FEATURE ARTICLE The Science of Seaweeds Marine macroalgae benefit people culturally, industrially, nutritionally, and ecologically.

Ole G. Mouritsen

acroalgae are, loosely of the calcium layer is precisely con- speaking, those that can trolled by the polysaccharides that are be seen with the naked present on their cell walls. eye. Most of them are Seaweeds, especially the brown al- Mclassified as benthic, which is to say gae, are generally made up of three that they fasten themselves to the sea- distinctly recognizable parts. At the bed. But there is no need to be so formal bottom there is a root-like structure, in talking about benthic macroalgae. the holdfast, which, as the name im- We commonly refer to them all the time plies, secures the organism to its habi- by the single term seaweeds, and we tat. It is usually joined by a stipe (or mcike use of them far more often than stem) to the leaf-like blades. The sea- most people reaUze. weed can have one or more blades, Macroalgae come in a great many and the blades can have different varieties. Some of the larger ones have shapes. In some cases, the blades have complex structures with special tissues a distinct midrib. Photosynthesis takes that provide support or transport nu- place primarily in the blades and it trients and the products of photosyn- is, therefore, important that the stipe thesis; others are made up of cells that is long enough to place them suffi- are all virtually identical. The smallest ciently close to the surface of the water seaweeds are only a few millimeters to reach the light. Some species have or centimeters in size, while the largest air-filled bladders, a familiar sight on routinely grow to a length of 30 to 50 bladder wrack, which ensure their ac- meters. Seaweed cells also come in dif- cess to light by holding them upright ferent sizes; in many species they can in the water. These bladders can be up measure one centimeter or more. These to 15 centimeters in diameter. Because large cells can contain several cell nuclei brown algae are so much like plants, and organelles in order to ensure that they are often confused with them. the production of proteins is sufficient Not all seaweeds share these struc- to sustain the function of the cell and the tures. Some smaller species have a tis- rapid growth of the seaweed as a whole. sue that has a less distinctive structure, Macroalgae are classified into three consisting only of filaments of cells, major groups: brown algae {Phaeophy- the brown ones are the largest. Even which may or may not be branched. ceae), green algae {Chlorophyta), and red though we talk about the three groups But almost all varieties have found algae {Rhodophyta). As all of the groups of seaweeds as if they were closely re- their place, one way or another, into contain chlorophyll granules, their lated, this is true only to a minor ex- the human diet. characteristic colors are derived from tent. For example, brown algae and red Originally, seaweeds intended for other pigments. Many of the brown algae belong to two different biological human consumption were collected algae are referred to simply as kelp. kingdoms and are, in a sense, less re- along the seashore or picked in the It is estimated that 1,800 different lated to each other than, for example, sea. Those that were eaten fresh were brown macroalgae, 6,200 red macroal- a jellyfish is to a bony fish. Green algae harvested locally and consumed in gae, and 1,800 green macroalgae are and red algae are more closely relat- short order. As seaweeds can be dried found in the marine environment. Al- ed to higher plants than brown algae though the red algae are more diverse. are and, together with diatoms, they evolved earUer than brown algae. Placing Hana-Tsunomata seaweed in cham- pagne {above) causes the frond to réhydrate Adapted with permission from Seaweeds: Edible, Most species of seaweeds have soft and unfold while dancing on the bubbles. Available, and Sustainable by Ole G. Mourit- tissues but some are, to a greater or A dried specimen of the red alga Claudea sen, published by the University of Chicago Press. lesser degree, calcified, an example be- elegans {opposite) is part of the collection of ©2013 Ole G. Mouritsen. AH rights reserved. ing calcareous red algae. The growth London's Natural History Museum.

