Miuraea migitae, a new record of the order Bangiales (Bangiophyceae, Rhodophyta) from Korea
© The Author(s) 2016
Received: 10 August 2016
Accepted: 5 November 2016
Published: 16 November 2016
We found specimens of foliose Bangiales from the subtidal zone of Udo, Jeju Island, Korea. In molecular analyses of rbcL sequences, these Korean specimens were almost identical to Miuraea migitae from Osaka, Japan. In the morphological comparison, Korean specimens were consistent with habitat, color, and vegetative characteristics with the description of M. migitae. This is the first record of M. migitae outside the type locality and Nagasaki in Japan.
This study confirms that new or unrecorded species of the order Bangiales may be discovered from subtidal habitats.
The order Bangiales (Nägeli 1874) is an order of distinctive and morphologically simple red algae that represents an ancient lineage (Butterfield 2000). The foliose Bangiales includes the most highly valued seaweeds grown in aquaculture from Korea, Japan, China, and Southeast Asia for the past several hundred years (Mumford and Miura 1988). This order has been considered monophyletic with the single family Bangiaceae. Traditionally, Bangia Lyngbye and Porphyra C. Agardh have been recognized on the basis of gametophyte morphology: unbranched uni- to multiseriate filaments in the genus Bangia and blade in the genus Porphyra (Oliveira et al. 1995). Recently, the revision of the order Bangiales, based on the phylogeny using nrSSU and rbcL genes, has greatly improved the taxonomic understanding of this group (Sutherland et al. 2011). According to Sutherland et al. (2011), the order Bangiales was split into eight of foliose (Boreophyllum, Clymene, Lysithea, Miuraea, Porphyra, Pyropia, and Wildemania) and seven of filamentous genera.
The genus Miuraea was established by Sutherland et al. (2011) based on molecular analyses and composed of only one species, M. migitae (N.Kikuchi, S.Arai, G.Yoshida & J.A.Shin) N.Kikuchi, S.Arai, G.Yoshida, J.A.Shin & M.Miyata. This species was originally described as Porphyra migitae, based on the specimen collected from Misaki town in Osaka Prefecture, Japan (Kikuchi et al. 2010). M. migitae was distinguished from other foliose Bangiales species by growing on the subtidal habitat and having fire red to pink color (Kikuchi et al. 2010). The distribution of M. migitae was reported only from Japan (Osaka and Nagasaki), attached to the dead bivalve shell and rope (Sutherland et al. 2011).
In Korea, the study of Porphyra has been carried out on morphology, physiology, flora, and culture by several authors (Hwang and Lee 2001; Kim and Kim 2011). To date, seven species of Porphyra and 13 species of Pyropia J.Agardh (previously known Porphyra from Korea) have been reported from Korea, mostly collected in the intertidal zone (Kim et al. 2013). Two species, Pyropia koreana (M.S. Hwang & I.K. Lee) M.S. Hwang, H.G. Choi, Y.S. Oh & I.K. Lee and Pyropia yezoensis (Ueda) M.S. Hwang & H.G. Choi, are known from subtidal habitats (Hwang and Lee 2001; Kim and Kim 2011). However, the specimens of the order Bangiales from subtidal habitats have been scarcely explored because of the difficulty of sampling in this environment, despite the possibility of discovering new or unrecorded species.
In this study, we collected foliose Bangiales specimens from a depth of 15 m in Udo, Jeju Island, Korea. We conducted morphological observations and rbcL sequence analysis in order to confirm the taxonomic position of these subtidal specimens. This is the first record of the occurrence of the order Bangiales species from under 15 m depth of subtidal habitats in Korean coasts.
Four samples were collected by SCUBA diving from a depth of 15 m of Udo (33° 30′ N, 126° 55′ E), Jeju Island, Korea, in 9 May 2015 (E15019) and 17 May 2016 (E16064, E16065, E16066). Thalli were mounted on herbarium sheets as voucher specimens. Some parts of thallus were cutoff to stain with 1% aqueous aniline blue acidified with a drop of 1% HCL and to make permanent slide in a solution of 50% Karo syrup for microscopic observations. Photomicrographs were taken with a Canon EOS 600D digital camera mounted on the Olympus BX43 microscope. Voucher specimens were deposited in the herbarium of Jeju National University, Korea (JNUB).
