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Page 1 of 43 European Journal of Phycology 1 2 3 4 5 6 7 Advancing the taxonomy of economically important red seaweeds (Rhodophyta) 8 9 Phaik-Eem Lim a, Li-En Yang b, Ji Tan c, Christine A. Maggs d and Juliet Brodie e Formatted: English (U.K.) 10 11 Formatted: English (U.K.) 12 Formatted: English (U.K.) 13 Formatted: English (U.K.) 14 aInstitute of Ocean andFor Earth Sciences Peer (IOES), Unive rsityReview of Malaya, 50603 Kuala Only Lumpur, 15 Malaysia. 16 b 17 Jiangsu Marine Fisheries Research Institute, Nantong, Jiangsu 226007, China. 18 cDepartment of Agricultural and Food Sciences, Universiti Tunku Abdul Rahman (UTAR), 19 20 31900 Kampar, Perak, Malaysia. 21 dFaculty of Science and Technology, Bournemouth University, Talbot Campus, Poole, 22 23 Dorset, BH12 5BB, UK. 24 eNatural History Museum, Department of Life Sciences, Cromwell Road, London, SW7 25 5BD, UK. 26 27 28 29 30 Contact: Phaik-Eem Lim, email: phaikeem@um.edu.my Formatted: English (U.K.) 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 1 58 59 60 URL: http:/mc.manuscriptcentral.com/tejp Email: ejp@nhm.ac.uk European Journal of Phycology Page 2 of 43 1 2 3 4 5 6 7 8 Abstract 9 10 11 The cultivation of red seaweeds for food (nori), agar and carrageenans is the basis of a Formatted: Level 1, Indent: 12 First line: 0", Adjust space valuable industry. However, taxonomic knowledge of these cultivated seaweeds and their between Latin and Asian text, 13 Adjust space between Asian text 14 wild relatives has notFor kept pace with Peer advances in molecular Review systematics despite the Only and numbers 15 fundamental importance of being able to identify commercially important species and strains, 16 17 discover cryptic and endemic taxa and recognize non-native species with potentially 18 damaging diseases and epiphytes. This review focuses on molecular taxonomic advances in 19 20 the cultivated red algae with the highest commercial value globally: Eucheuma , 21 Kappaphycus , Porphyra sensu lato Porphyra /Pyropia and Gracilaria . All four genera are 22 23 similarly taxonomically challenging. They are speciose, morphologically plastic, have poorly 24 resolved species boundaries, and a stable taxonomy for each genus is yet to be achieved. 25 Eucheuma and Kappaphycus are frequently misidentified and the molecular markers cox 2-3 26 27 spacer, cox 1 and RuBisCO spacer have helped to in understand ing phylogenetic 28 relationships , and identify ing new species and haplotypes. In Porphyra sensu lato (Bangiales) 29 30 species identification and phylogenetic relationships were highly problematic until a major 31 taxonomic revision based on a two-gene phylogeny (18S and rbc L) resulted in nine genera of 32 33 bladed species. Pyropia , with at least 89 species, three in nori cultivation, has potential for 34 new commercial evaluation. The recently published Porphyra genome will aid the Formatted: Font: Italic 35 36 exploration of evolutionary relationships in this group. In Gracilaria sensu lato , earlier 37 efforts to resolve species-level taxonomy and generic descriptions were superseded by 38 application of molecular tools, including DNA sequences of the RuBisCO spacer, rbc L gene, 39 40 18S and the ITS region. Relationships between clades are now fairly well established, but 41 much research on species and genera is still needed. Studies of these cultivated red algal 42 43 genera highlight the need for a robust taxonomy, a more standardized approach to the 44 molecular markers used and a comprehensive dataset for each representative species. 45 46 RecentCurrent work on DNA-based species delimitation, the emergence of high throughput 47 sequencing , multi-gene phylogenies and publication of whole genomes (e.g. Porphyra 48 Formatted: Font: Italic 49 umbilicalis ) and the large number of genomes in the pipeline (e.g. Gracilaria ) is increasingly 50 improving our understanding of phylogenomic relationships and hence a better understanding 51 of species relationships. This knowledge, in turn, can then be applied to improving red 52 53 seaweed aquaculture. 