Notes on Six Unrecorded Indigenous Species of Filamentous cyanobacteria (Cyanophyceae, Cyanophyta) in Korea

Byoung Cheol Yim, Mi Ae Song, Sung Do Bang, Sung Ro Yoon and Ok Min Lee

296Korean J. Environ. Biol. 35(3) : 296~304(2017) https://doi.org/10.11626/KJEB.2017.35.3.296

INTRODUCTION

Though they are microscopic in size and simple in cel- lular structure, the cyanobacteria played dramatic roles in Earth’s remote past, photosynthetic cyanobacteria produced Earth’s first oxygen atmosphere, thereby reducing carbon dioxide levels and influencing the global climate. Cyano- bacteria remain important today, having both positive and negative impacts from the human perspective. Some cya- nobacteria have potential biotechnological applications in producing medicinal compounds and hydrogen-based ener- gy. The tendency of many cyanobacteria to produce toxins and form harmful blooms is an increasingly serious concern worldwide (Robarts and Zohary 1987; Kim et al. 1995;

Graham et al. 2009). The harmful cyanobacterial genera that mainly cause bloom, such as Microcystis, Oscillatoria, Anabaena and Aphanizomenon have been intensively stud-

ied.

Filamentous cyanobacteria are consecutively connected, either long or short; they mainly attach to submerged sub- strates including aquatic plants, submerged land plants, and rocks, and sometimes they free-float. Although filamentous cyanobacteria produce toxins including Anatoxin (Anaba- ena), their main problem is bloom caused by the produc- tion of odorous substances such as Geosmin and 2-MIB in drinking water supplies (Saadoun et al. 2001; You et al.

2013).

The 4,598 taxa of cyanobacteria have been reported to AlgaeBase (Guiry and Guiry 2017), and 343 taxa have been reported in Korea (Kim 2015). In Oscillatoria, 305 taxa have been reported in AlgaeBase, and 18 have been report- ed in Korea, and in Phormidium, 211 have been reported in AlgaeBase, and 42 taxa has been reported in Korea. Fewer taxa have been reported for Anagnostidinema, Komvopho- ron, Hydrpcoleum and Pseudanabaena in Korea, but studies on Korean cyanophytes are still scarce. For this study, we collected and identified unrecorded filamentous cyano-

* Corresponding author: Ok Min Lee, Tel. 031-249-9643, Fax. 031-241-0860, E-mail. [email protected]

ⓒ2017. Korean Society of Environmental Biology.

Notes on Six Unrecorded Indigenous Species of Filamentous cyanobacteria (Cyanophyceae, Cyanophyta)

in Korea

Byoung Cheol Yim, Mi Ae Song, Sung Do Bang, Sung Ro Yoon and Ok Min Lee*

Department of Life Science, College of Natural Science, Kyonggi University, Suwon 16227, Republic of Korea

Abstract - Samples were collected between August 2016 and May 2017 at Sangju-si, Gyeongsang- buk-do, Jeju-do, and Uljin-gun, Gangwon-do. As a result, one genus and six species were newly recorded in Korea. The unrecorded indigenous genus was Borzia, and the six species were Anagnostidinema acutissimum, Komvophoron bourrellyi, Hydrocoleum stankovicii, Borzia trilocularis, Phormidium tinctorium and Pseudanabaena lohchoides. Phormidium tinctorium and Pseudanabaena lohchoides had been reported to inhabit freshwater, but in this study, these were found in brackish water. It had also been reported that B. trilocularis trichomes are composed of up to 8 cells, but in this study, a maximum of 10 cells was observed.

Key words : Borzia, brackish water, Oscillatoriales, Synechococcales

<Original article>

Six Unrecorded Indigenous Species of Filamentous cyanobacteria in Korea 297

phytes in Korea from freshwater streams and ponds and brackish water to add the cyanophycean flora of Korea.

