Microb. Resour. Syst. 39
June
（1）
：33
2023─ 40, 2023

Vol. 39, No. 1

Additional polyamine analysis of the algae belonging to the phyla
Glaucophyta, Rhodophyta and Chlorophyta
─Polyamine analysis of algae V─

Koei Hamana1)＊, Takemitsu Furuchi2), Hidenori Hayashi1),
Takeshi Uemura2) and Masaru Niitsu2)
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, Japan1)

To prepare a cellular polyamine distribution catalogue of the three algal phyla Glaucophyta, Rhodophyta andChlorophyta in Archaeplastida, we analyzed 2 strains (2 species) of glaucophytes, 14 strains (10 species) of red algae and
27 strains (22 species) chlorophyte green algae. The acid-extracted polyamines from the algae were analyzed by HPLC
and HPGC-MS. Putrescine and spermidine were the polyamines of Cyanophora and Glaucophyra of Glaucophyta. In theunicellular acidothermophilic Rhodophyta, Cyanidium, Cyanidioschyzon and Cyanidiococcus contained putrescine,spermidine and spermie, and norspermidine, homospermidine and thermospermine were added in Galdieria.
Multicellular marine Asparagopsis contained homospermidine and aminopropylhomospermidine. Caldopentamine andthermopentamine were distributed in multicellular freshwater Hildenbrandia. In the Chlorophyta, putrescine andspermidine were the major polyamines in Carolibrandtia, Picochlorum, achlorophylus Prototheca and phototrophic/
heterotrophic Auxenochlorella. Norspermidine was added to endosynbiotic Protodesmus. Coccomyxa and photobiontic
Asterochloris contained putrescine, norspermidine, spermidine, homospermidine and spermine. Grecesiella andbacteriovory-potent Pyramimonas and Pterosperma contained putrescine, norspermidine and spermidine. Snow alga
Chloromonas contained diaminopropane, putrescine, norspermidine and spermidine. Gymnomonas contained putrescinealone.

Key words: alga, Chlorophyta, Glaucophyta, polyamine, Rhodophyta

Glaucophytes of the phylum Glaucophyta, red algae

names are confusing, Archaeplastida is composed ofof the phylum Rhodophyta and green algae of thethe phyla Glaucophyta, Rhodophyta and Chloroplas-

phylum Chlorophyta have plastid(s) as a result of thetida (including Chlorophyta, Streptophyta and Cha-

primary endosymbiosis of a phototrophic cyanobac-

rophyta) (Leliaert et al., 2012; Lewis & McCourt,

terium, which evolved independently without sec-2004). Therefore, green algae were divided into chlo-

ondary and tertiary endosymbiosis and the threerophyte green algae, streptophyte green algae andphyla are located together in Archaeplastida (un-charophyte green algae in our studies (Hamana et al.,ranked) of the kingdom Plantae (NBRP ALGAE,

2004, 2013, 2018a).

2009; MCC-NIES, 1983). On the other hand, the phy-

Following to our previous reports (–Polyamine

lum Chlorophyta and the phylum Streptophyta, an-analysis of algae I, II, III and IV–) (Hamana et al.,other green algal phylum, are located together in

2017, 2018a, b, 2022), we additionally analyzed 2

Viridiplantae (unranked) in Plantae (NBRP ALGAE,

strains (2 species) of glaucophyte algae in Glauco-2009; MCC-NIES, 1983). Although taxonomical rank

phyta, 14 strains (10 species) of red algae in Rhodophyta and 27 strains (22 species) of chlorophyte＊

Corresponding author

green algae in Chlorophyta and report in –Polyamine

E-mail: koeihamana@gmail.com

analysis of algae V–. Endosymbiotic green alga iso-Accepted: March 22, 2023

lated from ciliate and photobiontic (photo-symbiotic)
─ 33 ─

Polyamines of glaucophytes, red algae and green algae

Hamana et al.

green algae isolated from lichen (Leliaert et al., 2012;

in, Dowex 50WX8 (3 cm I.D. ×1 cm or 1 cm I.D. ×3

Lewis & McCourt, 2004) are distributed. A hot-cm). The polyamines were eluted with 6M HCl andspring green alga and a snow green alga were iso-then analyzed with by high-performance liquid chro-lated in Japan (Satoh et al., 2010; Matsuzaki et al.,matography (HPLC) on a Hitachi L6000 (Hamana et2020). Achlorophyllous (colorless) green alga Pro︲

al., 2016a, b).

thotheca (Suzuki et al., 2018) and bacterivory-potent(HFB), HPGC-mass spectrometry (HPGC-MS) on agreen algae (Bock et al., 2021) have also been found.

