Bangiales

Bangiales Temporal range: Stenian to present, Disputed Rafatazmia from late Statherian ~1047–0 Ma Pha. Proterozoic Archean Had.
Bangia spp.
Scientific classification
Clade:	Archaeplastida
Division:	Rhodophyta
Class:	Bangiophyceae
Subclass:	Bangiophycidae
Order:	Bangiales Nägeli, 1847
Families
†Rafatazmia? Bangiaceae Granufilaceae

Bangiales is an order of multicellular red algae of the class Bangiophyceae containing the families Bangiaceae, Granufilaceae,^[1] and possibly the extinct genus Rafatazmia with one species, Rafatazmia chitrakootensis.^[2] They are one of the oldest eukaryotic organisms, possibly dating back to 1.6 billion years old. Many species are used today as food in different cultures worldwide. Their sizes range from microscopic (Bangiomorpha) to up to two meters long (Wildemania occidentalis).^[3] Many of its species are affected by Pythium porphyrae, a parasitic oomycete.^[4][5][6][7] Similar to many other species of red algae, they reproduce both asexually and sexually. They can be both filamentous or foliose, and are found worldwide.^[8]

History

The first categorization of red algae currently placed inside Bangiales was the now-deprecated genus Phyllona by botanist John Hill in 1773. Bangiales itself was first categorized by Carl Nägeli in 1847. However, Bangiaceae had been categorized seventeen years prior in 1830 by Jean Étienne Duby and Bangia even earlier in 1819, by Hans Christian Lyngbye. Between 1819 and 1833, there were many discoveries by botanists like Carl Adolph Agardh and Gaillon; however many early genera were later deprecated and recategorized. No new discoveries were made until the late 19th century, where taxa such as Wildemania and Pyropia were discovered and classified. More modern discoveries include a new family (Granufilaceae) and several new genera, like Clymene, Neoporphyra, and Neothemis. As of 2024, the newest genus, Kuwaitiella, was discovered in 2022.^[1] Ongoing research continues to rearrange species, as recent genetic studies have revealed that many early morphologically classified genera were incorrect.^[9]

Human use

Sheets of nori.

Members of Bangiaceae, one of only two known living classes of Bangiales, are used to make laverbread, rong biển, edible seaweed, zǐcài, gim,^[10] and nori. Most edible farmed seaweeds within Bangiaceae are made from two genera of red algae, Porphyra and Pyropia. They are farmed in the ocean in countries including Ireland, the United Kingdom,^[11][12] Japan, Korea, and China.^[13] Pyropia is one of the most farmed seaweeds for human consumption.^[14] The farming of Pyropia species have been recorded as early as the 17th century, however industrial-scale farms only became common in the 1960s after the availability of artificial seed production and synthetic nets. Specifically, P. tenera and N. yezoensis are mainly used to make most edible seaweed products. Total Pyropia yields have reached three million tonnes as of 2020, with China contributing over three-quarters of the harvests.^[15] Pythium porphyrae, a parasitic oomycete, causes red rot disease or akasugare which severely harms seaweed farms in Japan and Korea. There are other pests to these organisms, including Olpidiopsis pyropiae, another oomycete. These diseases cause over US$10 million annually in damages to Pyropia harvests and Pythium porphyrae alone may cause crop losses of up to 20%. Pythium porphyrae has only been naturally observed infecting two species in Bangiales: Pyropia plicata and Neopyropia yezoensis.^[16] However, Diehl et al. (2017) have found that the parasite can successfully infect other Pyropia and Porphyra species.^[6] Some Porphyra species can be used to make biomaterials for biomedicines.^[17] Despite the foliose algae being the most commonly farmed species, the filamentous algae are also sometimes consumed. Both types of consumed algae have nutritional value;^[18] nori contains nutrients including proteins, vitamins (especially Vitamin A, Vitamin B1, Vitamin B2, and Vitamin C), minerals (including potassium, calcium, magnesium, iron, and zinc), and fibers.^[19] Many seaweed products contain high amounts of heavy elements like iodine and iron,^[20] along with toxic elements including cadmium and arsenic.^[21] Despite their classification as red algae, the edible species will turn green when prepared. This is evident in products like gim.^[22]

Description

A specimen of Bangia fuscopurpurea, a filamentous species, from the New York Public Library.

