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Red algae

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Red algae
Temporal range: Mesoproterozoic–present[1]
A-D : Chondrus crispus Stackhouse,
E-F : Mastocarpus stellatus J.Ag.
Scientific classification Edit this classification
Clade: Diaphoretickes
Clade: CAM
Clade: Archaeplastida
Division: Rhodophyta
Wettstein, 1922

Classification is currently disputed. See Taxonomy.

The red algae, or Rhodophyta (/roʊˈdɒfɪtə/ roh-DOF-it-ə, /ˌroʊdəˈfaɪtə/ ROH-də-FY-tə; from Ancient Greek ῥόδον (rhodon) 'rose' and φυτόν (phyton) 'plant'), are one of the oldest groups of eukaryotic algae.[2] The Rhodophyta also comprises one of the largest phyla of algae, containing over 7,000 currently recognized species with taxonomic revisions ongoing.[3] The majority of species (6,793) are found in the Florideophyceae (class), and mostly consist of multicellular, marine algae, including many notable seaweeds.[3][4] Approximately 5% of the red algae occur in freshwater environments with greater concentrations found in the warmer area.[5] There are no terrestrial species, which is assumed to be traced back to an evolutionary bottleneck where the last common ancestor lost about 25% of its core genes and much of its evolutionary plasticity.[6]

The red algae form a distinct group characterized by having eukaryotic cells without flagella and centrioles, chloroplasts that lack external endoplasmic reticulum and contain unstacked (stoma) thylakoids, and use phycobiliproteins as accessory pigments, which give them their red color.[7] Red algae store sugars as floridean starch, which is a type of starch that consists of highly branched amylopectin without amylose,[8] as food reserves outside their plastids. Most red algae are also multicellular, macroscopic, marine, and reproduce sexually. The red algal life history is typically an alternation of generations that may have three generations rather than two.[9]

Chloroplasts evolved following an endosymbiotic event between an ancestral, photosynthetic cyanobacterium and an early eukarytoic phagotroph.[10] This event (termed primary endosymbiosis) resulted in the origin of the red and green algae, and the glaucophytes, which make up the oldest evolutionary lineages of photosynthetic eukaryotes.[11] A secondary endosymbiosis event involving an ancestral red alga and a heterotrophic eukaryote resulted in the evolution and diversification of several other photosynthetic lineages such as Cryptophyta, Haptophyta, Stramenopiles (or Heterokontophyta), Alveolata, Centrohelids, Katablepharids, and Telonemi.[11] In addition to multicellular brown algae, it is estimated that more than half of all known species of microbial eukaryotes harbor red-algal-derived plastids.[12]

The coralline algae, which secrete calcium carbonate and play a major role in building coral reefs, belong here. Red algae such as dulse (Palmaria palmata) and laver (nori/gim) are a traditional part of European and Asian cuisines and are used to make other products such as agar, carrageenans and other food additives.[13]

Unicellular members of the Cyanidiophyceae are thermoacidophiles and are found in sulphuric hot springs and other acidic environments,[14] an adaptation partly made possible by horizontal gene transfers from prokaryotes.[15] The remaining taxa are found in marine and freshwater environments. Most rhodophytes are marine with a worldwide distribution, and are often found at greater depths compared to other seaweeds. While this was formerly attributed to the presence of pigments (such as phycoerythrin) that would permit red algae to inhabit greater depths than other macroalgae by chromatic adaption, recent evidence calls this into question (e.g. the discovery of green algae at great depth in the Bahamas).[16] Some marine species are found on sandy shores, while most others can be found attached to rocky substrata.[17] Freshwater species account for 5% of red algal diversity, but they also have a worldwide distribution in various habitats;[5] they generally prefer clean, high-flow streams with clear waters and rocky bottoms, but with some exceptions.[18] A few freshwater species are found in black waters with sandy bottoms [19] and even fewer are found in more lentic waters.[20] Both marine and freshwater taxa are represented by free-living macroalgal forms and smaller endo/epiphytic/zoic forms, meaning they live in or on other algae, plants, and animals.[7] In addition, some marine species have adopted a parasitic lifestyle and may be found on closely or more distantly related red algal hosts.[21][22]