JEOL JMS-700 was performed (Hamana et al., 2016a,

We referred green algal taxonomy to NBRP ALGAEb). Molar concentrations of cellular polyamines per(2009), MCC-NIES (1983), NCBI (1988) and/or Algae-

gram of wet weight of the starting algae were

Base (1996).

roughly estimated from the HPLC and HPGC were

After the heptafluorobutyrization

The axenic or unialgal strains supplied by theperformed using authentic polyamine standards and

MCC-NIES (Microbial Culture Collection, National

are shown in Table 1. Minor (0.01-0.02 μmol/g wet

Institute for Environmental Studies) were cultured

weight in Table 1) polyamines are possible to extract

under the light (10-14 h/24 h) using 1-10 l of the liq-

from some contaminations in non-axenic algal sam-uid media designed by MCC-NIES (1983). Threeples.

axenic achlorophyllous Prototheca strains were purchased from JCM (Japan Collection of Microorgan-

Glaucophyte algae

isms, RIKEN BioResource Research Center) (1981)

The phylum Glaucophyta consists of the class Glau-and cultivated in axenically the heterotrophic culture

cophyceae containing the four genera Cyanophora,

medium in the dark. The dried powders of Sun

Cyanoptyche, Glaucocystis and Gloeochaete. It has

Chlorella strain (Sun Chlorella Co., Japan) of Chlorella

been reported that putrescine (4) and spermidine (34)and CHIKUGO C-5 strain (Chlorella vulgaris)

were major polyamines in the one species of Glauco︲(WAKANDO Co. Japan) of Parachlorella were com-

cystis and three species of Cyanophora (Hamana &mercially available as a food material. Freshwater

Matsuzaki, 1985; Hamana & Niitsu, 2006). Addition-

red alga“Tansui-benimadara”(Hildenbrandia rivu︲

ally Cyanophora cuspidata and Glaucocystis miyajii

laris) and freshwater green alga“Kawashiogusa”

analyzed in the present study contained putrescine(Cladophora glomerata) were collected in Gunma andand spermidine (Table 1). Although glaucophytes

Tochigi, Japan by the advise of Gunma Museum of

belonging to the genera Cyanoptyche and Gloeo︲

Natural History, Gunma, Japan. Marine red algachaete have never been analyzed, the ubiquitous oc-“Kagikenori”(Asparagopsis taxiformis) was suppliedcurrence of putrescine and spermidine within thefrom The Kuroshio Biological Research Institute, Ko-

phylum Glaucophyta was suggested. The unicellu-

chi, Japan. Other four dried red-algal seaweeds (Di︲lar, phototrophic, eukaryotic glaucophytes grow un-

genea simplex, Chondrus yendoi, Caulacanthus ustula︲der mesophilic and neutrophilic conditions and it has

tus and Gloiopeltis tenax) and fresh green-algal

been known that they evolved by the primary sym-

seaweed (Monostroma nitidum) were purchased frombiosis of a phototrophic cyanobacterium. Further-a market in Maebashi, Gunma.

more, secondary endosymbiosis of glaucophyte into

Axenic unicellular algae harvested at the stationary

other eukaryotic organism has not been found in thephase (2-10 g wet weight, after the check of contami-

varieties of eukaryotic unicellular and multicellularnation under a microscope), almost-axenic dried pow-

algae. Polyamine distribution profiles of the glauco-

der (2-10 g wet weight, after rehydration) and non-phytes were identical to one of the two polyamine-axenic, fresh macroalgae isolated from fields (100-distribution types, putrescine plus spermidine type

200 g wet weight, after the washing by sonication,and putrescine plus homospermidine (44) type, foundcetrifugation and filtration), were homogenized in 5%

in major mesophilic, neutrophilic cyanobacteria of theperchloric acid (PCA). The PCA extract was sub-phylum Cyanobacteria (Hamana et al., 2016a).

jected to a column containing a cation-exchange res─ 34 ─

Table 1 Concentration of polyamines of glaucophytes, red algae and chlorophyte green algae of Archaeplastida

Microb. Resour. Syst. June 2023
Vol. 39, No. 1

─ 35 ─

Polyamines of glaucophytes, red algae and green algae

Hamana et al.