As of 2011, there are seven filamentous genera and eight foliose genera, however this has since been increased to fourteen foliose genera.^[23][1][9]

Filamentous genera

Filamentous red algae have thin strands. Generally, the filamentous species are much smaller; Bangia's filaments are only a few micrometers thick.^[24] The largest filamentous species can grow up to 35 centimeters of length.^[25] Despite their small size and thin thalli, they are commercially used as food in East Asian cultures, where they can be known as "红毛菜" (hóng máo cài).^[18] They include Bangia, Dione, Kuwaitiella, Minerva, Pseudobangia, Granufilum (in Granufilaceae), and the extinct Bangiomorpha.

Foliose genera

The foliose species are similar to large, extremely flat sheets of paper. They are one cell thick, and are most widely used in human consumption due to their macroscopic size and easier accessibility.^[26] They are also called the "bladed" algae, referring to their extreme thinness.^[27] They include Boreophyllum, Clymene, Fuscifolium, Lysithea, Miuraea, Neomiuraea, Neoporphyra, Neopyropia, Neothemis, Phycocalidia, Porphyra, Pyropia, Uedaea, and Wildemania.

Distribution

These red algae are found globally in rivers and oceans.^[28] Oceanic species are generally littoral, living near the shore in shallow water or in the intertidal zones.^[29] Some species of genera including Porphyra grow on coastal rocks.^[30] They are common in temperate areas such as the British Isles, Japan, Korea, and New Zealand,^[31] with New Zealand alone hosting over 30 species.^[6] Some species, like Wildemania spp., prefer cold water,^[32] while other genera, like Phycocalidia, prefer tropical zones.^[33]

Reproduction

Red algae of the order Bangiales undergo an unusual triphasic haploid-diploid life cycle; they can alternate between sexual and asexual reproduction. The distinction is primarily caused by environmental factors.^[34] They were originally proposed to have two phases in its life cycle, the diploid sporophyte and the haploid gametophyte. The sporophyte stage releases spores into the environment which then grow into full-sized algae, while the gametophyte stage requires two parents to undergo sexual reproduction which leads to the sporophyte stage again. However, these algae were recently discovered to undergo a third, diploid phase of life cycle known as the conchosporophyte. The conchosporophyte is parasitically grown on the sporophyte, and is thus an asexual manner of reproduction which results in an exact copy of its parent's genome. The conchosporophyte was previously believed to be part of the sporophyte, however modern research suggests otherwise. Despite the phylogenetic differences of the filamentous and foliose algae, both types reproduce in this manner.^[8][35]

Taxonomy

Bangiales includes two families and possibly Rafatazmia, for a total of 20 to 22 genera in Bangiaceae, 1 in Granufilaceae, and 1 incertae sedis. Traditionally, Bangiaceae only contained two genera, the filamentous Bangia and the foliose Porphyra.^[27] In 2011, there were 15 genera and 185 species, however a large reanalysis in 2020 reorganized many genera which brings the total to 22 to 24 as of 2024.^{[36][37][23][1]}

Bangiaceae

Pyropia plicata, a species of the genus Pyropia that lives in the intertidal zone.

Bangiomorpha pubescens

• Bangia Lyngbye
• †Bangiomorpha N.J.Butterfield
• Boreophyllum S.C.Lindstrom, N. Kikuchi, M.Miyata, & Neefus
• Clymene W.A.Nelson
• Dione W.A.Nelson
• Fuscifolium S.C.Lindstrom
• Kuwaitiella A.H.Hasan, P.Van der Aa, F.C.Küpper, D.Al-Bader & A.F.Peters, 2022
• Lysithea W.A.Nelson
• Minerva W.A.Nelson
• Miuraea N.Kikuchi, S.Arai, G.Yoshida, J.A.Shin, & M.Miyata
• Neomiuraea N.Kikuchi, S.Arai, G.Yoshida, J.A.Shin & Miyata, 2018
• Neoporphyra J.Brodie & L.-E.Yang, 2020
• Neopyropia J.Brodie & L.-E.Yang, 2020
• Neothemis A.Vergés & N.Sánchez
• Phycocalidia Santiañez & M.J.Wynne, 2020
• Porphyra C.Agardh
• Porphyrea? Solier (uncertain status)
• Pseudobangia K.M.Müller & R.G.Sheath
• Pyropia J.Agardh
• Spermogonia? Bonnemaison (uncertain status)
• Uedaea J.Brodie & L.-E.Yang, 2020
• Wildemania De Toni