Taxonomy

Further information: Wikispecies:Rhodophyta

In the system of Adl et al. 2005, the red algae are classified in the Archaeplastida, along with the glaucophytes and green algae plus land plants (Viridiplantae or Chloroplastida). The authors use a hierarchical arrangement where the clade names do not signify rank; the class name Rhodophyceae is used for the red algae. No subdivisions are given; the authors say, "Traditional subgroups are artificial constructs, and no longer valid."[23]

Many studies published since Adl et al. 2005 have provided evidence that is in agreement for monophyly in the Archaeplastida (including red algae).[24][25][26][27] However, other studies have suggested Archaeplastida is paraphyletic.[28][29] As of January 2011, the situation appears unresolved.

Below are other published taxonomies of the red algae using molecular and traditional alpha taxonomic data; however, the taxonomy of the red algae is still in a state of flux (with classification above the level of order having received little scientific attention for most of the 20th century).[30]

  • If one defines the kingdom Plantae to mean the Archaeplastida, the red algae will be part of that kingdom
  • If Plantae are defined more narrowly, to be the Viridiplantae, then the red algae might be considered their own kingdom, or part of the kingdom Protista.

A major research initiative to reconstruct the Red Algal Tree of Life (RedToL) using phylogenetic and genomic approaches is funded by the National Science Foundation as part of the Assembling the Tree of Life Program.

Classification comparison

Classification system according to
Saunders and Hommersand 2004[30] 		Classification system according to
Hwan Su Yoon et al. 2006[31] 		Orders Multicelluar? Pit plugs? Example
Cyanidiales No No Cyanidioschyzon merolae
Rhodellales No No Rhodella
Compsopogonales, Rhodochaetales, Erythropeltidales Yes No Compsopogon
Rufusiales, Stylonematales Yes No Stylonema

Bangiales

Yes Yes Bangia, "Porphyra"

Porphyridiales

No No Porphyridium cruentum
Hildenbrandiales Yes Yes Hildenbrandia
Batrachospermales, Balliales, Balbianiales, Nemaliales, Colaconematales, Acrochaetiales, Palmariales, Thoreales Yes Yes Nemalion
Rhodogorgonales, Corallinales Yes Yes Corallina officinalis
Ahnfeltiales, Pihiellales Yes Yes Ahnfeltia
Bonnemaisoniales, Gigartinales, Gelidiales, Gracilariales, Halymeniales, Rhodymeniales, Nemastomatales, Plocamiales, Ceramiales Yes Yes Gelidium

Some sources (such as Lee) place all red algae into the class "Rhodophyceae". (Lee's organization is not a comprehensive classification, but a selection of orders considered common or important.[32])

A subphylum - Proteorhodophytina - has been proposed to encompass the existing classes Compsopogonophyceae, Porphyridiophyceae, Rhodellophyceae and Stylonematophyceae.[33] This proposal was made on the basis of the analysis of the plastid genomes.

See also: Eukaryote § Phylogeny

Species of red algae

Over 7,000 species are currently described for the red algae,[3] but the taxonomy is in constant flux with new species described each year.[30][31] The vast majority of these are marine with about 200 that live only in fresh water.

Some examples of species and genera of red algae are:

Morphology

Red algae have double cell walls.[34] The outer layers contain the polysaccharides agarose and agaropectin that can be extracted from the cell walls by boiling as agar.[34] The internal walls are mostly cellulose.[34] They also have the most gene-rich plastid genomes known.[35]

Pit connections and pit plugs

Main article: Pit connection

Pit connections

Pit connections and pit plugs are unique and distinctive features of red algae that form during the process of cytokinesis following mitosis.[36][37] In red algae, cytokinesis is incomplete. Typically, a small pore is left in the middle of the newly formed partition. The pit connection is formed where the daughter cells remain in contact.