Red algae

was detected as a major polyamine in the freshwater

The phylum Rhodophyta is divided into the threemulticellular red algae located in the orders Thore-

subphyla Cyanidiophytina, Proteorhodophytina andales, Batrachospermales and Compsopognales (Ha-Eurhodophytina. Primitive unicellular acidothermo-mana et al., 2018b).

philic red algae have been isolated from terrestrial

Diaminopropane, norspermidine, norspermine andacidic hot springs and are located in the order Cy-

thermospermine and caldopentamine (3333) and/or

anidiales of the subphylum Cyanidinophytina. Cy︲

thermopentamine distributions were widely spreadanidiococcus yangmingshanensis (Liu et al., 2020),

within the subphylum Eurhodophytina. Occurrence

newly analyzed in the present study, as well as Cy︲of penta-amines may be related to multicellular form

anidium caldarium and Cyanidioschyzon melorae in-in red algae. Penta-amines were not found in unicel-

cluding previously and newly analyzed strains, con-lular red algae such as Porphyridium (order Porphy-

tained ubiquitously putrescine (4), spermidine (34)ridales), Dixoniella and Bulboplastis (order Dixoniella-and spermine (343) (Table 1). Galdieria partita (Ha-les) (Hamana et al., 2018b).

mana et al., 2018b) and G. sulphuraria contained diaminopropane (3), norspermindine (33), norspermine

Chlorophyte green algae(333), and/or thermospermine (334) in addition to pu-

The phylum Chlorophyta is divided into the classes

trescine, spermidine and/or spermine (Table 1). The

Chlorophyceae, Chlorodentrophyceae, Chloropicophy-

results show that an aminopropyl-transfer activity toceae, Mamiellophyceae, Nephroselmidophyceae

aminopropyl moiety of diqminopropane, norspermi-(=Nephrophyceae), Palmophyllophyceae, Pedinophy-

dine and spermidine in Galdieria species. The distri-ceae, Picocytophyceae, Pycnococcaceae, Pyramimo-

bution of the tetra-amines norspermine, spermine

nadophyceae, Trebouxiopyceae and Ulvophyceae

and thermospermine in the unicellular freshwater(Guiry & Guiry, 2019; Lopes Dos Santos et al., 2017).

red algae grown at 40°C may be correlated to their

We referred to the taxonomy of the class Prasino-slight thermophily. Diaminohexane (6) detected inphyceae shown in NBRP ALGAE (2009) and MCC-

Galdieria sulphuraria NIES-3892 and N-(3-NIES (1983).

hydroxypropyl)-1,4-diaminobutane (43OH) detected in

In the class Trebouxiophyceae, we have reported

C. caldarium NIES-3891 were first found within thethat non-photosynthetic achlorophyllous heterotro-

phylum Rhodophyta, however phylogenetic signifi-

phic Helicospiridium and Prototheca contained pu-

cance on the distribution of the diamine and alkanol-

trescine (4), norspermidine (33) and spermidine (34)polyamine is not clear.

by HPLC analysis (Hamana et al., 2004). Since HPLC

Six multicellular red algal seaweeds belonging tois insufficient for the analysis of norspermidine, somethe subphylum Eurhodophytina were newly ana-

Prototheca species were reanalyzed by HPGC-MS inlyzed. Asparagopsis taxiformis contained homosper-

the present study. Heterotrophic Prototheca species

midine (44) and aminopropylhomospermidine (344) as

were cultured in Pro medium (to 100 ml MBM medi-

a major polyamine. Thermopentamine (3343) wasum add 100 mg proteose peptone) (MCC-NIES, 1983)

found as a major polyamine in Gloiopeltis tenax col-in the dark in the previous and present studies.

lected in Mie, Japan as well as another sample col-Three Prototheca species were newly analyzed in thelected in Ise, Japan. The freshwater thalloid multi-

present study by HPLC and HPGC-MS. The data ofcellular red alga Hildenbrandia rivularis“Tansui-these three species show the absence of norspermi-

benimadara”belonging to the order Hildenbrandiales

dine (Table 1). Previous polyamine data of eight oth-

(AlgaeBase, 1996) was collected from a liver in Japan.

er Prototheca strains analyzed by Hamana et al.

