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Quadricoccopsis Gen. Nov., a New Genus of Quadricoccus-Like

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Quadricoccopsis Gen. Nov., a New Genus of Quadricoccus-Like Fottea, Olomouc, 18(2): 189–199, 2018 189 DOI: 10.5507/fot.2018.005 Quadricoccopsis gen. nov., a new genus of Quadricoccus–like algae in Oocystaceae from China (Trebouxiophyceae, Chlorophyta) Xudong Liua,b, Huan Zhua, Huiyin Songa,b, Benwen Liua,b, Qinghua Wanga,b, Guoxiang Liua* & Zhengyu Huc a Key Laboratory of Algal Biology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, P.R China; *Corresponding author e–mail: [email protected] b University of Chinese Academy of Sciences, Beijing 100049, P.R China c State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, China Abstract: Members of Quadricoccus–like algae are characterized by oval to ellipsoid cells adherent to the bowl–shaped or stretched, empty mother cell walls and are common in phytoplankton of inland waters. To date, the morphologically similar genera Quadricoccus and Lobocystis are accepted for this group and the former had been phylogenetic positioned in Oocystaceae. In this study, seven strains of Quadricoccus–like algae were identified and successfully cultured in the laboratory. Light and electron microscope observations and phylo- genetic analysis revealed that the strains represent three different species within a new genus, described here as Quadricoccopsis gen. nov. It differed from genus Quadricoccus by characteristically cell adherent mode that two pairs of daughter cells connected to the mother cell remnant respectively by the pole and median portion and distinguished from Lobocystis by variable 2–4–8 autospores, characteristically cell adherent mode and only found in limnetic water. The three new species, described here as Q. simplex, Q. parva and Q. glomerata, differed in cell size, colony morphology and autospore number. Phylogenetic analysis revealed the genus Quadricoccopsis in Oocystaceae and a close relationship with Oocystidium, which is far away from the phylogenetic position of Quadricoccus in one of the granulated clades. The Quadricoccus–like algae were, therefore, proved to be a para- phyly. Furthermore, apart from Planctonema–like algae, the Oocystaceae characteristic cell wall ultrastructure, which is multi–layered with cellulose fibrils in each layer perpendicular to those of the adjoining layer, is not shown again in genus Quadricoccopsis. Different cell wall substructures may be related to the colony formation mechanism. Whether the ultrastructure criterion is applied to all the Oocystaceae needs to be re–evaluated and, further, the definition of this family should be discussed. Key words: Cell wall ultrastructure, Oocystaceae, Quadricoccopsis simplex, Quadricoccopsis parva, Quadricoccopsis glomerata, Quadricoccus INTRODUCTION and Dimorphococcus Braun. Komárek & Fott (1983) placed the genera Quadricoccus, Lobocystis, Members of Quadricoccus–like algae are characterized Dictyosphaerium, Dichotomococcus and two different by oval to ellipsoid cells adherent to the bowl–shaped or genera Dactylosphaerium Steinecke and Dimorphococcopsis stretched empty mother cell walls by either the median Jao into the subfamily Dictyospaerioideae. They were or end portion (Komárek & Fott 1983), which repre- all characteristically distinguished by mother cell wall sent a common morphotype of coccoid green algae in remnant connections in colony formation. Among them, phytoplankton of inland waters. The remnants of mother members in genus Quadricoccus and genus Lobocystis cell walls develop a system of stems connecting the share a similar oval to cylindrical cell shape and thus individual cells to colonies and thus play a vital role were often confused by previous researchers (Hindák in such morphotype. They were included in the genus 1977; Komárek & Fott 1983). Quadricoccus Fott and Lobocystis Thompson up to now. The genus Quadricoccus was first erected by According to Thompson (1952), the Quadricoccus– Fott in 1948 with type species Q. verrucosus Fott. like members resembled those grouped in the genera Then, another 3 species were described based on smooth Dictyosphaerium Nägeli, Dichotomococcus Korshikov (Q. laevis Fott and Q. ellipticus Hortob) or warty (Q. 190 Liu et al.: Quadricoccopsis gen. nov., a new genus of Quadricoccus–like algae verrucosus and Q. ovalis Hindák) cell walls and the still on the type species of genus Lobocystis, a formal adherent portion of the daughter cells on the empty wall taxonomic emendment of the genus was not made by of the mother cell (Q. verrucosus and Q. laevis adhere by either Hindák or Comas & Perez. Therefore, the mean- the ends whereas Q. ellipticus and Q. ovalis adhere by ing of Fott (1975) is still accepted (Comas & Perez the median portion). However, the surface