of cryptomonad species vary considerably, and each microtubular root is composed of different numbers of microtubules. Nam and Shin (2016) divided these microtubular roots, except the Rhs and SRm, into two types based on origin and extension path. The dorsal roots originate near the dorsal basal body and extend in a counterclockwise direction, whereas the intermediate roots originate between two basal bodies. R. salina had three types of microtubular roots, of which the 4r and 9r were considered dorsal roots and the 2r was the intermediate root. This microtubular root composition is characteristic of C. paramecium and the diplomorph of P. sulcata (Roberts et al. 1981;Hill and Wetherbee 1986). However, in consideration of their spatial arrangement, the microtubular roots of R. salina are similar to those of diplomorphs of P. sulcata. Additionally, the genus Rhinomonas, which is closely related to the genus Rhodomonas, has one dorsal root and three intermediate roots, and there seems to be a significant difference between these two genera (Nam et al. 2013).

    In conclusion, we aimed to reveal the flagellar apparatus in R. salina and presented a three-dimensional reconstruction. The overall structure of the flagellar apparatus in R. salina was similar to that in other cryptomonads, especially the diplomorph of P. sulcata. The unique flagellar apparatus components in R. salina are the two AFs connecting the ventral basal body to the SRm and the ML dividing into three directions at the tip. To date, the flagellar apparatuses of eight phototropic species, including R. salina and a phagotrophic cryptophycean species, have been studied (Roberts et al. 1981;Gillott and Gibbs 1983;Roberts 1984;Hill and Wetherbee 1986;Kim and Archibald 2013;Nam et al. 2013;Nam and Shin 2016). In Pyrenomonadaceae, the flagellar apparatuses of the genera Rhodomonas and Rhinomonas have been described (Nam and Shin 2016). The absence of data on the flagellar apparatus in the genus Storeatula limits accurate taxonomic and phylogenetic conclusions for Pyrenomonadaceae. However, we identified many differences between Rhinomonas and Rhodomonas (Table 1).

    ACKNOWLEDGEMENTS

    This research was funded by the National Research Foundation (NRF) of Korea (NRF-2016R1C1B1008520) and the Nakdonggang National Institute of Biological Resources (NNIBR202001103).

    Figure

    KJEB-38-2-278_F1.gif

    Transmission electron micrographs of the general structure and rim fiber (RF) in Rhodomonas salina CCMP1419. A. Oblique cross-section showing the chloroplast (Cp), pyrenoid (Py), and invaginated nucleomorph (Nm). B. Cross -section at the gullet (Gu) level showing the peripheral Cp, Py, Nm, Golgi body (G), and ejectosome (Ej). C. Longitudinal section showing striated patterns of the RF. D. Cross-section of the Gu showing the RF that partially covers the Gu. VB, ventral basal body; SR, striated fibrous root. Scale bars: A=1 μm, B=0.5 μm, C-D=0.2 μm.

    KJEB-38-2-278_F2.gif

    Transmission electron micrographs of the rhizostyle (Rhs) in Rhodomonas salina CCMP1419. A-B. Serial longitudinal sections showing that the Rhs originates near the basal bodies and extends to the posterior. C. Median longitudinal section showing the Rhs arranged perpendicular to the striated fibrous root (SR). D. Section showing that the Rhs dissociates at the posterior end of the cell. E. Cross -section at the basal body level showing four rhizostylar microtubules with wing-like lamellar projections (arrowhead). F. Cross-section at the nucleus level showing that the outer rhizostylar microtubule does not have a wing-like projection. DB, dorsal basal body; DF, dorsal flagellum; Ej, ejectosome; L, lipid; N, nucleus; VB, ventral basal body; VF, ventral flagellum; 9r, nine -stranded microtubular root. Scale bars: A-B=1 μm, C=0.5 μm, D-F=0.2 μm.

    KJEB-38-2-278_F3.gif

    Transmission electron micrographs of the flagellar apparatus at the basal body level in Rhodomonas salina CCMP1419. A-D. Serial cross-sections of the basal bodies in the posterior to anterior direction showing the spatial relationships between components of the flagellar apparatus. E. Longitudinal section of two flagella showing a striated fibrous root-associated microtubular root (SRm) consisting of three microtubules. F-G. Cross-sections of basal bodies showing the striated fibrous root (SR), connecting fiber (C1) and mitochondrion- associated lamella (ML). H. Cross-section of basal bodies showing that the ML extends in three directions. AF, anchoring fiber; C2, connecting structure; DB, dorsal basal body; Mt, mitochondrion; Rhs, rhizostyle; VB, ventral basal body; 2r, two-stranded microtubular root; 9r, nine -stranded microtubular root. Scale bars: A-H=0.2 μm.

    KJEB-38-2-278_F4.gif

    Transmission electron micrographs of the nine -stranded microtubular root (9r) in Rhodomonas salina CCMP1419. A-B. Serial cross-section at the ventral basal body (VB) level showing that the 9r consists of six microtubules at the origin point. C-E. Serial longitudinal sections of two flagella showing the path of the 9r. C1, connecting fiber; DB, dorsal basal body; DF, dorsal flagellum; Rhs, rhizostyle; VF, ventral flagellum. Scale bars: A-E=0.2 μm.

    KJEB-38-2-278_F5.gif

    Transmission electron micrographs of microtubular roots in Rhodomonas salina CCMP1419. A-B. Serial cross -sections of two basal bodies showing the spatial relationships between three types of microtubular roots (2r, 4r, and 9r). C. Oblique cross-section of two basal bodies showing that the four-stranded microtubular root (4r) extends to the dorsal right side with the two-stranded microtubular root (2r). D-G. Cross-sections of microtubular roots showing that the 4r forms a C-shape with the 9r near the dorsal basal body (DB) and moves toward the 2r. DF, dorsal flagellum; Gu, gullet; SR, striated fibrous root; SRm, striated fibrous root -associated microtubular root; VB, ventral basal body; VF, ventral flagellum. Scale bars: A-G=0.2 μm.

    KJEB-38-2-278_F6.gif

    Diagrammatic reconstructions of the flagellar apparatus in Rhodomonas salina CCMP1419. Not to scale. A. Diagram showing the overall flagellar apparatus from the front. B. Diagram showing the apparatus from the right side. C. Diagram showing a planar view from above. D. Diagram showing a magnified view from above. E. Diagram showing a magnified view from the oblique left side. AF, anchoring fiber; C1, connecting fiber; C2, connecting structure; DF, dorsal flagellum; ML, mitochondrion-associated lamellar root; Rhs, rhizostyle; SR, striated fibrous root; SRm, striated fibrous root-associated microtubular root; VF, ventral flagellum; 9r, nine -stranded microtubular root; 4r, four-stranded microtubular root; 2r, two-stranded microtubular root.

    Table

    Comparison of the characteristics of flagellar apparatus components among Pyrenomonadaceae species

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    Vol. 40 No. 4 (2022.12)

    Journal Abbreviation 'Korean J. Environ. Biol.'
    Frequency quarterly
    Doi Prefix 10.11626/KJEB.
    Year of Launching 1983
    Publisher Korean Society of Environmental Biology
    Indexed/Tracked/Covered By

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