458 American Scientist, Volume 101 www.americanscientist.org 2013 November-December 459 Nori is made from masses in the Sargasso Sea) secrete the macroscopic Blades also enormous quantities of slime, which large blades of the produce sperm ensures that the egg and sperm cells haploid generation cells. of Porptiyra. stick close to each other and do not go astray. The red alga Porphyra has an espe-. cially complicated life cycle, with a fascinating aspect that merits further discussion because of the interesting 2 It sheds history associated with its discovery. asexual ^ It relates directly to the cultivation of spores to Porphyra for the production of nori, reproduce, which is especially widely used in Jap- Haploid conchospores Blades also form and are released produce egg cells. anese cuisine—most familiarly, as for and deposited on a the wrapping for maki rolls. substrate. The blades used in nori produc- tion grow while the seaweed is in the Egg cells remain generation that reproduces sexually, on the blade where although the organism itself can actu- they can be Microscopic filamentous ally develop asexually from spores. fertilized by sperm organisms bore themseives cells, resulting in The blades produce egg cells and into the caicium shells of the release of a sperm cells. The egg cells remain on dead molluscs. zygote. the blades, where they are fertilized by the sperm cells. The fertilized eggs can then form a new type of spores, which The the red alga Porphyra, used for making Japanese nori, has a highly complex life cycle. are released. These spores germinate into a calcium-boring filament stage that can grow in the shells of dead bi- and, in that form, kept for a long time by fragmentation—that is, the blades valves, such as oysters and clams, in and transported easily, they were rec- shed small pieces that develop into the process developing spots that give ognized early on as a valuable food- completely independent organisms. the organism a pinkish sheen. stuff and became a trading commod- Asexual reproduction allows for Until the 1940s it was thought that ity. Over time, the fast propagation of this sexual stage was actually an en- demand for seaweeds, the species but car- tirely separate species of alga, given for a multiplicity of The life history ries with it an inherent the name Conchocelis rosea. Without an purposes, grew so danger of limited ge- understanding of the true life cycle, it great that for many netic variation. Sexual was not possible to grow Porphyra ef- centuries they have of algae is reproduction ensures fectively in aquaculture. No one knew been actively culti- better genetic varia- where the spores for the fully grown vated, especially in the complicated, tion, but it leaves the Porphyra originated. This was the Far East. species that depend and this is on this method of The Complex Life of reproduction with a Sea Green what really an enormous The life history of algae match-making T is complicated, and differentiates problem, as • ' this is what really dif- the egg and ferentiates them from them from sperm cells plants. In fact, macroal- need to find gae can pass through each other in life stages so distinct plants. water that is of- that, in the past, they ten turbulent. have been mistaken for separate spe- Some species solve the match- cies. Seaweed reproduction can involve making problem by equipping the either exclusively sexual or asexual reproductive cells with light-sensi- phases, while some species display an tive eyespots or with flagella so that alternation of generations that involves they can swim. Others make use both in succession. In the former, the of chemical substances, kpown as seaweed produces gametes (egg and pheromones or sex attractants. sperm cells) with a single set of chro- These are secreted and released A newly discovered mosomes and, in the latter, spores con- by egg cells and serve to attract species of red sea- taining two sets of chromosomes. Some the sperm. Some species (for weed is now named species can also reproduce asexually example, the large seaweed Porphyra migitae.

460 American Scientist, 'Volume 101 main reason for the recurring prob- Einally, after nine years' worth of the results were quickly put to use in lems experienced by the Japanese sea- effort to grow the alga in light- and Japan. Drew-Baker died at a relafively weed fishers in their attempts to culti- temperature-controlled tanks, she young age in 1957, apparently unaware vate Porphyra in a predictable manner. discovered that the spores would ger- that her curiosity and seminal research It was an English minate if they were had laid the foundafions for the devel- alga researcher. Dr. allowed to settle on a opment of the most valuable aquacul- Kathleen Mary Drew- Marine algae sterilized oyster shell. ture industry in the