Granufilaceae

• Granufilum X.F.Zhao, 1995

• Granufilum rivulare X.F.Zhao, 1995

Incertae sedis

• †Rafatazmia? Bengtson, 2017

• †Rafatazmia chitrakootensis? Bengtson, 2017

Records

If Rafatazmia is confirmed to be included in this order, then it would contain the oldest confirmed multicellular eukaryotic organism, dating to around 1.6 billion years during the Statherian period of the Paleoproterozoic era.^[38] In addition, Bangiomorpha is an extinct genus of algae in Bangiaceae containing one species, Bangiomorpha pubescens, which was the first confirmed organism to undergo sexual reproduction approximately one billion years ago during the Stenian period.^[39] Modern record-holders include Porphyra purpurea, with 251 genes comprising one of the largest known plastid genomes,^[40] and Pyropia tenera, as the globally second-most-farmed seaweed only behind the brown algae Saccharina japonica.^[41]

References

1. Michael D. Guiry (2024). "Bangiales Nägeli, 1847". WoRMS. World Register of Marine Species. Retrieved 20 February 2024.
2. Azmi, R.J. (1998). "Discovery of Lower Cambrian small shelly fossils and brachiopods from the Lower Vindhyan of Son Valley, Central India". Journal of the Geological Society of India. 52 (4).
3. Fretwell, Kelly. "Wildemania occidentalis, formerly Porphyra occidentalis". Biodiversity of the Central Coast. Retrieved 18 March 2024.
4. Spencer, M. A. (2004). "Pythium porphyrae. (Descriptions of Fungi and Bacteria)". IMI Descriptions of Fungi and Bacteria. 162 (Sheet 1617). Retrieved 10 October 2017. A description is provided for Pythium porphyrae. Information is included on the disease caused by the organism, its transmission, geographical distribution, and hosts. DISEASES: Red-rot disease, red-wasting disease. HOSTS: Bangia atropurpurea, Callophyllis adhaerens, Polyopes affinis (syn
5. Arasaki, Satoshi (1947). "アサクサノリの腐敗病に關する研究" [Studies on the Wasting Disease of the Cultured Lavers (Porphyra tenera)]. Nippon Suisan Gakkaishi (Bulletin of the Japanese Society of Scientific Fisheries) (in Japanese). 13 (3): 74–90. doi:10.2331/suisan.13.74.
6. Diehl, Nora; Kim, Gwang Hoon; Zuccarello, Giuseppe C. (March 2017). "A pathogen of New Zealand Pyropia plicata (Bangiales, Rhodophyta), Pythium porphyrae (Oomycota)". Algae. 32 (1): 29–39. doi:10.4490/algae.2017.32.2.25.
7. Takahashi, Minoru; Ichitani, Takio; Sasaki, Minoru (1977). "ノリ赤腐病を起因するPythium porphyrae" [Pythium porphyrae sp. nov. causing red rot of marine algae Porphyra spp.]. Transactions of the Mycological Society of Japan. 18 (3): 279–285.
8. Mikami, Koji; Takahashi, Megumu (January 2023). "Life cycle and reproduction dynamics of Bangiales in response to environmental stresses". Seminars in Cell & Developmental Biology. 134: 14–26. doi:10.1016/j.semcdb.2022.04.004. PMID 35428563.
9. Hasan, Amal Hajiya; Van der Aa, Pierrot; Frithjof C., Küpper; Al-Bader, Dhia; Peters, Akira F. (28 July 2022). "Kuwaitiella rubra gen. et sp. nov. (Bangiales, Rhodophyta), a new filamentous genus and species from the north-western Indian Ocean". Phycological Research. 70 (4): 192. doi:10.1111/pre.12498. hdl:2164/19385.
10. "홍조류" [Red algae]. Global World Encyclopedia (in Korean). Vol. 13. Beomhan. 2004. ISBN 89-8048-326-0 – via Wikisource.