Although contamination of bacteria in the field sam-(2004) (not reanalyzed in the present study) should beples was not excluded, homospermidine, homosper-

excluded. Incorporation of spermidine and spermine

mine (444) and 2-hydroxyputrescine (H-Put, H-4) werefrom proteose peptone in Pro medium, containing thedetected in the red algal samples. Homospermidine

two polyamines, is not excluded.
─ 36 ─

Microb. Resour. Syst. June 2023

Vol. 39, No. 1

Although it is known that Auxenochlorella protothe︲34). This is the first report on the detection of thecoides grows both phototrophically and heterotrophi-

three modified polyamines in the Chlorella samples.

cally, the alga did not grow well in various photo-

Polyamine profiles were varied in the five Cocco︲

trophic growth media under the absence of proteosemyxa strains, however thermospermine and N-(3-hy-

peptone. We cultured five strains of the alga in Pro

roxpropyl)norspermidine (333OH) were detected in

medium in the light or dark in the previous andoleaginous NBRC 112354 strain, grown at 25-30°C,

present studies. Polyamine data of the strain IAM

isolated from a hot spring, Japan (Satoh et al., 2010)

C-206 by HPLC in Hamana et al. (2004) should be col-(Table 1).

lected, as shown in the present polyamine analysis

Although the above green algae belonging to theby HPGC-MS in addition to HPLC (Table 1). Poly-class Trebouxiophyceae are terrestrial freshwater

amine distributions were common in the five strains.

algae, marine Picochlorum oculatum which was iso-Relatively higher putrescine level was found in thelated in Japan contained putrescine, cadaverine (5)dark, while relatively higher levels of spermidine andand spermidine alone (Table 1).

spermine which are produced from putrescine, were

In the class Prasinophyceae, marine Tetraselmis

found in the cells cultured under the light, as foundverrucosa was added, and compared with other ma-

in NIES-2165 strain and NIES-2163 strain (Table 1)rine and freshwater Tetraselmis species and othershowing a phototrophic growth affect in their cellu-

marine species of the class. Freshwater T. cordifor︲

lar polyamine levels but not in their polyamine pro-mis containing homospermidine and norspermine

files.

and marine T. subcordiformis containing nor-Endosymbiotic Protodesmus globulifer (endosymbi-

spermine were specific in the class, as shown in the

ont in Paramecium bursaria) (Nakahara, MCC-NIES,

previous report (Hamana et al., 2018a). Bacterivory-1983), Carolibrandtia ciliaticola (Brandtia ciliaticola)

potent Pyramimonas parkeae and Pterosperma crista︲(endosymbiont in Cyclotrichium viride) (Hoshina &tum (Bock et al., 2021) contained putrescien, norsper-

Nakada, 2018; Hoshina et al., 2018) and another endo-

midine and spermidine, as a typical polyamine profile

symbiotic Chlorella variabilis (endosymbiont in Para︲in the class (Table 1).

mecium bursaria F36) (Hoshina et al., 2004; Minaeva

In the class Chlorophyceae, the psychrophilic snow

& Ermilova, 2017) have different polyamine profiles

green alga Chloromonas fukushimae (Matsuzaki et(Hamana et al., 2018a) (Table 1). A photosynthetical., 2020) isolated in Japan and a naked green flagel-symbiont, Asterochloris cf. glomerata (symbiont inlate, Gymnomonas nepalensis (formerly Dunaliella

Cladia aggregata) (Ohmura, MCC-NIES, 1983) con-lateralis) (Watanabe & Nakada, 2018) were available.

tained thermospermine (334) but not homospermi-

Graesiella emersonii was reclassified from former

dine (44) whereas another photobiontic Trebouxia

Chlorella emersonii or Chlorella pyrenoidosa (Nozaki

species contained homospermidine but not thermo-

et al., 1995). C. fukushimae grown at 5°C contained aspermine (Hamana et al., 2018a) (Table 1). There is ahigh-level of diaminopropane in addition to putres-

possibility that the symbiotic process of the chloro-cine, norspermidine and spermidine and G. emersonii

phytes was affected by their polyamine profiles.

contained cadaverine in addition to putrescine, nor-

Diversity of Chlorella-clade has been discussed

spermidine and spermidine (Table 1). The occur-(Darienko et al., 2010; Krivina & Temraleeva, 2020;

rence of diaminopropane in the snow green alga may

Nozaki et al., 1995). Although taxonomy of the six

be correlated to its psychrophily. The occurrence ofChlorella food materials (supplements) supplied fromputrescine alone found in G. nepalensis (belonging toYaeyama, nichie, ORIHIRO, Sun Chlorella, Chlorella

the order Volvocales) is the first report on the occur-

Industry and WAKANDO is not clear, two samples

rence of a diamine alone in algae.

contained N-(3-hydroxypropyl)-1,4-diaminobutane

In the macro-algal class Ulvophceae, Monostroma(43OH) and other two samples contained 2-hydroxy-

nitidum used for seaweed food materials and fresh-

putrescine (H-Put, H-4) and N1-acetylspermidine (Ac-water Cladophora glomerata“Kawashiogusa”for─ 37 ─