world. Baker, who discovered They would even the secret of the sexual are a much grow on an eggshell. A Lighting the Ocean Garden segment of the Porphy- few months later, the As in green plants, photosynthesis en- ra Ufe cycle. Drew-Bak- hetter source resulting small, rose- ables seaweeds to convert sunUght into er was unaware of the ate sprouts produced chemical energy, which is then bound difficulfies of the sea- of iron than their own spores that, by the formafion of the sugar glucose. weed fishers. Instead, in turn, could gerrrii- Glucose is the building block for the she was preoccupied nate and develop into seaweeds' carbohydrates and, at the with shedding Hght on foods such as the well-known large same time, an energy source for the the mystery of why the purple laver. producfion of other organic substanc- species of laver {Por- spinach and Drew-Baker pub- es that the seaweeds need in order to phyra umbilicalis) that lished her results in grow and to carry out life processes. grew around the coast egg yolks. 1949. Shortly thereafter The photosynthetic process uses up of England seemed the Japanese phycolo- carbon dioxide, which is thereby re- to disappear during gist Sokichi Segawa re- moved from the water. In addition, the summer, reappearing again only peated her experiments using local va- phosphorous, a variety of minerals, toward the end of autumn. She tried riefies of Porphyra and found that they and especially nitrogen are required. without success to germinate spores behaved in the same way as the EngUsh Oxygen is formed as a by-product, dis- that she had collected. species. The mystery was solved and solved in the water, and then released into the atmosphere. This by-product is of fundamental importance for those organisms that must, like humans, have oxygen to be able to breathe. Pho- Sea Vegetable Harvest in Maine tosynthesis can even, to a certain extent, be carried out when seaweeds are ex- • n 1971 Shep Erhart and his wife posed to air and parfially dehydrated. Linette began to harvest sea- During the night, when the light I:. weeds at Erenchman's Bay in level is low, photosynthesis stops and Maine, where they had settled af- the seaweeds begin to take in oxygen, ter giving up the idea of becoming burn glucose, and give off carbon di- farmers. They now run Maine Coast oxide. Under normal condifions, pho- Sea Vegetables, a company which tosynthesis is the dominant process, al- has its own building and 20 employ- lowing the seaweeds to build up their ees who transform the locally har- carbohydrate content. To the extent that vested seaweeds into more than 20 they have access to Ught in the water, different products. seaweeds actuaUy ufilize sunlight more The raw material for this busi- efficiently than terrestrial plants. Seaweed- ness is delivered by about 60 sea- The red macroalgae normally grow infused ice weed harvesters who work along at the greatest depths, typically as far as cream over the coasts of Maine and Nova Sco- 30 meters down, the green macroalgae lu I se tia, where algae are found in abun- thrive in shaUow water, and the brown dance. Shep trains the harvesters algae in between. This distribufion of himself. It is of utmost importance to him that they understand the prin- species according to the depth of the ciples of collecting the different types of marine algae sustainably so that water is somewhat imprecise, however; they do the least harm to the environment. a given species can be found at a loca- Maine Coast Sea Vegetables processes about 50 tons of dried seaweeds fion where there are opfimal condifions annually, of which about 60 percent is the dulse for which the company is with respect to substrate, nutritional especially famous. Eating dulse is an old tradifion in Maine, brought to its elements, temperature, and Ught. shores by settlers from Wales, Ireland, and Scotland. I have become a great In excepfionally clear water, one can fan of their applewood smoked dulse; I eat it as if it were candy. find seaweeds growing as far as 250 When dried dulse is brought to the factory, it is sorted by hand, and epi- meters below the surface of the sea. phytes, small crustaceans, and bivalves are picked off. The bone-dry dulse is It is said that the record is held by a placed in a sealed room to reabsorb some moisture and then left to ripen for calcareous red alga that was found at a a couple of weeks. During ripening, tlie seaweeds' enzymes tenderize the depth of 268 meters, where ordy 0.0005 blades so that they become softer and more flavorful. In tightly sealed pack- percent of the sunlight penetrates. ages, the chewy blades have a shelf life of about a year. — Ole G. Mouritsen Even though the waters at that depth 462 American Scientist, Volume 101 I may appear pitch-dark to human eyes, this is where an existing blade grows ganic