incrustations 2002). Subsequently, apart from the type species, four on the warty species (Q. verrucosus and Q. ovalis) were extra recognisable species were proposed into Lobocystis always considered doubtful (Williams 1967; Hindák (Izaguirre 1991; Comas & Perez 2002; Stoyneva 1977; Hindák 1984; Hindák 1988; Krienitz & Bock 2008; Fanés et al. 2009). The phylogenetic position of 2011). According to the observation of Q. ovalis by Lobocystis has not been studied up to now. Hindák (1984), the granulation density on the cell wall In this study, seven strains, which share a varied considerably in both the vegetative cells and the similar morphology with the genera Quadricoccus and empty cell walls: from smooth walls without conspicu- Lobocystis, were collected in China. Morphological ous granules to warty walls with dense granulation along and phylogenetic analyses identified these strains to the entire surface. Hindák further speculated that the be a new genus, Quadricoccopsis gen. nov., with three intensity of granulation on Q. ovalis was obviously different new species. dependent on the chemistry of water in his later study (Hindák 1988). Though the dispute had always existed, all the species were accepted by most researchers. In Material and Methods 1998, a new species, Q. euryhalinicus Kuylenstierna, was proposed for characteristically having typically two Quadricoccopsis simplex samples (strain LXD53) were collected autospores attached at each end of a tubular mother cell from the Yingze Lake in Yingze Park (37°51’N, 112°33’E, alt. 792 m, Taiyuan, Shanxi Province, China, in Aug. 2015). wall (Kuylenstierna & Karlson 1998). Up to now, Three strains of Quadricoccopsis parva were respectively five species have been accepted based on the Algaebase sampled in a fish pond (strain LXD126, 25°42'N, 115°36'E, alt. (Guiry & Guiry 2017). Recent studies by Krienitz & 161 m, Huichang, Jiangxi Province, China, in Feb. 2017), an Bock (2011) and Štenclová et al. (2017) positioned the artificial pond in a botanical garden (strain LXD135, 21°55'N, genus Quadricoccus in Oocystaceae (Trebouxiophyceae) 101°15'E, alt. 546, Jinghong, Yunnan Province, China, in Apr. as a sister to the genus Amphikrikos Korshikov. 2017) and an artificial pond at the roadside (strain LXD143, The genus Lobocystis, erected by Thompson in 31°6'N, 115°42'E, alt. 348, Luotian, Hubei Province, China, 1952 with original type species Lobocystis dichotoma, in Aug. 2017). Three Quadricoccopsis glomerata were strain LXD117 (collected from the same fish pond with strain LXD126, shared a similar morphology with Quadricoccus, especially 25°42’N, 115°36’E, alt. 161 m, Huichang, Jiangxi Province, with the two–celled groups of Q. ellipticus (Hindák 1977; China, in Feb. 2017), strain LXD134 (collected from the same Comas & Perez 2002). Later, Fott (1975) pointed the artificial pond with strain LXD135, 21°55'N, 101°15'E, alt. 546, L.dichotoma was identical with Dictyosphaerium planc- Jinghong, Yunnan Province, China, in Apr. 2017) and strain tonicum Tiffany et Ahlstrom and proposed the combined LXD144 (collected from a fish pond at the roadside, 30°55'N, type species Lobocystis planctonica (Tiffany et Ahlstrom) 115°31'E, alt. 120, Luotian, Hubei Province, China, in Aug. Fott. However, Hindák considered the Dictyosphaerium 2017). Two additional Oocystaceae samples were identified planctonicum and Lobocystis dichotoma var. mucosa and sequenced herein for phylogenetic analysis. Samples were isolated into a single colony using the serial Bourrelly could not be included in Lobocystis since the dilution pipetting technique (Hoshaw & Rosowski 1973) and daughter cells did not remain enclosed in the mother cell maintained in liquid BG11 medium (Stanier et al. 1971) with wall (Hindák 1977) Later, Hindák proposed a possible a constant light source of 30–50 μmol.m–2.s–1 and a temperature generic feature of Lobocystis that reproduction by only 2 of 25 °C. Photomicrographs were taken on an Olympus BX53 autospores (Hindák 1988). Then, Comas & Perez (2002) light microscope (Olympus Corp., Tokyo, Japan) equipped supported this point and supplemented the demarcation with an Olympus BX53 camera. For transmission electron of Lobocystis by basically formed by bi–celled groups microscopy (TEM), cells were fixed in 3% glutaraldehyde in 0.1 M cacodylate buffer and fixed in 1% aqueous OsO in 0.1 enclosed in the mother cell wall and cells with 1–2 4 M cacodylate buffer, dehydrated in acetone and embedded large parietal pyrenoid–bearing chloroplasts. Hindák in Spurr’s resin. Ultrathin sections were stained with uranyl (1977) implied that these two species might belong to acetate and lead citrate (Reynolds 1963). The induction of Quadricoccus. However, Komárek & Fott (1983) con- zoospores and gametes was performed by flooding and light sidered that
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