MATERIALS AND METHODS

We collected filamentous cyanobacteria from both fresh- water and brackish water from small streams in Sangju-si, Gyeongsangbuk-do, and Uljin-gun, Gangwon-do, and from a small pond and a bay in Jeju-do from July 2016 to May 2017 (Table 1). We collected planktonic cyanobacteria with a 20 μm-mesh phytoplankton net; benthic cyanobacteria, we collected the samples by scrubbing submerged plants and rocks. We stored and sealed each sample opaque containers and transported them to the laboratory (Crispim et al. 2004);

some samples were fixed with 1% formalin aldehyde. We made enrichment cultures of the algae in BG-11 (Sigma C3061), and deposited the samples at the Nakdonggang National Institute of Biological Resources and the National Institute of Biological Resources. The samples were exam- ined under an Olympus BX41 light microscope (at ×400- 1,000; Olympus, Tokyo, Japan) and photographed using an AxioCam HRC camera (Carl Zeiss, Oberkochen, Germany).

The taxonomic classification system was based on Komárek et al. (2014) and AlgaeBase (Guiry and Gui- ry 2017), and we identified the cyanobacteria following Prescott (1982), Hirose et al. (1977), Chung (1993), Wehr and Sheath (2003), Komárek and Anagnostidis (2005), and John et al. (2011).

RESULTS AND DISCUSSION

In this study, one genus and six species of filamentous cyanobacteria were newly recorded in Korea. The newly recorded genus was Borzia, and the newly recorded species

were Anagnostidinema acutissimum, Komvophoron bour- rellyi, Hydrocoleum stankovicii, Borzia trilocularis, Phor- midium tinctorium and Pseudanabaena lohchoides.

The characteristics of the species are as follows.

Order Oscillatoriales Family Coleofasciculaceae Genus Anagnostidinema



Anagnostidinema acutissimum (Kufferath)

Strunecký,

Bohunická,

J.

R.

Johansen and J.

Komárek 2017 (Fig.

1)

The thallus is mucilaginous and membranaceous. These cyanobacteria consists of fine blue-green trichome bundles and sometimes free-floating solitary trichomes. Trichomes are blue-green in color and straight, but a small number of cells are attenuated and bent at the ends. At the cross- walls, constriction occurs inconspicuously or not, and there are cyanophycin granules near the cross-wall. The cells are 1.5-2.5 μm and 3-7 μm long.

Ecology: This species lives in freshwater and is benthic in shallow stagnant water. We collected it from submerged plants in freshwater streams.

Distribution: Arctic: Svalbard (Spitsbergen; Matula et al.

2007); Europe: Georgia (Barinova et al. 2011), Germany (Täuscher 2011, 2014), Lithuania (Karosiene and Kas- peroviciene 2009), Romania (Caraus 2012, 2017); North America: Arkansas (Smith 2010); Asia: Russia (Medvedeva and Nikulina 2014)

Site of collection: Gyonchun-gyo, Gyeongsangnam-do (July 28, 2016)

Specimen Locality: KTSN 120000207789

Order Oscillatoriales Family Gomontiellaceae Genus Komvophoron

Sampling sites Local name Latitude Longitude

1 Gyonchun-gyo, Donam-dong, Sangju-si, Gyeongsangnam-do 36° 45′ 45.46″ 128° 25′ 87.55″

2 Jungdong-gyo, Shinam-ri, Jungdong-myeon, Sangju-si, Gyeongsangnam-do 36° 40′ 35.94″ 128° 30′ 51.93″

3 83, Ojo-ri, Seongsan-eup, Seoguipo-si, Jeju-do 33° 45′ 92.91″ 126° 92′ 00.69″

4 57-9, Ojo-ri, Seongsan-eup, Seoguipo-si, Jeju-do 33° 45′ 25.51″ 126° 91′ 91.37″

5 Uljin-daegyo, Susan-ri, Geunnam-myeon, Uljin-gun, Gangwon-do 36° 97′ 79.31″ 129° 30′ 31.11″



Komvophoron bourrellyi X.

Turon,

M.

Hernández- Mariné and J.

Catalan 1991 (Fig.

2)

Trichomes are solitary, short, and composed of 2-50 cells.

They are straight or bent in shape and deeply constricted at the cross-walls. The cell is red in color, barrel-shaped, and homogeneous without granules or aerotopes. The apical cell is rounded or hemispherical in shape and is 1.8-2.2 μm wide and 1-2.3 μm long.