carbon generated per square me- there is still sufficient light to allow and new blades are formed. The oldest ter on an annual basis. Macroalgae can the alga to photosynthesize. In turbid blades are outermost, eventually wear- produce between 2 and 14 kilograms, waters, seaweeds grow only in the top, ing down and falling off as the sea- whereas terrestrial plants, such as trees well-lit layers of water, if at all. weed ages. As a result, the stipe can be and grasses in temperate cUmates, and Formerly it was thought that sea- several years old, while the blades are microalgae can generate only about 1 weed species had adapted to their annuals. This growth mechanism al- kilogram. The vast productive capacity habitat by having pigments that were lows the seaweed to protect itself from of macroalgae can possibly be best illus- sensitive to the different wavelengths becoming overgrown by smaller algae, trated by the fact that the largest brown of the light spectrtim. In this way they called epiphytes, which fasten on to it. algae can grow up to half a meter a day. could take advantage of precisely that On certain seaweed species, the That amounts to a couple of centime- part of the spectrum that penetrated to epiphytes are found overwhelmingly ters an hour! the depths at which they lived. For ex- on the stipes, which can become cov- ample, the blue and violet wave- Underwater Dinner Harvest lengths reach greater depths. The Seaweeds are made up of a spe- red algae that live in these waters cial combination of substances, must contain pigments that ab- which are very different from sorb blue and violet light and, as the ones typically found in ter- a consequence, appear to have restrial plants and which allow the complementary color red. Ex- them to play a distinctive role in periments have since shown that human nutrition. Most notably, this otherwise elegant relation- the mineral content of seaweeds ship does not always hold true. is 10 times as great as that found Seaweed species that live at the Omelette (tamago-yaki) with Nori in plants grown in soil; as a con- ocean's surface may also contain 1 sheet of nori seaweed sequence, people who regularly pigments that protect them from 3 eggs eat seaweeds seldom suffer from the sun's ultraviolet light. mirin (sweet rice wine) mineral deficiencies. In addition, Given that all the substances salt and sugar marine algae are endowed with a that seaweeds need in order to 1. Crack the eggs into a bowl. Add a little salt, wide range of trace elements and survive are dissolved in the wa- sugar, and mirin (optional) and whisk every- vitamins. Because they contain a ter, macroalgae, unlike plants, thing together lightly with a fork. large volume of soluble and in- have no need of roots, stems, or soluble dietary fiber, which are real leaves. Nutrients and gases 2. Heat a pan that has been greased with a tiny either slightly, or else completely, are exchanged directly across the amount of fat, preferably one that has virtually indigestible, seaweeds also have surface of the seaweed by dif- no flavor of its own. a low calorie coimt. fusion and active transport. In 3. Pour the egg mixture into the pan a little at a Marine algae possess a fan- some species there is no mean- time over low heat. tastic ability to take up and con- ingful differentiation, and each 4. Place the nori sheet on the surface and, using centrate certain substances from cell draws its supply of nutrients chopsticks or a wooden spatula, fold the set seawater. For example, the iodine from the surrounding water. On egg mixture together on itself several times to concentration in konbu and other the other hand, specialized cell create a flat, layered omelette (tamago). types of kelp is up to 100,000 types and tissues that assist in the times as great in the cells of the 5. Remove the omelette from the pan and press distribution of nutrition within seaweeds as in the surrounding it into shape with a bamboo rolling mat, the organism can be found in a water, and the potassium con- which will imprint a nice surface texture on it. number of brown macroalgae. centration is 20-30 times greater. Access to nitrogen is an im- On the other hand, the sodium portant limiting factor in sea- content is appreciably lower than weed growth, particularly for green ered with them, while the blades re- that of salt water. Depending on the algae. The increasing runoff into the tain a smooth surface as long as they species, fresh seaweeds are 70-90 per- oceans of fertilizer-related nitrogen are young and still growing. Finally, cent water by weight. The composition from fields and streams has created some types of seaweeds, such as blad- of the dry ingredients in the different favorable conditions for the growth of der wrack {Fucus vesiculosus) and the types of seaweeds can vary a great