Shortly after the pit connection is formed, cytoplasmic continuity is blocked by the generation of a pit plug, which is deposited in the wall gap that connects the cells.

Connections between cells having a common parent cell are called primary pit connections. Because apical growth is the norm in red algae, most cells have two primary pit connections, one to each adjacent cell.

Connections that exist between cells not sharing a common parent cell are labeled secondary pit connections. These connections are formed when an unequal cell division produced a nucleated daughter cell that then fuses to an adjacent cell. Patterns of secondary pit connections can be seen in the order Ceramiales.[37]

Pit plugs

After a pit connection is formed, tubular membranes appear. A granular protein, called the plug core, then forms around the membranes. The tubular membranes eventually disappear. While some orders of red algae simply have a plug core, others have an associated membrane at each side of the protein mass, called cap membranes. The pit plug continues to exist between the cells until one of the cells dies. When this happens, the living cell produces a layer of wall material that seals off the plug.

Function

The pit connections have been suggested to function as structural reinforcement, or as avenues for cell-to-cell communication and transport in red algae, however little data supports this hypothesis.[38]

Reproduction

The reproductive cycle of red algae may be triggered by factors such as day length.[2]

Fertilization

Red algae lack motile sperm. Hence, they rely on water currents to transport their gametes to the female organs – although their sperm are capable of "gliding" to a carpogonium's trichogyne.[2]

The trichogyne will continue to grow until it encounters a spermatium; once it has been fertilized, the cell wall at its base progressively thickens, separating it from the rest of the carpogonium at its base.[2]

Upon their collision, the walls of the spermatium and carpogonium dissolve. The male nucleus divides and moves into the carpogonium; one half of the nucleus merges with the carpogonium's nucleus.[2]

The polyamine spermine is produced, which triggers carpospore production.[2]

Spermatangia may have long, delicate appendages, which increase their chances of "hooking up".[2]

Life cycle

They display alternation of generations; in addition to gametophyte generation, many have two sporophyte generations, the carposporophyte-producing carpospores, which germinate into a tetrasporophyte – this produces spore tetrads, which dissociate and germinate into gametophytes.[2] The gametophyte is typically (but not always) identical to the tetrasporophyte.[39]

Carpospores may also germinate directly into thalloid gametophytes, or the carposporophytes may produce a tetraspore without going through a (free-living) tetrasporophyte phase.[39] Tetrasporangia may be arranged in a row (zonate), in a cross (cruciate), or in a tetrad.[2]

The carposporophyte may be enclosed within the gametophyte, which may cover it with branches to form a cystocarp.[39]

These case studies may be helpful to understand some of the life histories algae may display:

In a simple case, such as Rhodochorton investiens:

In the Carposporophyte: a spermatium merges with a trichogyne (a long hair on the female sexual organ), which then divides to form carposporangia – which produce carpospores.

Carpospores germinate into gametophytes, which produce sporophytes. Both of these are very similar; they produce monospores from monosporangia "just below a cross wall in a filament"[2] and their spores are "liberated through apex of sporangial cell."[2]

The spores of a sporophyte produce either tetrasporophytes. Monospores produced by this phase germinate immediately, with no resting phase, to form an identical copy of parent. Tetrasporophytes may also produce a carpospore, which germinates to form another tetrasporophyte.[verification needed][2]

The gametophyte may replicate using monospores, but produces sperm in spermatangia, and "eggs"(?) in carpogonium.[2]

A rather different example is Porphyra gardneri:

In its diploid phase, a carpospore can germinate to form a filamentous "conchocelis stage", which can also self-replicate using monospores. The conchocelis stage eventually produces conchosporangia. The resulting conchospore germinates to form a tiny prothallus with rhizoids, which develops to a cm-scale leafy thallus. This too can reproduce via monospores, which are produced inside the thallus itself.[2] They can also reproduce via spermatia, produced internally, which are released to meet a prospective carpogonium in its conceptacle.[2]