Ecology: This species lives in marine areas in epibiotes on ascidians from the Mediterranean Sea (Turon et al. 1991), but we collected it from submerged plants in freshwater streams.

Distribution: Europe: Spain (De la Rosa Álamos 2016;

Gallardo et al. 2016)

Site of collection: Jungdong-gyo, Gyeongsangnam-do (September 20, 2016)

Specimen Locality: KTSN 120000207790

Order Oscillatoriales Family Microcoleaceae Genus Hydrocoleum

Hydrocoleum stankovicii Cado 1958 (Fig.

3)

Filaments are solitary or in groups and do not form com- pact thalli; they are not branched or calcified. The sheath is fine, colorless, and uneven from the outside, containing several blue-green trichomes, and it does not show constric- tion at the cross-walls. The trichome is attenuated toward the end, and the apical cell is conical-round and has conical calyptra. The cells are approximately 6 μm wide and 3.5-6 μm long.

Ecology: This species lives in freshwater, we collected it from submerged plants in freshwater streams.

Distribution: Yugoslavia (Komarek and Anagnostidis 2005)

Site of collection: Jungdong-gyo, Gyeongsangnam-do (Sep-

at Gyongchun-gyo, Gyeongsangbuk-do, on July 28, 2016. Scale bars represent 10μm.

Six Unrecorded Indigenous Species of Filamentous cyanobacteria in Korea 299

tember 20, 2016)

Specimen Locality: KTSN 120000005865

Order Oscillatoriales

Family Phormidiaceae

Genus Borzia F. Cohn ex M. Gomont 1892

Trichomes are solitary or aggregated in small groups.

Fig. 2. Microscopic photographs of Komvophoron bourrellyi X. Turon, M. Hernández-Mariné and J. Catalan found at Jungdong-gyo, Gyeo- ngsangbuk-do, on September 20, 2016. Scale bars represent 10μm.

Fig. 3. Microscopic photographs of Hydrocoleum stankovicii Cado found at Jungdong-gyo, Gyeongsangbuk-do, on September 20, 2016.

Scale bars represent 10μm.

They are short, consisting of up to eight cells, and are composed of simple structures. The species is normally immotile and can be constricted at the cross-walls. There is no sheath; however, thin mucilage is found occasionally.

The cell is cylindrical or barrel shaped, and the apical cell is rounded. In terms of dimensions, it is isodiametric.

Order Oscillatoriales Family Phormidiaceae Genus Borzia

Borzia trilocularis Cohn ex Gomont 1892 (Fig.

4) Trichomes are solitary and straight, they are very short and lack mucilaginous sheath. They are straight, normally consisting of three to eight cells. They are blue-green in color and distinctly constricted at the ungranulated cross- walls. They can be intensely creeping or immotile. The cell is barrel shaped, with large prominent granules inside.

The apical cell is hemispheric. The cell is 5-8 μm wide and 2-6.1 μm long.

Ecology: This species lives in freshwater or terrestrial wa- ter, and we collected it from submerged plants in the brack- ish water of a small bay (salinity 18‰).

Distribution: Europe: Georgia (Barinova et al. 2011), Ro- mania (Caraus 2012, 2017), Spain (Alvarez-Cobelas and Gallardo 1988); North America: Arkansas (Smith 2010);

South America: Argentina (Tell 1985), Brazil (Bicudo 1965;

Azevedo et al. 1996; Werner 2010); South-west Asia: India (Chatterjee and Keshri 2005; Gupta 2012), Iran (Afsharza- deh et al. 2003), Iraq (Maulood et al. 2013)

Site of collection: 57-9, Ojo-ri, Jeju-do (May 20, 2017) Specimen Locality: KTSN 120000212682

Order Oscillatoriales Family Phormidiaceae Genus Phormidium

Fig. 4. Microscopic photographs of Borzia trilocularis Cohn ex Gomont 1892 found in a small bay in Jeju-do on May 20, 2017. Scale bars represent 10μm.