Genomic DNA was extracted from the specimens using the DNeasy Plant Mini Kit (Qiagen, Hilden, Germany) following the manufacturer’s instruction. The primer pairs for rbcL gene were rbcLJNF1-rbcLJNR1 and rbcLJNF2-rbcLJNR2 (Kang and Kim 2013). Amplification condition for rbcL consisted of 7 min at 97 °C for pre-denaturation, followed by 45 cycles of 1 min at 97 °C, 1 min 47 °C, and 2 min at 72 °C, with a final 7 min extension cycle at 72 °C, and a soak cycle at 4 °C. PCR products were purified using the AccuPrep® PCR Purification Kit (Bioneer, Daejeon, Korea) following the manufacturer’s instructions. Nucleotide sequences of rbcL were determined on strands of PCR amplification products at the Macrogen sequencing facility (Macrogen Inc., Seoul, Korea). The sequences were edited using Mega ver. 7.0.14 (Tamura et al. 2013), and multiple sequence alignments were constructed with 39 taxa of the order Bangiales from GenBank with two taxa of Hildenbrandiales as out-group.
Maximum likelihood (ML) analysis was conducted using RAxML software (Stamatakis 2006) with the GTR + I + Γ evolutionary model to confirm the taxonomic position of Korean specimens. We used 1000 independent tree inferences using the “-#” option to generate bootstrap values for phylogenetic analysis with the algorithm “a” of “-f” option to search the best-scoring tree in one program run. The other options were used as a default set of the software.
Miuraea migitae (N.Kikuchi, S.Arai, G.Yoshida & J.A.Shin) N.Kikuchi, S.Arai, G.Yoshida, J.A.Shin & M.Miyata
Basionym: Porphyra migitae N.Kikuchi, S.Arai, G.Yoshida & J.A. Shin
Type locality: Misaki town, Osaka Prefecture, Japan.
Holotype: SAP105477 (Kikuchi et al. 2010).
Korean name: Chambunhonggim (참분홍김).
To date, M. migitae has been only collected from the subtidal zone in Udo, Jeju Island, Korea. The habitat is an area in a strong current and is covered with sand and a rhodolith bed.
Miuraea migitae has been known as an endemic species in the subtidal zone of Japan. It is characterized by monostromatic thallus elliptic and obovate in shape, with fire red to pink color and 25 cm length × 13 cm width in size (Kikuchi et al. 2010). According to the culture study by Kikuchi et al. (2010), M. migitae can be distinguished from other subtidal species of Bangiales in Japan by the presence of asexual reproductive subcycles involving archeospores and neutral spores on the foliose thallus. Although our specimens were not observed any archeospores and neutral spores on thallus, Korean specimens were consistent with habitat, color, and vegetative characteristics in the description of M. migitae.
Morphological features of Miuraea migitae and five foliose Bangiales species having similar morphology or habitat from Korea
6–15-m depth of subtidal zone
Low intertidal zone
Low intertidal to 5-m depth of subtidal zone
Upper to middle intertidal zone
Middle intertidal to 5-m depth of subtidal zone
Fire red, pink
Yellowish brown, pale-green toward the base
Purple, greenish red, brownish red
Bright red, brownish red
Yellowish red, brownish red, greenish red
Brownish red, greenish red
Narrow elliptic, elliptic, obovate, circular
Elliptical, linear, lanceolate
Elliptical, round, ovate, obovate
Round, ovate, obovate, oblanceolate, reniform
Cordate, rotund, navel
Cuneate, round, cordate
Cuneate, round, cordate, umbilicate
Vegetative cell shape
Oblong, triangular, polygonal
Circle, rectangle, triangle
Vegetative cell size (μm)
8–17 × 6–10
7–11 × 6–9
12–15 × 7–10
13–17 × 9–10
15–21 × 9–12
13–19 × 7–14
Basal cell shape
Basal cell size (μm)
15–35 × 6–20
18–42 × 13–21
22–27 × 13–16
22–25 × 9–12
22–33 × 13–21
22–33 × 10–23
Projection of rhizoidal filaments
Division formula of spermatangia
4 × 4 × 8
4 × 2 × 8
4 × 2–4 × 4–8
4 × 2–4 × 4
4 × 2–4 × 4–8
4 × 2–4 × 8–16
Division formula of zygotosporangia
2 × 2 × 4
2 × 2 × 2–4
2 × 2 × 4
2 × 1 × 2
2–4 × 1–2 × 2–4
2 × 2 × 4
This study, Kikuchi et al. 2010
Kim and Kim 2011
