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Polyamine Analysis of Unicellular, Colonial, and Multicellular Green

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Polyamine Analysis of Unicellular, Colonial, and Multicellular Green Microb. Resour. Syst. Dec.34（2 ）：732018─ 82, 2018 Vol. 34, No. 2 Polyamine analysis of unicellular, colonial, and multicellular green algae —Detection of aminobutylcadaverine, N 1-aminopentylspermidine, N 8-aminopentylspermidine, and penta-amines— Koei Hamana1)＊, Masaki Kobayashi2), Takemitsu Furuchi2) , Hidenori Hayashi1) and Masaru Niitsu2) 1)Faculty of Engineering, Maebashi Institute of Technology 460-1 Kamisadori-machi, Maebashi, Gunma 371-0816, Japan 2)Faculty of Pharmacy and Pharmaceutical Sciences, Josai University 1-1 Keyakidai, Sakado, Saitama 350-0295, Japan To obtain the relation between cellular polyamine distribution profiles and multicellular evolution in green algae, we acid-extracted polyamines from 59 additional unicellular, colonial and multicellular green-algal samples (52 species), newly analyzed them with HPLC and HPGC, and compared them with 124 previously analyzed green algal polyamine profiles. Tetra-amines, norspermine and/or spermine, which are distributed as major polyamines predominantly in multicellular, macro green algae, were found also in unicellular photobiontic Trebouxia species and endosymbiotic Chlorella variabilis (Trebouxiophyceae), respectively. In the class Chlorophyceae, colonial freshwater Volvox, Pleodorina, Eudorina, Yamagishiella, Pandorina, Tetrabaena and Gonium (Volvocales) always contain putrescine, norspermidine and spermidine as major polyamines, similar to unicellular Chlamydomonas and Haematococcus, indicating that there is no correlation between their colony-forming and polyamine profiles. A novel triamine, aminobutylcadaverine, homospermidine and homospermine were all detected as minor polyamines in another colonial alga, Westella (Sphaeropleales). Furthermore, the aminobutylcadaverine level increased, and novel tetra-amines N1-aminopentylspermidine and N 8-aminopentylspermidine appeared in a culture supplemented with 1 mM cadaverine. The occurrence of thermospermine was limited in multicellular thallic freshwater Prasiola (Trebouxiophyceae) and multicellular thallic marine Ulva (Ulvophyceae). Caldopentamine, homocaldopentamine and/or thermopentamine were distributed as minor polyamines in unicellular coenocytic Codium, multicellular branched-filamentous Aegagropila, thallic Monostroma (Ulvophyceae) and filamentous Spirogyra (Zygnematophyceae) in addition to Prasiola and Ulva, suggesting that the occurrence of penta-amines is related to multicellular and macro green-algal evolution. Key words: aminobutylcadaverine, aminopentylspermidine, green alga, penta-amine, polyamine, thermosper- mine INTRODUCTION green algal samples belonging to the two phyla We have analyzed various eukaryotic algae to Chlorophyta (divided into four classes reveal the phylogenetic significance of polyamine Trebouxiopyceae, Chlorophyceae, Prasinophyceae, distribution profiles in varieties of unicellular algae and Ulvophyceae) and Streptophyta (divided into six by secondary and tertiary symbioses and their evo- classes Mesostigmatophyceae, Chlorokybophyceae, lution into multicellular forms (Hamana, 2008; Klebsormidiophyceae, Zygnematophyceae, Hamana & Matsuzaki, 1982, 1985; Hamana & Niitsu, Coleochaetophyceae, and Charophyceae) (Inouye, 2006; Hamana et al., 1988, 1990, 2004a, 2004b, 2013, 2007; Finet et al., 2010; Leliaert et al., 2012), 1,3-diami- 2016b, 2017). Within the 124 previously analyzed nopropane (3) (numeric codes of polyamines abbrevi- ated as the number of methylene (CH2) groups between amino (NH2) or imino (NH) groups), putres- ＊Corresponding author cine (4), cadaverine (5), spermidine (34), norspermi- E-mail: [email protected] dine (33), homospermidine (44), norspermine (333), Accepted: September 1, 2018 spermine (343) and thermospermine (334) were wide- ─ 73 ─ Polyamines of green algae Hamana et al. ly distributed (Hamana & Matsuzaki, 1982; Hamana mance gas chromatography (HPGC) technique devel- et al., 1988, 2004a, 2013). Non-photosynthetic achloro- oped with a long capillary column and a high-perfor- phyllous heterotrophic green algae Polytoma, mance liquid chromatography (HPLC) method Polytomella, Prototheca, and Helicospiridium belong- advantageous for minor polyamine analysis (Hamana ing to the class Trebouxiophyceae or Chlorophyceae et al., 2016a, 2016b; Niitsu et al., 2014). contained putrescine, norspermidine and spermidine (Hamana et al., 2004a). In the multicellular terrestri- MATERIALS AND METHODS al green algae, such as Nitella and Chara, belonging The green microalgae strains supplied by the to the class Charophyceae, two unusual tetra-amines, Microbial Culture Collection at the National Institute aminopropylhomospermidine (344) and canavalmine for Environmental