Six Unrecorded Indigenous Species of Filamentous cyanobacteria in Korea 301



Phormidium tinctorium Kützing ex Gomont 1892

(Fig.

5)

Thallus is tufty with fasciculated and penicillated fila- ments. It is dark olive to brown in color, forms gelatinous or membranaceous mats, and attaches to substrates. Fila- ments are nearly straight and densely arranged in parallel.

The sheath is fine, strongly mucilaginous, and diffluent.

Trichomes are indistinctly to distinctly constricted and un- granulated at the cross-walls; sometimes they are lengthily attenuated at the ends. The apical cell is either acute-coni- cal or cylindrical-conical and without calyptra. The cell is 6-8.5 μm wide and 5-11 μm long.

Ecology: This species lives in freshwater and is benthic (mainly on stony substrate) in streams and rivers. We col- lected this species from submerged stone in a brackish stream (salinity 0.1‰).

Distribution: Europe: Germany (Täuscher 2014), Romania (Caraus 2002, 2017), Spain (Alvarez-Cobelas and Gallardo

1988); Asia: South China Sea (Phang et al. 2016); Pacific Islands: Hawaiian Islands (Sherwood 2004)

Site of collection: Uljin-daegyo, Gangwon-do (May 31, 2017)

Specimen Locality: KTSN 120000212680

Order Synechococcales Family Pseudanabaenaceae Genus Pseudanabaena

Pseudanabaena lonchoides Anagnostidis 1961 (Fig.

6) Thallus is usually thin, fine, and indefinite. It forms a mat to attach to substrates, but it can be free-floating. Trichomes are commonly bright blue-green in color and less frequently bluish to greenish. They are straight or variously curved but sometimes slightly screw-like or coiled in shape. Normally, they are densely arranged, entangled, or parallel. The tri- chomes vary in length, and the cross-walls are constricted

represent 10μm.

and not granulated. The trichomes have large or small aero- topes like spherical or lance-like at each end. The apical cell is acute-conical and does not have calyptra or thickened cell walls. The cell is 0.6-1.3 μm wide and 0.8-1.8 μm long.

Ecology: This species lives in thermal, brackish and salty water. We collected it from submerged plants in a eutrophic salt water pond (salinity 35 ‰).

Distribution: Europe: Turkey (Europe) (Aysel 2005); South America: Argentina (Rodriguez et al. 2006)

Site of collection: 83, Ojo-ri, Jeju-do (May 19, 2017) Specimen Locality: KTSN 120000212679

ACKNOWLEDGEMENT

This research was supported by a grant from the Nak- donggang National Institute of Biological Resources, fund- ed by the Ministry of Environment (MOE) of the Republic

of Korea (The 2016 project Finding of Freshwater Biore- sources Microalgae and Biodiversity Research of Diatoms in Freshwater Habitat) and the National Institute of Biolog- ical Resources, also funded by the MOE (NIBR201701204).

REFERENCES

Afsharzadeh S, T Nejadsatari, MR Rahiminejad and M Ebra- himnejad. 2003. Study of algal flora in Zayanderoodriver.

Iran. J. Bio. 14:32-45.

Alvarez-Cobelas M and T Gallardo. 1988. Catálogo de las algas continental esespañolas V. Cyanophyceae Schaffner 1909. Acta Bot. Malacitana 13:53-76.

Anagnostidis K. 1961. Untersuchungenüber die Cyanophyceen einiger Thermen in Griechenland. Inst. Syst. Bot. & Pflanz- engeogr. Univ. Thessaloniki 7:1-322.

Aysel V. 2005. Check-list of the freshwater algae of Turkey. J.

Black Sea/Mediterranean Environ. 11:1-124.

Fig. 6. Microscopic photographs of Pseudanabaena lonchoides Anagnostidis found in small ponds in Jeju-do on May 19, 2017. Scale bars represent 10μm.

Six Unrecorded Indigenous Species of Filamentous cyanobacteria in Korea 303

Azevedo MT de P, NMC Nogueira and CL Sant’Anna. 1996.

Criptógamos do Parque Estadual das Fontes do Ipiranga, São Paulo, SP. Algas, 8: Cyanophyceae. Hoehnea 23:1-38.