The molecular analyses demonstrated that the rbcL sequences from Korean specimens and M. migitae from Japan (EU521643) were almost identical with 0.2% genetic distances. Lindstrom and Fredericq (2003) mentioned that the sequence divergences of rbcL within species of Porphyra from different populations differed by 0.1% in Porphyra fallax from British Columbia, Canada, to 0.9% in Porphyra pseudolanceolata and P. pseudolinearis from Alaska, USA. The sequence divergence between Korean and Japanese specimens fell into the intraspecific variation, showing the specimens to be conspecific. In the phylogenetic tree, Miuraea formed a clade with four genera, Pyropia, Wildemania, Boreophyllum, and Lysithea, without supporting value. These phylogenetic relationships were different from two previous studies: one is that the genus Miuraea formed a basal node of the order Bangiales except for two filamentous genera Dione and Minerva (Sutherland et al. 2011), in the other is that the genus Miuraea formed a sister clade composed of Boreophyllum, Fuscifolium, Pyropia, Wildemenia, and an undescribed filamentous genus (Sánchez et al. 2014). In addition, the taxonomic confusion still remained on the phylogenetic relationships of three genera, Porphyra, Bangia, and Clymene, even though they had moderate support value in the rbcL tree (Sutherland et al. 2011; Sánchez et al. 2014).
The new record of M. migitae from Korea extends the distribution range of this species previously restricted to only two localities, Osaka and Nagasaki in Japan (Guiry and Guiry 2016). Udo of Jeju Island is distant from the type locality of M. migitae, Osaka, Japan. Hwang (2008) mentioned that Udo had been connected with Osaka by shipping previously (before 1945). Although the origin of this species is unclear, this report indicated that this species might be occurred in Korea prior to that time. Lack of the records on the distribution of M. migitae from Udo before our finding might be due to the difficulty of collecting in its subtidal habitat where there are swift currents. Since the foliose thallus of M. migitae is growing up to 28 cm as the maximum length and producing asexual reproductive cells during summer season (Kikuchi et al. 2010), it can be a potential genetic resource for plant breeding to increase the production in seaweed aquaculture.
In conclusion, we collected the foliose Bangiales specimens from the subtidal zone of Udo, Jeju Island. Based on molecular and morphological analyses, these specimens were identified as M. migitae, previously considered endemic in Japan. This is a new record for Korea and indicates that collections from the subtidal zone are necessary to increase understanding of the biodiversity of seaweeds including potential genetic resources in Korea. In further studies, we are performing morphological and molecular investigations of the order Bangiales to understand the accurate phylogenetic relationships.
We thank all members of the Molecular Phylogeny of Marine Algae laboratory at Jeju National University for collecting the samples. This work was supported by a grant from the National Institute of Biological Resources (NIBR), funded by the Ministry of Environment (MOE) of Korea (NIBR201624202 for the Graduate Program of the Undiscovered Taxa from Korea).
Availability of data and materials
The sequences are available in the GenBank (http://www.ncbi.nlm.nih.gov/).
YHK carried out the research and drafted the manuscript. HWL collected the samples from the subtidal zone by SCUBA diving. MSK designed this study and revised the manuscript. All authors read and approved the final manuscript.
The authors declare that they have no competing interests.
Consent for publication
Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
- Butterfield NI. Bangiomorpha pubescens n. gen., n. sp.: implications for the evolution of sex, multicellularity, and the Mesoproterozoic/Neoproterozoic radiation of eukaryotes. Paleobiology. 2000;26:386–404. http://dx.doi.org/10.1666/0094-8373(2000)026<0386:BPNGNS>2.0.CO;2.View ArticleGoogle Scholar
- Guiry MD and Guiry GM. AlgaeBase. World-wide electronic publication, National University of Ireland, Galway. 2016. http://www.algaebase.org. Accessed 19 July 2016.