Studies (MCC-NIES) and the (434), were found in addition to the common Biological Resource Center, National Institute of diamines, triamines and tetra-amines (Hamana et al., Technology and Evaluation (NBRC) were cultivated 2013). phototrophically in the light (10—14 h/24 h) at Outside of the 124 previously analyzed green algal 20-25℃ using 1-10 l of the liquid media designed by samples, we selected Trebouxia species isolated as a MCC-NIES (http://mcc.nies.go.jp, 2017) and NBRC photobiont (photosynthetic symbiont) in lichen (https://www.nite.go.jp/en/nbrc, 2017), respectively. (Ahmadjian, 1960; Inouye, 2007) and endosymbiotic DBT microalgal strains were purchased from the Chlorella variabilis isolated from the ciliate Department of Biotechnology, Institute of Paramecium bursaria (Hoshina et al., 2004; Minaeva Environmental Biology Co. (DBT) and cultured pho- & Ermilova, 2017). Multicellular freshwater Prasiola totrophically in the media (1-1.5 l) designed by DBT. japonica with membranous thalli belongs to the class In the additional mass culture of three unicellular Trebouxiophyceae. Multicellular seaweeds, such as algae, the medium was supplemented with 1 mM thallic (foliose) Monostroma and Ulva, branched fila- cadaverine (cadaverine 2HCl, Sigma, USA). The mentous Chaetomorpha and Caulerpa, and unicellu- dried powders of Dunaliella DIC strain (DIC lar coenocytic Codium and Halimeda, belong to the LIFETEC Co.), Yaeyama Chlorella strain (Yaeyama class Ulvophyceae (Lewis & McCourt, 2004). Shokusan Co.), Sun Chlorella strain (Sun Chlorella Multicellular branched-filamentous freshwater Co.), nichie strain (nichie Co.), ORIHIRO strain Aegagropila and marine Valonia aegagropila forming (ORIHIRO Co.) of Chlorella, and Chlorella Industry bubble colonies with large spherical single coenocyt- (Chikugo) strain (Chlorella Industry Co.) of ic cells are also found in this class. Gonium, Parachlorella are commercially available in Japan as Tetrabaena, Pandorina, Yamagishiella, Eudorina, food supplements. The freshwater macroalga Pleodorina and Volvox are the genera of colony “Kawa-nori” (Prasiola japonica) was kindly supplied (coenobium)-forming microalgae, as the members of by Kuwaya Co., Minakami (cultured in the Tone the order Volvocales (Chlamydomonadales) of the River) and Misato-kan of Tange Spa, Nakanojo (col- class Chlorophyceae were evolved from a single lected in the Tange River), and collected by primitive Chlamydomonas-like alga (Arakaki et al., Hamana, K. with the support of Shimonita Shizenshi- 2013; Herron et al., 2009; Inouye, 2007; Lewis & kan in the Aokura River, Shimonita, Gunma, Japan. McCourt, 2004; Nozaki et al., 2000). Westella and The marine green macroalgae “Hitoegusa” Pediastrum (Sphaeropleales) are colony-forming (Monostroma nitidum),“Ana-aosa” (Ulva perusa), (colonial) genera, and Stigeoclonium (Chaetophorales) “Suji-aonori” (Ulva prolifera) and“Kubirezuta” and Oedogonium (Oedogoniales) form branched-fila- (Caulerpa lentillifera), and the freshwater green mac- ment and linear-filament, respectively, in the class roalga“Marimo” (Aegagropila linnaei) were pur- Chlorophyceae (Inouye, 2007; Lewis & McCourt, chased from the markets in their habitats in Japan 2004). (Table 1). “Aomidoro” (Spirogyra sp.) were collected To reveal the polyamine components related to from paddy fields in Gunma. Marine“Futo-juzumo” multicellular morphological development and colony- (Chaetomorpha spirales),“Tama-baronia” (Valonia forming in addition to their phylogenetic locations, aegagropila) and“Uchiwa-sabotengusa” (Halimeda here we newly analyzed polyamines of 59 additional discoidea), and freshwater“Hime-furasukomo” green-algal samples (52 species) including the above- (Nitella flexilis) were purchased from aquarium mar- mentioned green algae by employing a high-perfor- kets in Chiba, Gunma and Saitama, respectively. ─ 74 ─ Microb. Resour. Syst. Dec. 2018 Vol. 34, No. 2 Table 1 Concentration of polyamines of green algae Table 1. Concentration of polyamines of green algae Polyamines (μmol/g wet weight) Green algae Ref. Dap Put Cad Dah NSpd Spd APCad HSpd ABCad NSpm Spm TSpm APHSpd Can HSpm AP1Spd AP8Spd CPen HCPen TPen AP4NSpd AP4Spd Phylum Chlorophyta 3 4 5 6 33 34 35 44 45 333 343 334 344 434 444 534 345 3333 3334 3343 3(3)3 3(3)4 Class Prasinophyceae Tetraselmis cordiformis NIES-18 (freshwater) - 1.49 0.25 - 0.01 0.52 - 0.25 - 0.32 0.02 - - - - - - - - - - - Tetraselmis subcordiformis NIES-2572 (marine) - 0.36 0.03 - 0.10 0.56 - - - 1.20 - - - - - - - - - - - - + 1 mM Cad (5) - 0.05 >2.0 - 0.05 0.50 0.05 - - 0.99 - - - - - - - - - - - - Class Trebouxiophyceae Trebouxia anticipsta NIES-1271 (photobiont) (Japan) - 0.20 0.10 - - 0.60 - 0.17 - 0.07 - - - - - - - - - - - - Trebouxia corticola NIES-1278 (photobiont) (Japan) - 0.25 0.10 - - 0.55 - 0.15 - 0.05 - - - - - - - - - - - - Trebouxia erici NIES-2185 (photobiont)
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