11. Kain, J.M. 1991. Cultivation of attached seaweeds. in Guiry, M.D. and Blunden, G. 1992. Seaweed Resources in Europe: Uses and Potential. John Wiley and Sons, Chichester ISBN 0-471-92947-6
12. Hardy, F.G. and Guiry, M.D. 2006. A Check-list and Atlas of the Seaweeds of Britain and Ireland. British Phycological Society, London. ISBN 3-906166-35-X
13. Niwa, Kyosuke (November 2020). "Molecular evidence of allodiploidy in F1 gametophytic blades from a cross between Neopyropia yezoensis and a cryptic species of the Neopyropia yezoensis complex (Bangiales, Rhodophyta) by the use of microsatellite markers". Aquaculture Reports. 18: 100489. doi:10.1016/j.aqrep.2020.100489.
14. Reynolds, Daman; Caminiti, Jeff; Edmundson, Scott; Gao, Song; Wick, Macdonald; Huesemann, Michael (12 July 2022). "Seaweed proteins are nutritionally valuable components in the human diet". The American Journal of Clinical Nutrition. 116 (4): 855–861. doi:10.1093/ajcn/nqac190. PMID 35820048.
15. "Pyropia spp". Seaweed Insights. 2022. Archived from the original on 1 December 2023. Retrieved 28 March 2024.
16. Dumilag, Richard V. (September 2019). "Detection of Pythium porphyrae infecting Philippine Pyropia acanthophora based on morphology and nuclear rRNA internal transcribed spacer sequences". Journal of General Plant Pathology. 85 (1): 72–78. Bibcode:2019JGPP...85...72D. doi:10.1007/s10327-018-0815-2.
17. Iqbal, Khushboo; Chaudhary, Anchal; Sharma, Sandhya; Varma, Ajit; Thakur, Indu Shekhar; Mishra, Arti (2022). "Algae-based biomaterials for biomedicines". Algae-Based Biomaterials for Sustainable Development. pp. 251–276. doi:10.1016/B978-0-323-96142-4.00003-8. ISBN 978-0-323-96142-4.
18. Cao, Min; Wang, Dongmei; Mao, Yunxiang; Kong, Fanna; Bi, Guiqi; Xing, Qikun; Weng, Zhen (14 December 2017). "Integrating transcriptomics and metabolomics to characterize the regulation of EPA biosynthesis in response to cold stress in seaweed Bangia fuscopurpurea". PLOS ONE. 12 (12): e0186986. Bibcode:2017PLoSO..1286986C. doi:10.1371/journal.pone.0186986. PMC 5730106. PMID 29240755.
19. "About Seaweed". Nagai Nori Co., Ltd. 2015.
20. "Laver nori". www.hospitalityinfocentre.co.uk. Archived from the original on 3 November 2013. Retrieved 20 February 2024.
21. Bito T, Teng F, Watanabe F (2017). "Bioactive Compounds of Edible Purple Laver Porphyra sp. (Nori)". J Agric Food Chem (Review). 65 (49): 10685–10692. Bibcode:2017JAFC...6510685B. doi:10.1021/acs.jafc.7b04688. PMID 29161815.
22. "laverbread – WalesOnline". www.walesonline.co.uk. Retrieved 10 August 2008.
23. Sutherland; et al. (October 2011). "A New Look at an Ancient Order: Generic Revision of the Bangiales (Rhodophyta)". J. Phycol. 47 (5): 1131–1151. Bibcode:2011JPcgy..47.1131S. doi:10.1111/j.1529-8817.2011.01052.x. PMID 27020195. S2CID 2779596.
24. Wehr & Sheath 2003, p. 918.
25. Wehr & Sheath 2003, p. 197–224.
26. Wells, Emma (2010), A Field Guide to the British Seaweeds, National Marine Biological Analytical Quality Control Scheme (p 24) Archived 27 March 2012 at the Wayback Machine.
27. Reddy, Maggie M.; De Clerck, Olivier; Leliaert, Frederik; Anderson, Robert J.; Bolton, John J. (15 January 2018). "A rosette by any other name: species diversity in the Bangiales (Rhodophyta) along the South African coast". European Volume of Phycology. 53 (1): 67. Bibcode:2018EJPhy..53...67R. doi:10.1080/09670262.2017.1376256.