- Hwang KS. The searching and tourism resource plan of Jeju-Japan sea route before independence. J Korean Reg Dev Assoc. 2008;20:113–32.Google Scholar
- Hwang MS, Lee IK. Two species of Porphyra (Bangiales, Rhodophyta), P. koreana sp. nov. and P. lacerata Miura from Korea. Algae. 1994;9:169–77.Google Scholar
- Hwang MS, Lee IK. Taxonomy of the genus Porphyra (Bangiales, Rhodophyta) from Korea. Algae. 2001;16:233–73.Google Scholar
- Kang JC and Kim MS. A novel species Symphyocladia glabra sp. nov. (Rhodomelaceae, Rhodophyta) from Korea based on morphological and molecular analyses. Algae.2013;28:149–160. http://dx.doi.org/10.4490/alga.2013.28.2.149.
- Kikuchi N, Arai S, Yoshida G, Shin JA, Broom JE, Nelson WA, et al. Porphyra migitae sp. nov. (Bangiales, Rhodophyta) from Japan. Phys Chem Chem Phys. 2010;49:345–54. http://dx.doi.org/10.2216/09-82.1.Google Scholar
- Kim H-S and Kim S-M. Algal Flora of Korea. Vol. 4, No. 1, Rhodophyta: Stylonematophyceae, Compopogonophyceae, Bangiophyceae. Primitive red algae. National Institute of Biological Resources, Ministry of Environment, Incheon, Korea, 142 pp. 2011.Google Scholar
- Kim H-S, Boo SM, Lee IK and Son CH. National list of species of Korea. Marine Algae. National Institute of Biological Resources, Ministry of Environment, Incheon, Korea, 336 pp. 2013.Google Scholar
- Lindstrom SC, Fredericq S. rbcL gene sequences reveal relationships among north-east Pacific species of Porphyra (Bangiales, Rhodophyta) and a new species, P. aestivalis. Phycol. Res. 2003;51:211–24. http://dx.doi.org/10.1046/j.1440-1835.2003.00312.x.Google Scholar
- Mumford TF, Miura A. Porphyra as food: cultivation and economics. In: Lembi CA, Waaland JR, editors. Algae and human affairs. London: Cambridge University Press; 1988. p. 87–117.Google Scholar
- Nägeli C. Die neuern Algensysteme und Versuch zur Begründung eines eigenen Systems der Algae und Florideen. Schulthess, Zurich, Switzerland, 275 pp., pls I-X. 1874.Google Scholar
- Oliveira MC, Kurniawan J, Bird CJ, Rice EL, Murphy CA, Singh RK, et al. A preliminary investigation of the order Bangiales (Bangiophyceae, Rhodophyta) based on sequences of nuclear small-subunit ribosomal RNA genes. Phycol Res. 1995;43:71–9. http://dx.doi.org/10.1111/j.1440-1835.1995.tb00007.x.View ArticleGoogle Scholar
- Sánchez N, Vergés A, Peteiro C, Sutherland JE and Brodie J. Diversity of bladed Bangiales (Rhodophyta) in western Mediterranean: recognition of the genus Themis and descriptions of T. ballesterosii sp. nov., T. iberica and Porphyra parva sp. nov. J. Phycol. 2014;50: 908–929. http://dx.doi.org/10.1111/jpy.12223.
- Stamatakis A. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics. 2006;22:2688–90. http://dx.doi.org/10.1093/bioinformatics/btl446.View ArticlePubMedGoogle Scholar
- Sutherland JE, Lindstrom S, Nelson WA, Brodie J, Lynch MDJ, Hwang MS, et al. A new look at an ancient order: generic revision of the Bangiales (Rhodophyta). J Phycol. 2011;47:1131–51. http://dx.doi.org/10.1111/j.1529-8817.2011.01052.x.View ArticlePubMedGoogle Scholar
- Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Molec Biol Evol. 2013;30:2725–9. http://dx.doi.org/10.1093/molbev/mst197.View ArticlePubMedPubMed CentralGoogle Scholar