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Morphological, Biochemical, and Phylogenetic Assessments of Eight Botryococcus Terribilis Strains Collected from Freshwaters of Transylvania

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Morphological, Biochemical, and Phylogenetic Assessments of Eight Botryococcus Terribilis Strains Collected from Freshwaters of Transylvania J Appl Phycol (2015) 27:865–878 DOI 10.1007/s10811-014-0387-2 Morphological, biochemical, and phylogenetic assessments of eight Botryococcus terribilis strains collected from freshwaters of Transylvania Adriana Hegedűs & Aurel Mocan & Lucian Barbu-Tudoran & Cristian Coman & Bogdan Drugă & Cosmin Sicora & Nicolaie Drago Received: 1 April 2014 /Revised and accepted: 24 July 2014 /Published online: 19 August 2014 # Springer Science+Business Media Dordrecht 2014 Abstract Botryococcus braunii is a green unicellular our strains to Botryococcus terribilis species. Detailed analy- microalga with a unique potential to produce large quantities ses regarding the growth performances, ultrastructural charac- of hydrocarbons similar to fossil fuel. Up to now, B. braunii is teristics, and hydrocarbon and fatty acid profiles were also the most studied species of the Botryococcus genus. The included in our study. The micrographs obtained in scanning taxonomic affiliation of eight different strains of the genus electron, transmission electron, and light microscopies Botryococcus collected from freshwaters of Transylvania was showed a high degree of similarity to other strains affiliated investigated based on their morphological characteristics and to the B chemical race. Also, gas chromatography–mass spec- molecular profile using small subunit (SSU) ribosomal RNA trometry assay showed for the first time the ability of (rRNA) genes and internal transcribed spacer 2 (ITS2) B. terribilis strains to synthesize C30–C32 botryococcenes, sequence-structure analysis. The phylogenetic inference using which are known to be specific to the B-type Botryococcus ITS2 sequence-structure molecular marker, an approach ad- strains. dressed for the first time in the issue of Botryococcus genus phylogeny, generated similar results with the 18S rRNA gene Keywords Botryococcus terribilis . Botryococcenes . based analysis. In both phylogenetic trees we constructed, the 18S rDNA . ITS2 sequences of our strains formed an independent cluster within the B-race clade. Based on the phylogenetic data and the presence of long mucilaginous processes which emerged from Introduction the periphery of the colonies, we established the affiliation of The genus Botryococcus includes green colonial microalgae Electronic supplementary material The online version of this article which are widespread from temperate to tropical freshwater (doi:10.1007/s10811-014-0387-2) contains supplementary material, bodies. The feasibility of biofuel production using which is available to authorized users. Botryococcus strains (Moldowan and Seifert 1980;Audino : : A. Hegedűs(*) C. Coman B. Drugă et al. 2002; Summons et al. 2002; Ghasemi et al. 2012)is Institute of Biological Research, 48 Republicii Street, based on their unique potential to synthesize large quantities 400015 Cluj-Napoca, Romania of hydrocarbons (Largeau et al. 1980a, b; Wake and Hillen e-mail: [email protected] 1980, 1981;Hillenetal.1982; Metzger et al. 1985a). The A. Mocan ability of Botryococcus genus to produce different types of Institute of Public Health “Professor Iuliu Moldovan”, 6 Pasteur hydrocarbons was intensively studied, and four chemical Street, 400349 Cluj-Napoca, Romania races were defined: (i) the A race, fatty-acid-derived n-- L. Barbu-Tudoran : N. Drago alkadiene and triene hydrocarbons (Largeau et al. 1980a; Faculty of Biology and Geology, Babeş-Bolyai University, 5-7 Casadevall et al. 1984, 1985; Metzger et al. 1985a, b, 1986, Clinicilor Street, 400006 Cluj-Napoca, Romania 1993; Metzger and Largeau 2005); (ii) the B race, triterpenoid (squalenes and botryococcenes) hydrocarbons (Ben-Amotz C. Sicora Biological Research Center, 16 Parcului Street, 455200 Jibou, et al. 1985;Wolfetal.1985; Metzger et al. 1987;Okada Romania et al. 1995; Dayananda et al. 2006); (iii) the L strains, a single 866 J Appl Phycol (2015) 27:865–878 tetraterpenoid hydrocarbon named lycopadiene (Metzger and Materials and methods Casadevall 1987); and more recently (iv) the S race, epoxy-n- alkane and saturated n-alkane chains with 18 and 20 carbon Strain cultures and growth assay atoms (Kawachi et al. 2012). Except for the chemical classi- fication, the taxonomy of the genus Botryococcus is still Eight Botryococcus strains were investigated in this study unclear. Although most of the studies assigned the investigat- (see the list in Online Resource 1): AICB 413, AICB 414, ed strains to Botryococcus braunii species (Watanabe and AICB 416, AICB 418, AICB 440, AICB 442, AICB 870, Tanabe 2013), some authors emphasized the morphological and AICB 872. Botryococcus isolates