Polyamines of glaucophytes, red algae and green algae

Hamana et al.

comparison to another freshwater ulvophyte Aegag︲

Hamana, K., Matsuzaki, S., Niitsu, M. & Nagashima,

rophila linnari“Marimo”were newly analyzed. A

H. 1990. Polyamines of unicellular thermoacidophilic

penta-amine, caldopentamine (3333), was detected in

red alga Cyanidium caldarium. Phytochemistry

the M. nitidum samples of the present study, sug-

29: 377-380.

gesting that penta-amines are distributed in the classHamana, K., Aizaki, T., Arai, E., Saito, A., Uchikata,(Table 1). C. glomerata contained 2-hydroxyputres-

K . & O h n i s h i , H . 2004. D i s t r i b u t i o n o fcine but not penta-amines, however it is not similarnorspermidine as a cellular polyamine within

to A. linnari (Hamana et al., 2018a) in their polyamine

micro green algae including non-photosynthetic

profiles. 2-hydroxyputrescine was found in freshwa-

achlorophyllus Polytoma, Polytomella, Prototheca

ter Chlorella food materials belonging to the classand Helicosporidium. J. Gen. Appl. Microbiol. 50:

Trebouxiophyceae of the phylum Chlorophyta in ad-289-295.

dition to freshwater red alga H. rivularis (Table 1).

H a m a n a , K . , N i i t s u , M . & H a y a s h i , H . 2013.
Occurrence of homospermidine and

ACKNOWLEDGMENTS

thermospermine as a cellular polyamine in

We thank MCC-NIES and JCM for supplying algae

unicellular chlorophyte and multicellularand advice on algal culture in the present study.

charophyte green algae. J. Gen. Appl. Microbiol.
59: 313-319.
Hamana, K., Furuchi, T., Hayashi, H. & Niitsu, M.

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Cyanidiococcus gen. nov., a new extremophilic redalgal genus sister to Cyanidioschyzon

Watanabe, S. & Nakada, T. 2018. Gymnomonas(Cyanidioschyzonaceae, Rhodophyta). J. Phycol. 56:

nepalensis gen. et sp. for the naked flagellate

1428-1442.

strain ‘Nepal’ formerly identified as Dunaliella─ 39 ─

Polyamines of glaucophytes, red algae and green algae

Hamana et al.

lateralis (Volvocales, Chlorophyceae). Phycol. Res.
66: 167-172.

灰色藻植物門，紅藻植物門，および緑藻植物門に属する藻類のポリアミンの追加分析
─藻類のポリアミン分析Ⅴ─
浜名康栄 1），古地壯光 2），林秀謙 1），植村武史 2），新津勝 2）

前橋工科大学工学部，2）城西大学薬学部

1）

藻類における細胞内ポリアミン成分構成のカタログ化のため，古色素体類（Archaeplastida）に位置する灰色藻植物門，紅藻植物門，緑藻植物門に属する新規の各 2 株（2 種），14 株（10 種），27 株（22 種）から酸抽出したポリアミン画分を高性能液体クロマトグラフィー（HPLC）と高性能ガスクロマトグラフィー・質量分析（HPGC-MS）により追加分析した．灰色藻植物門の Cyanophora と Glaucophyra はプトレスシンとスペルミジンであった．紅藻植物門では，単細胞好熱性
Cyanidium，Cyanidioschyzon，Cyanidiococcus はプトレスシン，スペルミジン，スペルミンで，Galdieria ではノルスペル
ミジン，ノルスペルミン，サーモスペルミンが追加．多細胞海産 Asparagopsis ではホモスペルミジンとアミノプロピルホモ
スペルミジンなどが，多細胞淡水産 Hildenbrandia ではカルドペンタミン，サーモペンタミンなどが追加された．緑藻植物
門では，Carolibrandtia，Picochlorum，Auxenochlorella，葉緑体欠損 Prototheca はプトレッシン，スペルミジン．共生藻
Protodesmus にはノルスペルミジンが追加．Coccomyxa と共生藻 Asterochloris ではノルスペルミジン，ホモスペルミジン，
スペルミンが追加．Graesiella と細菌食能を有する Pyramimonas と Pterosperma ではプトレッシン，スペルミジン，ノルス ペ ル ミ ジ ン． 氷 雪 藻 Chloromonas で は ジ ア ミ ノ プ ロ パ ン， プ ト レ ッ シ ン， ス ペ ル ミ ジ ン， ノ ル ス ペ ル ミ ジ ン．
Gymnomonas ではプトレッシンのみであった．

─ 40 ─