Ochrophyte

Ochrophytes Temporal range: Middle Proterozoic [1] 1000–0 Ma Pha. Proterozoic Archean Had.
Dense kelp forest with understory at Partridge Point near Dave's Caves, Cape Peninsula
Scientific classification
Domain:	Eukaryota
Clade:	Sar
Clade:	Stramenopiles
Clade:	Gyrista
Division:	Ochrophyta Cavalier-Smith 1986, emend. Cavalier-Smith & Chao 1996 [2]
Classes and possible taxa [3] [4]
Chrysista Aurearenophyceae Chrysophyceae Chrysoparadoxophyceae Eustigmatophyceae Olisthodiscophyceae Phaeosacciophyceae Phaeophyceae Phaeothamniophyceae Picophagea Raphidophyceae Schizocladiophyceae Synchromophyceae Xanthophyceae Actinophryida? Diatomista Diatomeae Dictyochophyceae Bolidophyceae Pelagophyceae
Diversity
23,314 described species [5] >100,000 estimated species [6]
Synonyms
Heterokontophyta Guiry, R.A.Andersen & Moestrup 2023 [7] Ochrista Cavalier-Smith 1986 [8] [9] Stramenochromes Leipe et al. 1994 [9]

Ochrophytes, also known as heterokontophytes or stramenochromes, are a phylum of algae. They are the photosynthetic stramenopiles, a group of eukaryotes, organisms with a cell nucleus, characterized by the presence of two unequal flagella, one of which has tripartite hairs called mastigonemes. In particular, they are characterized by photosynthetic organelles or plastids enclosed by four membranes, with membrane-bound compartments called thylakoids organized in piles of three, chlorophyll a and c as their photosynthetic pigments, and additional pigments such as β-carotene and xanthophylls. Ochrophytes are one of the most diverse lineages of eukaryotes, containing ecologically important algae such as brown algae and diatoms. They are classified either as phylum Ochrophyta, Heterokontophyta or as subphylum Ochrophytina within phylum Gyrista. Their plastids are of red algal origin.

Etymology

Throughout history, different names have been used to describe photosynthetic stramenopiles. The more widely used name is the phylum —or division, in botanical nomenclature— Ochrophyta, ^[10] based on the golden alga Ochromonas . ^[11] This name was first coined by evolutionary biologist Thomas Cavalier-Smith in 1986 as Ochrista, ^[11] later renamed to Ochrophyta to comply with the recommendations of the International Code of Botanical Nomenclature. ^{[12] [13]} In 2017, the same author lowered it to a subphylum inside phylum Gyrista, and modified the name to Ochrophytina to match the -phytina suffix used for botanical subdivisions. ^[14] Despite this, Ochrophyta is preferred over Ochrophytina by the scientific community. ^[2]

The alternative name Heterokontophyta is more familiar among phycologists. ^[7] The origin of this name is the class Heterokontæ (from Greek hetero 'different'and kontos 'pole'), introduced by Finnish biologist Alexander Ferdinand Luther  [ fi ] in 1899 to include yellow-green freshwater algae, ^[15] now part of Xanthophyceae and Raphidophyceae. This name referenced, among other traits, the two unequal flagella characteristic of all stramenopiles, also known as heterokonts. ^{[16] : 229} Eventually it was expanded to include more algae and became the division Heterokontophyta, coined by Christiaan van den Hoek in 1978 ^{[17] [a]} and used to describe all photosynthetic stramenopiles. ^{[16] : 229}

Characteristics

Ochrophytes are eukaryotic organisms composed of cells that are either naked or covered by scales, lorica or a cell wall. They can be single-celled, colonial, coenocytic or multicellular. Some Phaeophyceae (brown algae, seaweeds) develop as large multicellular thalli with differentiated tissues. ^[7] All ochrophytes uniformly have tubular mitochondrial cristae. ^[18] This is a common trait shared with their relatives, heterotrophic stramenopiles, as well as other closely related groups such as Rhizaria, Telonemia and Alveolata. ^{[19] [20]} As primarily photosynthetic eukaryotes, they are considered algae, distinguished from other groups of algae by specific morphological and ultrastructural traits, such as their flagella, chloroplasts and pigments. ^[18]

Diagram of a simplified ochrophyte cell showing the different compartments. af, anterior flagellum; es, eyespot; fs, flagellar swelling; g, Golgi apparatus; gl, girdle lamella; m, mitochondria (in orange); n, nucleus (in purple, nucleolus in darker purple); p, plastid (stroma in light green, thylakoids in dark green); pc, periplastidial compartment (in pink); per, periplastidial endoplasmic reticulum (in blue); pf, posterior flagellum; v, vacuole.