54 55 56 57 2 58 59 60 URL: http:/mc.manuscriptcentral.com/tejp Email: ejp@nhm.ac.uk Page 3 of 43 European Journal of Phycology 1 2 3 4 5 6 7 Keywords : agar, Bangiales, carageenans, commercial value, Gracilariaceae, molecular 8 taxonomy, Solieraceae 9 10 11 12 13 14 For Peer Review Only 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 3 58 59 60 URL: http:/mc.manuscriptcentral.com/tejp Email: ejp@nhm.ac.uk European Journal of Phycology Page 4 of 43 1 2 3 4 5 6 7 Introduction 8 9 Red seaweeds have been collected from the wild for food and other products for thousands of 10 11 years (Tseng, 1935 , ; Brodie & Irvine, 2003; Collén et al. , 2014; Ramirez et al. , 2014 and 12 references therein). The main uses of red algae, apart from food, have been as a source of the 13 14 gelling hydrocolloidsFor agar and carrageenan Peer (Craigie , 1990).Review Until the Second World Only War 15 (WWII, 1939-1945), seaweeds were mostly harvested from natural populations (Marshall et 16 17 al., 1949), although Porphyra sensu latoPorphyra has been cultivated in China and Japan for 18 hundreds of years as food (Blouin et al. , 2011; Yang et al. , 2017). After WWII, in Asia the 19 20 need for a more reliable crop after a major failure of the nori harvest in Japan led to the 21 development of the modern nori industry (Yang et al. , 2017). Growing demand for products 22 th 23 over the second half of the 20 century (e.g. Marshall et al. , 1949; Kim, 2012) saw a 24 fundamental shift from wild harvesting in the North Atlantic of e.g.species including 25 Chondrus crispus in the North Atlantic to farmed crops, such as Eucheuma in warmer 26 27 tropical areas, particularly in the Pacific (Doty et al. , 1987). A more recent drive towards the 28 development and commercialization of functional foods, nutriceuticals, pharmaceuticals and 29 30 bioactives from seaweeds is pushing up demand and leading to innovative methods of 31 production (e.g. Hafting et al. , 2011; Gutierrez Cuesta et al. , 2016). Current research 32 33 indicates that macroalgal proteins contain all essential amino acids for food products and 34 have additional bioactives (Garcia-Vaquero & Hayes, 2016). 35 36 Despite the fundamental shift in the production and supply of red seaweeds and the 37 range of taxonomic tools now available, relatively little attention has been given to the 38 molecular taxonomy of species under cultivation. In general, the application of molecular 39 40 techniques in red algal taxonomy has revolutionized species concepts and taxonomic 41 relationships, uncovered cryptic diversity (Robba et al. , 2006; Diaz-Tapia et al. , 2017) and 42 43 provided a greater understanding of species distributions in different geographical areas 44 (Brodie et al. , 2007), including evidence of much greater endemism than originally thought 45 46 based on morphological identification (Brodie et al. , 2008, Payo et al. , 2013). Molecular 47 analysis has also revealed that in many groups of red seaweeds there is considerable genetic 48 49 diversity that is not reflected in the morphology at the species level (e.g. Sutherland et al. , 50 2011; Saengkaew et al. , 2016). 51 Twelve red algal taxa are listed as currently in aquaculture production (FAO, 2015) 52 53 and/or have been cultivated for consumption between 1990 and 2015 (Table 1), although the 54 number and identity of many of these species are uncertain. The main taxa in cultivation are 55 56 57 4 58 59 60 URL: http:/mc.manuscriptcentral.com/tejp Email: ejp@nhm.ac.uk Page 5 of 43 European Journal of Phycology 1 2 3 4 5 6 7 species of Kappaphycus , Eucheuma , Porphyra sensu lato Pyropia (as Porphyra ) and 8 Gracilaria . Estimates of their wet weight harvest per continent are given in Table 2. Formatted: Not Highlight 9 However, the reliability of these data is questionable as the figures are based on reported 10 11 “output from aquaculture activities designated for final harvest for consumption ” (FAO, Formatted: Not Highlight 12 2015). (Table 2). For details of dry tonnage of agarophyte and carrageenophyte seaweeds 13 14 for 2009 and 201 56 seeFor also Porse &Peer Rudolph (2017). Review The main sources of carrageenan Only are Formatted: Not Highlight 15 Eucheuma denticulatum , Kappaphycus alvarezii and Kappaphycus striatum (Ask & Azanza, 16 17 2002; Aquaculture Compendium, 2006), with Eucheuma “cottonii” making up 73% of the Formatted: Not Highlight 18 world consumption ; (Porse & Rudolph, 2017). and aAgar from cultivated red seaweeds Formatted: Not Highlight 19 20 comes mostly from the genus Gracilaria not identified to species level (FAO, 2015; Porse & Formatted: Font: Not Italic 21 Rudolph, 2017). Gelidium hasyields agar of better quality than Gracilaria but it is not Formatted: Not Highlight 22 23 possible yet to grow it in cultivation and wild stocks have been severely over-exploited 24 (Porse & Rudolph, 2017). 25 Commercial marine seaweed cultivation is practiced heavily in the Asian Pacific 26 27 region, with China, Indonesia and the Philippines contributing up to 88.7% (21 million 28 tonnes) of the global farmed algal production in 2012 (FAO, 2014; Valderrama, 2015). The 29 30 largest producer of agarophytes and carrageenophytes is Indonesia (Porse & Rudolph, 2017). 31 The carrageenan-producing seaweeds Kappaphycus and Eucheuma make up approximately 32 33 33% of total algal production (FAO, 2014).