Chemistry

Algal group δ13C range[40]
HCO3-using red algae −22.5‰ to −9.6‰
CO2-using red algae −34.5‰ to −29.9‰
Brown algae −20.8‰ to −10.5‰
Green algae −20.3‰ to −8.8‰

The δ13C values of red algae reflect their lifestyles. The largest difference results from their photosynthetic metabolic pathway: algae that use HCO3 as a carbon source have less negative δ13C values than those that only use CO2.[40] An additional difference of about 1.71‰ separates groups intertidal from those below the lowest tide line, which are never exposed to atmospheric carbon. The latter group uses the more 13C-negative CO2 dissolved in sea water, whereas those with access to atmospheric carbon reflect the more positive signature of this reserve.

Photosynthetic pigments of Rhodophyta are chlorophylls a and d. Red algae are red due to phycoerythrin. They contain the sulfated polysaccharide carrageenan in the amorphous sections of their cell walls, although red algae from the genus Porphyra contain porphyran. They also produce a specific type of tannin called phlorotannins, but in lower amount than brown algae do.

Genomes of red algae

Complete genome sequences are only available for 6 species of red algae, including 4 published in 2013.

Fossil record

One of the oldest fossils identified as a red alga is also the oldest fossil eukaryote that belongs to a specific modern taxon. Bangiomorpha pubescens, a multicellular fossil from arctic Canada, strongly resembles the modern red alga Bangia despite occurring in rocks dating to 1.2 billion years ago.[1]

Two kinds of fossils resembling red algae were found sometime between 2006 and 2011 in well-preserved sedimentary rocks in Chitrakoot, central India. The presumed red algae lie embedded in fossil mats of cyanobacteria, called stromatolites, in 1.6 billion-year-old Indian phosphorite — making them the oldest plant-like fossils ever found by about 400 million years.[48]

Red algae are important builders of limestone reefs. The earliest such coralline algae, the solenopores, are known from the Cambrian period. Other algae of different origins filled a similar role in the late Paleozoic, and in more recent reefs.

Calcite crusts that have been interpreted as the remains of coralline red algae, date to the terminal Proterozoic.[49] Thallophytes resembling coralline red algae are known from the late Proterozoic Doushantuo formation.[50]

Relationship to other algae

Chromista and Alveolata algae (e.g., chrysophytes, diatoms, phaeophytes, dinophytes) seem to have evolved from bikonts that have acquired red algae as endosymbionts. According to this theory, over time these endosymbiont red algae have evolved to become chloroplasts. This part of endosymbiotic theory is supported by various structural and genetic similarities.[51]

Human consumption

Several species are important food crops, in particular members of the genus Porphyra, variously known as nori (Japan), gim (Korea), 紫菜 (China), or laver (Britain). Dulse (Palmaria palmata)[52] is another important British species.[53] These rhodophyte foods are high in vitamins and protein and are easily grown; for example, nori cultivation in Japan goes back more than three centuries.

In East and Southeast Asia, agar is most commonly produced from Gelidium amansii.

See also

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  49. ^ Grant, S. W. F.; Knoll, A. H.; Germs, G. J. B. (1991). "Probable Calcified Metaphytes in the Latest Proterozoic Nama Group, Namibia: Origin, Diagenesis, and Implications". Journal of Paleontology. 65 (1): 1–18. JSTOR 1305691. PMID 11538648.
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  51. ^ Summarised in Cavalier-Smith, Thomas (April 2000). "Membrane heredity and early chloroplast evolution". Trends in Plant Science. 5 (4): 174–182. doi:10.1016/S1360-1385(00)01598-3. PMID 10740299.
  52. ^ "Dulse: Palmaria palmata". Quality Sea Veg. Retrieved 2007-06-28.
  53. ^ T. F. Mumford; A. Muira (1988). "Porphyra as food: cultivation and economics". In C. A. Lembi; J. Waaland (eds.). Algae and Human Affairs. Cambridge University Press, Cambridge. ISBN 978-0-521-32115-0. {{cite book}}: Unknown parameter |lastauthoramp= ignored (|name-list-style= suggested) (help)
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