28. Nelson, W. A. (2013). New Zealand seaweeds : an illustrated guide. Wellington, New Zealand: Te Papa Press. p. 140. ISBN 9780987668813. OCLC 841897290.
29. Hardy, F.G. and Guiry, M.D. 2003. A Checklist and Atlas of the Seaweeds of Britain and Ireland. British Psychological Society ISBN 0-9527115-16
30. "Algaebase :: Species Detail". www.algaebase.org. Retrieved 21 February 2024.
31. Brodie, J.A. and Irvine, L.M. 2003. Seaweeds of the British Isles. Volume 1 Part 3b. The Natural History Museum, London.ISBN 1 898298 87 4
32. Mols-Mortensen 2014, p. x.
33. Kavale, Monica Gajanan; Kazi, Mudassar Anisoddin; Brodie, Juliet (18 January 2021). "Phycocalidia species (Bangiales, Rhodophyta), from the warm West Coast of India". European Journal of Phycology. 56 (3): 337. Bibcode:2021EJPhy..56..337K. doi:10.1080/09670262.2020.1829714.
34. Necchi Jr, Orlando, ed. (2016). River Algae. p. 73. doi:10.1007/978-3-319-31984-1. ISBN 978-3-319-31983-4.
35. Mikami, Koji; Li, Chengze; Irie, Ryunosuke; Hama, Yoichiro (7 August 2019). "A unique life cycle transition in the red seaweed Pyropia yezoensis depends on apospory". Communications Biology. 2 (2 ed.): 299. doi:10.1038/s42003-019-0549-5. PMC 6685973. PMID 31396579.
36. Guiry, M.D. & Guiry, G.M. 2018. AlgaeBase. World-wide electronic publication, National University of Ireland, Galway. http://www.algaebase.org/browse/taxonomy/?id=5183 Archived 20 August 2018 at the Wayback Machine ; searched on 20 February 2024.
37. Zhao, X.F. "Granufilum rivulare X.F.Zhao, 1995". WORMS. AlgaeBase. Retrieved 20 February 2024.
38. Bengtson, Stefan; Sallstedt, Therese; Belivanova, Veneta; Whitehouse, Martin (2017). "Three-dimensional preservation of cellular and subcellular structures suggests 1.6 billion-year-old crown-group red algae". PLOS Biology. 15 (3): e2000735. doi:10.1371/journal.pbio.2000735. PMC 5349422. PMID 28291791.
39. Gibson, Timothy M.; Shih, Patrick M.; Cumming, Vivien M.; Fischer, Woodward W.; Crockford, Peter W.; Hodgskiss, Malcolm S.W.; Wörndle, Sarah; Creaser, Robert A.; Rainbird, Robert H.; Skulski, Thomas M.; Halverson, Galen P. (February 2018). "Precise age of Bangiomorpha pubescens dates the origin of eukaryotic photosynthesis". Geology. 46 (2): 135–138. Bibcode:2018Geo....46..135G. doi:10.1130/G39829.1.
40. Page 878 in Higgs, David C. (2009). "The Chloroplast Genome". The Chlamydomonas Sourcebook. pp. 871–891. doi:10.1016/B978-0-12-370873-1.00032-0. ISBN 978-0-12-370873-1.
41. Zhang, Lishu; Liao, Wei; Huang, Yajun; Wen, Yuxi; Chu, Yaoyao; Zhao, Chao (13 October 2022). "Global seaweed farming and processing in the past 20 years". Food Production, Processing and Nutrition. 4 (23): 2. doi:10.1186/s43014-022-00103-2.

Sources

• Mols-Mortensen, Agnes (2014). The foliose Bangiales (Rhodophyta) in the northern part of the North Atlantic and the relationship with the North Pacific foliose Bangiales – diversity, distribution, phylogeny and phylogeography (Thesis).
• Wehr, John D.; Sheath, Robert G., eds. (2003). Freshwater Algae of North America. doi:10.1016/B978-0-12-741550-5.X5000-4. ISBN 978-0-12-741550-5.