Barinova S, L Kukhaleishvili, E Nevo and Z Janelidze. 2011.

Diversity and ecology of algae in the Algeti National Park as a part of the Georgian system of protected areas. Turk. J.

Bot. 35:729-774.

Bicudo CEM. 1965. The Genus Borzia Cohn ex Gom. in S.

Paulo, Brazil. Rickia. 2:147-152.

Caraus I. 2002. The algae of Romania. Studiisi Cercetari, Uni- versitatea Bacau, Biologie 7:1-694.

Caraus I. 2012. Algae of Romania. A distributional checklist of actual algae. Version 2.3 third revision. University of Ba- cau, Bacau.

Caraus I. 2017. Algae of Romania. A distributional checklist of actual algae. Version 2.4. Studiisi Cercetari Biologie. 7:1- 1002.

Chatterjee S and JP Keshri. 2005. Borzia(Cyanophyta) in West Bengal, India, with the description of B. indica sp. nov.

Cryptogamie, Algologie 26:331-336.

Chung J. 1993. Illustration of the freshwater algae of Korea.

Academy Publishing co., Seoul.

Crispim CA, CC Gaylarde and PM Gaylarde. 2004. Biofilm- son church walls in Porto Alegre, RS, Brazil, with special attention to cyanobacteria. Int. Biodeterior. Biodegrad.

54:121-124.

De la Rosa Álamos J. 2016. Catálogo Florístico de las Cyano- prokariotas bentónicas del litoral de Andalucía. Act. Bot.

Malacitana 41:5-17.

Gallardo T, I Bárbara, J Afonso-Carrillo, R Bermejo, M Alta- mirano, A Gómez Garreta, MC Barceló Martí, J Rull Lluch, E Ballesteros and J De la Rosa. 2016. A new checklist of benthic marine algae of Spain. Algas. Boletín Informativo de la Sociedad Española de Ficología 51:7-52.

Gomont M. 1892. Monographie des Oscillariées(Nosto- cacéesHomocystées). Deuxièmepartie.-Lyngbyées. An- nales des Sciences Naturelles, Bot. 7:91-264.

Graham LE, JM Graham and LW Wilcox. 2009. Algae. Second edition. Pearson Benjamin Cummings. San Francisco.

Guiry MD and GM Guiry. 2017. AlgaeBase. World-wide elec- tronic publication, National University of Ireland, Galway.

[Available from: http://www.algaebase.org/. accessed 14 July 2017].

Gupta RK. 2012. Algae of India Volume 1. A checklist of Cy- anoprokaryota(Cyanophyceae). Salt Lake, Kolkata. Bot.

Sur. Indi. Ministry of Environment and Forests, India.

Hirose HM, T Akiyama, H Imahori, H Kasaki, S Kumano, H Kobayasi, E Takahashi, T Tsumura, M Hirano and T Yam- agishi. 1977. Illustrations of the Japanese freshwater algae.

Uchidarokakugo Publishing Co., Ltd., Tokyo.

John DM, BA Whitton and AJ Brook. 2011. The freshwater algal flora of the British Isles. An identification guide to freshwater and terrestrial algae. Second edition. Cambridge University Press, Cambridge.

Karosiene J and J Kasperoviciene. 2009. Filamentous epiphy- ton cyanobacteria(Oscillatoriales, Nostocales) new to algal flora of Lithuanian freshwater. Bot. Lithuanica 15:79-91.

Kim BC, EK Kim, DJ Pyo, HD Park and WM Heo. 1995. Tox- ic Cyanobacterial Blooms in Korean Lakes. J. Kor. Soc.

Water Quality 11:231-237(in Korean).

Kim HS. 2015. National list of species of Korea(Blue-green Algae). Jeonghang Publish. Co., Seoul.

Komárek J and K Anagnostidis. 2005. Cyanoprokaryota. 2.

Oscillatoriales. Süsswasserflora von Mitteleuropa 19/2.

Spektrum Akademischer Verlag, Heidelberg.