deal, algae, especially during the summer majority of the red algae, grow at the but the approximate proportions are when it is warm and the days are long. extremities of the blades. about 45-75 percent carbohydrates and Different species of seaweeds avail The overall effect of seaweeds on fiber, 7-35 percent proteins, less than 5 themselves of a variety of strategies the global ecosystem is enormous. It is percent fats, and a large number of dif- in order to grow. In sea lettuce (Ulva estimated that all algae, including the ferent minerals and vitamins. lactuca), the cells all undergo division phytoplankton, are jointly responsible Broadly speaking, the proteins in more or less randomly throughout for producing 90 percent of the oxygen seaweeds contain all the important the organism. Other species, among in the atmosphere and up to 80 per- amino acids, especially the essential them several types of brown algae, cent of the organic matter on Earth. We ones that cannot be synthesized by our have a growth zone at the end of the can compare their output with that of bodies and that we therefore have to stipe and at the bottom of the blade; plants by looking at the amount of or- ingest in our food. Porphyra has the

www.americanscientist.org 2013 November-December 463 Soluble dietary fiber, which is situ- ated in between the seaweed cells and binds them together, constitutes up to 50 percent of the organism. Composed of three distinct groups of carbohy- drates, namely, agar, carrageenan, and alginate, fiber can absorb water in the human stomach and intestines and form gelatinous substances that aid in the digestive process. Insoluble dietary fiber derived from the stiff cell walls of the seaweeds is present in lesser quantities, typically amounting to be- tween 2 percent and 8 percent of the dry weight. Cellulose is found in all three types of algae and xylan (another type of complex carbohydrate) in the red and green ones. The primary mineral components in seaweeds are iodine, calcium, phospho- rous, magnesium, iron, sodium, potas- sium, and chlorine. Added to these are many important trace elements such as zinc, copper, manganese, selenium, molybdenum, and chromium. The mineral composition, especially, varies A wild strain of Chandrus crispus, or Hana-Tsunomata in Japanese, appeals to both the eye significantly from one seaweed species and the palate. This seaweed has a distinct crunchy texture and a milder taste than most other to anotlier. Konbu contains mote than sea vegetables. Its flamboyant colors—pink, green, and yellow—are completely natural. 100-1,000 times as much iodine as nori. On average, dulse—a widely eaten red greatest protein content (35 percent) in which we include sugar alcohols seaweed—is the poorest choice in terms and members of the order Laminari- such as mannitol in brown algae and of mineral and vitamin content but, on ales the lowest (7 percent). sorbitol in red algae, can constitute up the other hand, it is far richer in po- Three groups of carbohydrates are to 20 percent of the seaweeds. The sea- tassium salts than in sodium salts. In found in seaweeds: sugars, soluble di- weed cells make use of several types of general, marine algae are a much better etary fiber, and insoluble dietary fiber. starch-like carbohydrates for internal source of iron than foods such as spin- Many of these carbohydrates are dif- energy storage; again, these vary ac- ach and egg yolks. An abundance of vi- ferent from those that make up ter- cording to species. For example, the tamins is present in seaweeds, namely, restrial plants and, furthermore, they brown algae contain laminarin, which vitamins A, B (Bl, B2, B3, B6, B12, and vary among the red, the green, and the is of industrial importance as it can be folate), C, and E, but no vitamin D. brown species of algae. The sugars. fermented to make alcohol. Seaweeds contain iodine, although the exact quantities again vary greatly by species. The iodine content is depen- dent on where the seaweed grew and how it has been handled after harvest. Furthermore, the iodine is not evenly distributed, being most abundant in the growing parts and least plentiful in the blades. In particular, the brown sea- weeds contain large amounts of iodine. It is not known for certain why brown seaweeds contain so much iodine, but this is probably linked to their capac- ity for rapid growth. Recent studies of the brown seaweed species oarweed {Laminaria digitata) discovered high concentrations of inorganic iodine in the form of iodide (I") in the cell walls. Iodide was found to act as the main an- tioxidant for this tissue. In addition, the study showed that the action of iodide was not accompanied by an accumula- Norwegian winged kelp (Alaria esculenta) is appearing on the menus of top restaurants. tion of organically bound iodine.