are deposited in the heterogeneity (Komárek and Marvan 1992) and the phyloge- Algae and Cyanobacteria Culture Collection of the netic divergence of Botryococcus genus(Kawachietal. Institute of Biological Research (AICB), Cluj-Napoca, 2012). The last group of authors established the relationship Romania (Drago et al. 1997). The strains were grown between the above mentioned four chemical races and their on BG-11 medium (Allen and Stanier 1968; Watanabe phylogenetic profile based on 31 new Botryococcus isolates. et al. 2000), in continuous irradiance of approximately Using 47 Botryococcus populations collected from differ- 150 μmol photons m−2 s−1, 25±2 °C, in aerated flasks ent biotopes all over the world, Komárek and Marvan (1992) (500 mL). Optical density (OD) measurements at 600 nm described 13 morphotypes (including the known species were taken every 2 days. In late exponential growth phase B. braunii (Kützing 1849) Botryococcus protuberans (approximately 30 days), the biomass was harvested and (Komárková 1991), and Botryococcus canadensis (Hindák aliquoted for subsequent morphological, biochemical, and 1991)), and they defined six new species: Botryococcus molecular analyses. Aliquots of 50 mL were filtered and comperei, Botryococcus australis, Botryococcus fernandoi, washed two times with distilled water to assess the dry Botryococcus neglectus, Botryococcus pila,and weight. The samples were dried (70 °C) to constant Botryococcus terribilis. Plain et al. (1993) contested the mor- weight (at least 24 h). The growth process was character- phological features as reliable criteria to distinguish among ized by the doubling time and the chlorophylls to carot- Botryococcus species due to the inherent morphological enoids ratio relative to the dry weight. The doubling time changes within a clonal strain. Thus, the plasticity of morpho- was calculated following the formula of Guillard (1973). logical characters remains a crucial aspect in solving the The assimilatory pigments were quantified based on taxonomic issue of the genus. Arnon (1949), Goodwin (1976), and Britton et al. (1995) According to Komárek and Marvan (1992), the distinctive protocols. morphological feature of B. terribilis colonies is the presence of “short or long, simple or irregularly branched gelatinous processes” emerging from the periphery of the colonies. This Light and electron microscopy species was signaled in Cuba (Komárek and Marvan 1992; Comas 1996), Brazil (Nogueira and Oliveira 2009;Rodrigues Light microscopy was performed using an Olympus et al. 2010; de Queiroz Mendes et al. 2012;Nascimentoetal. BX-41 microscope equipped with a photo camera. For 2013), Spain (Fanés Treviño et al. 2009), Sweden, Austria, scanning electron microscopy (SEM), algal samples Chad, and Czech Republic (Komárek and Marvan 1992). In a were concentrated by centrifugation and washed two recent study, de Queiroz Mendes et al. (2012)outlinedthe times with 0.1 M sodium phosphate buffer (pH 6.8), morphological and ultrastructural characters of a newly iso- followed by a final wash with distilled water. The cells lated strain of B. terribilis (FW-15) which agree in general were fixed in 4 % glutaraldehyde in sodium phosphate aspects with the original description of Komárek and Marvan buffer (4 °C) overnight and then fixed on copper (1992) and with other strains belonging to B. braunii species holders, covered by a 7-nm silver or gold layer. The (Wolf and Cox 1981; Berkaloff et al. 1984; Largeau et al. images were taken with a Jeol JSM5510lLV electron 1980b;Casadevalletal.1985; Metzger and Largeau 2005; microscope. For transmission electron microscopy Weiss et al. 2012). (TEM), fresh colonies were collected by centrifugation, In the present study, we aimed to establish the taxonomic fixed in 4 % glutaraldehyde for 1 h, and rinsed four affiliation of eight Botryococcus strains isolated from times with 0.1 M sodium phosphate buffer (pH 6.8). Transylvania (Romania), based on morphological characters Subsequently, the biomass was resuspended in 2 % supported by molecular data. To increase the resolution of the OsO4 in phosphate buffer, for 1 h. The fixed material phylogenetic analysis, both the small subunit ribosomal RNA was dehydrated through a graded ethanol series and (rRNA) gene sequences and the internal transcribed spacer 2 treatment with propylene oxide. The samples were em- (ITS2) sequence structures were used in the study. The ultra- bedded in a mix of propylene oxide and Epon 812 structural and biochemical characteristics of the investigated resin. A TEM Jeol JEM1010 microscope was used to strains were also included in our analysis. observe the thin sections. J Appl Phycol (2015) 27:865–878 867 Hydrocarbon (HC) and fatty acid (FA) analyses—gas was performed in 1 %w/v agarose gel (stained with chromatography–mass spectrometry (GC-MS) 1 μgmL−1 ethidium bromide), and photographs were taken with the BioDoc-it Imaging System
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