Komárek J, J Kastovsky, J Mares and JR Johansen. 2014. Tax- onomic classification of cyanoprokaryotes(cyanobacterial genera) 2014, using a polyphasic approach. Preslia 86:295- 335.

Matula J, M Pietryka, D Richter and B Wojtun. 2007. Cyano- prokaryota and algae of Arctic terrestrial ecosystems in the Hornsund area, Spitsbergen. Pol. Polar Res. 28:283-315.

Maulood BK, FM Hassan, AA Al-Lami, JJ Toma and AM Is- mail. 2013. Checklist of algal flora in Iraq. Baghdad. pp.

1-94. Ministry of Environment, Iraq.

Medvedeva LA and TV Nikulina. 2014. Catalogue of freshwa- ter algae of the southern part of the Russian Far East. pp.

1-271. Vladivostok. Dalnauka.

Phang SM, HY Yeong, ET Ganzon-Fortes, K Lewmanomont, A Prathep, LN Hau, GS Gerung and KS Tan. 2016. Ma- rine algae of the South China Sea bordered by Indonesia, Malaysia, Philippines, Singapore, Thailand and Vietnam.

Raffles Bull. Zool. Suppl. 40:13-59.

Prescott GW. 1982. Algae of the Western Great Lakes area.

WC Brown Company Publishers, USA.

Robarts RD and T Zohary. 1987. Temperature effects on photosynthetic capacity, respiration and growth-rates of bloom-forming cyanobacteria. N. Z. J. Mar. Freshwater Res. 21:391-399.

Rodriguez PL, H Pizarro, N Maidana, DS Afonso and SM Bonaventura. 2006. Epixylic algae from a polluted lowland river of Buenos Aires province(Argentina). Cryptogam.

Algol. 27:63-83.

Saadoun I, KK Schrader and WT Blevins. 2001. Identification of geosmin as a volatile metabolite of Anabaena sp. J. Ba- sic Microbiol. 41:51-55.

Sherwood AR. 2004. New records of freshwater macroalgae and diatoms from the Hawaiian Islands. Records of the

Hawaii biological Survey for 2003. Occasional Papers Ber- nice P. Bishop Museum 79:1-8.

Smith TE. 2010. Revised list of algae from Arkansas, U.S.A.

and new additions. Int. J. Algae 12:230-256.

Strunecky O, M Bohunická, JR Johansen, K Capková, L Raabová, P Dvorák and J Komárek. 2017. A revision of the genus Geitlerinema and a description of the genus Anag- nostidinema gen. nov.(Oscillatoriophycidae, Cyanobacte- ria). Fottea Olomouc 17:114-126.

Täuscher L. 2011. Checklisten und Gefährdungsgrade der Algen des Landes Brandenburg I. Einleitender Überblick, Checklisten und Gefährdungsgrade der Cyanobacteria/

Cyanophyta, Rhodophyta und Phaeophyceae/Fucophyceae.

Verhandlungen des Botanischen Vereins von Berlin und Brandenburg 144:177-192.

Täuscher L. 2014. Checkliste der Algen(Cyanobacteria et Phycophyta). pp. 44. In Bestandssituation der Pflanzen und Tiere in Sachsen-Anhalt. Natur und Text, Stuttgart.

Tell G. 1985. Catálogo de las algas de aguadulce de la Repúbli- ca Argentina. Bibliotheca Phycologica 70:1-283.

Turon X, M Hernández-Mariné and J Catalán. 1991. A new species of Komvophoron(Cyanophyta, Oscillatoriaceae) epibiont on ascidians from the Mediterranean Sea. Arch.

Hydrobio. 64:249-259.

Wehr JD and RG Sheath. 2003. Freshwater Algae of North America: Ecology and Classification. Academic Press, USA.

You KA, MS Byeon, SJ Youn, SJ Hwang and DH Rhew. 2013.

Growth Characteristics of Blue-green Algae(Anabaena spiroides) Causing Tastes and Odors in the North-Han River, Korea. Korean J. Ecol. Environ. 46:135-144(in Ko- rean).

Received: 20 August 2017 Revised: 13 September 2017 Revision accepted: 13 September 2017