Flagella

As stramenopiles (=heterokonts), their swimming cells frequently display two markedly unequal flagella: an anterior flagellum ("tinsel") with straw-like hollow tripartite hairs called mastigonemes, and an immature posterior smooth flagellum ("whiplash") lacking these hairs. ^{[21] [18]} The ciliary transition zone of the flagellum generally has a transitional helix. ^[7]

Chloroplasts

The ochrophytes are mostly photosynthetic. As such, they may possess one or more photosynthetic plastids (chloroplasts) per cell. ^[22] Some groups contain species with leucoplasts, chloroplasts that have lost photosynthetic capacity and pigments but presumably continue to play a role in the synthesis of amino acids, lipids and heme groups. ^[18] Ochrophytes have a distinct plastid ultrastructure in comparison to other algal groups. ^[22] Their chloroplasts originate from an event of secondary endosymbiosis from a red alga, which lead to four ^[b] surrounding membranes: two inner membranes, corresponding to the primary plastid membranes; a third membrane, corresponding to the plasma membrane of the red alga; and an outermost layer, corresponding to the phagosome membrane. ^[25] This characteristic differentiates them from archaeplastid algae (glaucophytes, red algae and green algae), whose chloroplasts have only two membranes. ^[26] The two outer layers of ochrophyte plastids are continguous with the endoplasmic reticulum (ER), together composing the chloroplast endoplasmic reticulum (CER), ^[22] also known as the periplastidial endoplasmic reticulum (PER), which is often connected to the nuclear envelope. The tripartite flagellar hairs, characteristic of stramenopiles, are produced within either the PER or the nuclear envelope. ^[18]

The periplastid compartment (PC), between the second and third layers, is a separate region that in other algal groups (i.e. cryptomonads and chlorarachniophytes) contains a nucleomorph, the vestigial nucleus of the secondary endosymbiont; however, no nucleomorphs are known within the ochrophytes. Instead, other structures have been observed within the PC, similarly to those seen in haptophytes and chromerid algae: ^[22] "blob-like structures" where PC proteins are localized, and a vesicular network. ^[25] Within the CER, there is a prominent region of tight direct contacts between the periplastid membrane and the inner nuclear envelope, where lipid transfers might occur, and perhaps exchange of other molecules. ^[25]

Commonly, within the plastid stroma, three stacked thylakoids differentiate into the "girdle lamella", which runs around the periphery of the plastid, beneath the innermost membrane. ^[22] The remaining thylakoids are arranged in stacks of three. ^[18] In synchromophytes and aurearenophytes, a consortium of several plastids, each surrounded by two or three inner membranes respectively, is enveloped by a shared outer membrane. ^[22]

Pigmentation

Chemical structure of fucoxanthin

Ochrophyte chloroplasts contain chlorophylls a and c as photosynthetic pigments, in addition to fucoxanthin. ^[21] Chlorophyll a binds to thylakoids, while the c pigment is present in the stroma. ^[18] The most frequent accessory pigment in ochrophytes is the yellow β-carotene. The golden-brown or brown pigmentation in diatoms, brown algae, golden algae and others is conferred by the xanthophyll fucoxanthin. In the yellow-green or yellow-brown raphidophyceans, eustigmatophyceans and xanthophyceans, vaucheriaxanthin is dominant instead. These pigment combinations extend their photosynthetic ability beyond chlorophyll a alone. Additionally, xanthophylls protect the photosystems from high intensity light. ^[18]

Storage products

Ochrophyte algae accumulate chrysolaminarin, a carbohydrate consisting of short chains of β-1,3-linked glucose molecules, as a storage product. ^{[18] [27]} It is stored in vesicles located within the cytoplasm, outside plastids, unlike other algae. ^[21] Cytoplasmic lipid droplets are also common. ^[18] They lack starch, which is the common storage product in green algae and plants. ^[7]

Diversity

According to a 2024 survey, photosynthetic stramenopiles include 23,314 described species, with 490 species of uncertain position. ^[5] However, they may amount to more than 100,000 estimated species, of which the majority are diatoms. ^[6] They are divided into the following classes: ^{[2] [23] [28]}

Dinobryon (Chrysophyceae)

Lyrella (Diatomeae)

Pelvetiopsis (Phaeophyceae)

• Aurearenophyceae – One species of unicellular marine algae, Aurearena cruciata. Cells alternate between a naked, swimming stage and a non-motile stage covered in a cell wall. ^{[29] [16] : 271}

• Bolidophyceae – 18 species ^[16] of marine unicellular algae that may be naked and flagellated, or spherical and silicified, covered in silica "shields". ^[30]

• Chrysoparadoxophyceae – One enigmatic species of sand-dwelling unicellular algae, Chrysoparadoxa australica. Cells have been observed covered in cell walls, from which they escape as naked zoospores instead of dividing. They are exceptional for only having two chloroplast membranes. ^[23]