464 American Scientist, Volume 101 The history of the discovery cause of what we often call "the of iodine as an element actually smell of the sea," but in large begins with seaweeds. Bernard quantities it results in the dis- Courtois (1777-1838), a French agreeable aroma that is associ- chemist, was working in his ated with rotten seaweeds and laboratory in 1811, extracting with fish that is no longer fresh. saltpeter from seaweeds for the DMS is the most abundant production of gunpowder for gaseous sulfur compound emit- Napoleon's army. He noticed ted into the Earth's atmosphere that his chemical experiments as a result of biological pro- with the seaweed ash gave rise Julie's Crispbread with Seaweeds cesses. When DMS is released to a violet-colored vapor that into the atmosphere, it, in tum, condensed as crystals on his cop- 1/2 cup rolled oats is oxidized to form particulate per vessels and, unfortunately, 1/2 cupflaxseed aerosol substances. These can caused them to corrode. Cour- 7 tbsp. sunflower seed cause condensation of water va- tois convinced first his French, 7 tbsp. pumpkin seed por, which brings about cloud and later his English, fellow 2 tsp. salt formation and thereby affects the chemists that his discovery had 1 cup flour weather. So although we may important dimensions. Their 1 tsp. baking powder find its odor offensive, many sci- work then rapidly led to the 4 tbsp. mixed seaweed granules (sea lettuce, entists think that the DMS gener- identification of the substance dulse, bullwhip kelp, giant kelp, mekabu) ated fiom the decomposition of that was the source of the va- 3/4 cup water marine algae, especially phyto- pors. It turned out to be a pre- 2 tbsp. grapeseed oil plankton, plays a vital role in the viously unknown element and, 1 In a bowl mix together the oats, seeds, sea- regulation of the Earth's climate. as the color violet is called iodes weeds, salt, and baking powder. When brown algae and some in Greek, the new element was types of red algae decay, they given the name iodine. Add water and mix well until the dough be- can cause the formation of an- Terrestrial plants are a poor comes sticky. other sulfurous gas, methyl source of iodine, which can Divide the dough into two and place one part mercaptan. This is the gas that result in iodine deficiency in on a piece of baking paper. smells like rotten cabbage and vegetarians and vegans. The On top of the dough add another piece of is often added to natural gas in accidental discovery of iodine baking paper and roll the dough out as thinly order to alert us to its presence. in seaweeds is a wonderful ex- as possible between the two. Conversely, fresh seaweeds, ample of how research and an With a knife or pizza wheel cut the top bak- much like a delightfully aromat- open mind on the part of the re- ing paper and divide the dough into squares ic ocean breeze, have a charac- searcher can lead to results that without cutting through the bottom paper. teristic, agreeable smell. In both have a major significance for the cases this is due to substances economy and for human health. Remove the top baking paper and place the called bromophenols, which the dough and the bottom paper on a baking seaweeds synthesize. They are Feast or Funk for the Senses sheet. released into the air and accu- Despite their importance to hu- Repeat the procedure with the other part of mulate in ocean-dwelling fish man diet, seaweeds have often the dough. and shellfish through their food been regarded with disdain. Bake the crispbread at 400° F for about 15-20 intake. The Roman poet Virgil is cred- minutes until golden brown. Because there are no bromo- ited with the saying that there After cooling a few minutes, the crispbread phenols in fresh water, fish that is nothing more worthless than can be broken along the scored lines. live in lakes and streams lack the washed-up seaweed: "nihil same pleasant odor and taste as vilior alga." He was absolutely their saltwater cousins. That is right insofar as dead, rotting yet one more way that seaweeds seaweeds give off a horrible stench. fimctions of the algae. DMSP accumu- contribute agreeably and meaningfully That unpleasant smell is due to a num- lates in those animals in the food chain to the human diet. ber of gases that are not dangerous, that feed on seaweeds. but are the source of odors that we DMSP has no taste and no smell, consider offensive. but dimethyl sulfide (DMS), a vola- One of the chief culprits is a chemi- tile gas that is a by-product of DMSP cal substance, dimethylsulfoniopro- breakdown, has a characteristic dis- For relevant Web links, consult this pionate (DMSP), which is foimd in red agreeable odor. It is formed when issue of American Scientist Online: and green algae, where it helps regu- DMSP is oxidized in the atmosphere late the osmotic balance of the cell in or when it is degraded by bacterial http://www.americanscientist.org/ relation to the surrounding salt water. action. It can also be released in the issues/id. 105/oast.asDx Some researchers think that DMSP is course of food preparation when fresh an important antioxidant, which pro- fish and shellfish are heated. When vides support for the physiological present in small quantities, DMS is the

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