• Chrysophyceae – Commonly known as golden algae, they amount to 1,274 species ^[5] of freshwater or terrestrial algae with diverse morphologies: unicellular, colonial, amoeboid, capsoid, and coccoid. A considerable portion are colorless heterotrophs. ^[31] Cells may be naked or covered by cell walls, organic loricas, scales made of organic or siliceous material, or even be embedded in mucilage. ^{[32] [16] : 223,239}

• Diatomeae ^[c] – The diatoms are the most species-rich ochrophyte group, with 14,684 described species ^[5] that occupy freshwater, marine, and terrestrial ecosystems. Primarily unicellular, with some forming colonies consisting of chains of cells. They are known for their two overlapping silica frustules that cover each cell. ^{[16] : 249}

• Dictyochophyceae – 217 species ^[5] of mostly unicellular algae, which may be naked or covered in organic scales, and exhibit shapes from amoeboid to radially symmetrical. ^{[16] : 260} Some, known as silicoflagellates, grow basket-like silica skeletons that hold the cytoplasm. ^{[16] : 226}

• Eustigmatophyceae – 218 species ^[5] of unicellular coccoid algae covered by cell walls, present in freshwater, terrestrial, and less frequently marine habitats. They lack the girdle lamella characteristic of all other ochrophytes. They are known for their large eyespot, which lies outside the chloroplast. ^{[16] : 224–225,257}

• Olisthodiscophyceae – Two marine unicellular flagellated species with flattened gliding cells that live close to the substrate. They have been observed in various shallow marine habitats. ^[34]

• Pelagophyceae – 31 species ^[5] of marine flagellates characterised by a dense perforated theca. Many have highly reduced flagellar apparatuses. ^[35]

• Phaeophyceae – Commonly known as brown algae, they are the second most species-rich group, with 2,124 primarily marine species. ^[5] They are multicellular algae that exhibit tissue differentiation and a complex polysaccharide metabolism. Cells are covered in cell walls composed of cellulose, alginates, and other polymers. ^[36]

• Phaeosacciophyceae – Eight species ^[5] of unicellular, colonial, filamentous or thallic forms, typically covered with cell walls. They can be freshwater, marine, or soil-dwelling. ^[28]

• Phaeothamniophyceae – 31 species ^[5] of filamentous, pseudofilamentous, coccoid or capsoid algae, previously classified as golden algae and xanthophytes. ^[37] Cells are covered in cell walls and surrounded by a gelatinous envelope. ^{[16] : 266}

• Picophagea – One species of tiny marine heterotrophic flagellates, Picophagus flagellatus. ^[3]

• Pinguiophyceae – Five species of either flagellated or nonmotile unicellular marine algae, with an unusually high amount of fatty acids. ^[38]

• Raphidophyceae – 58 species ^[5] of marine and freshwater unicellular flagellated algae. Their cells are covered with multiple surface structures, such as mucocysts and trichocysts. ^[39]

• Schizocladiophyceae – One species of filamentous alga, Schizocladia ischiensis. It is similar to the filamentous Phaeophyceae, but distinguished by the absence of cellulose in its cell wall, and the absence of intercellular cytoplasmic connections. ^{[40] [16] : 270}

• Synchromophyceae – Five species of marine unicellular algae without flagella, that can join to form meroplasmodia. Some are colorless. One genus, Synchroma , has unique chloroplast complexes. ^[3]
• Xanthophyceae – 616 species ^[5] of algae with an unusual yellow-green coloration. Some are macroscopic, either filamentous or siphonous, while others are single-celled and coccoid. ^{[16] : 245}

Reproduction

Ochrophytes are capable of asexual reproduction by fragmentation, propagules, vegetative cell division, sporogenesis or zoosporogenesis. In addition, they are capable of sexual reproduction through gametes, by three different modes: isogamy, anisogamy or oogamy. ^[7]

Ecology

Ochrophytes are present in nearly all environments. ^[27] Some classes are more common in marine habitats, while others are more frequent in freshwater or soil. ^[18] Among the ochrophyte lineages are the diatoms, the most abundant photosynthetic eukaryotes worldwide in marine habitats; multicellular seaweeds, such as brown algae (e.g., kelp) and golden algae; and an array of microscopic single-celled lineages that are also abundant, as evidenced by environmental sequencing. ^[22] Regarding nutrition, various ochrophytes are mixotrophic, usually through phagocytosis. ^[27]

Marine

Several classes of heterokont algae are exclusively known from marine habitats, such as Bolidophyceae, Pelagophyceae, Pinguiophyceae and Schizocladiophyceae. The brown algae (Phaeophyceae) are almost exclusively marine, with very few freshwater genera. ^[27]

Freshwater

Chrysophyceae, Phaeothamniophyceae and Xanthophyceae are predominantly freshwater classes. In lotic habitats (rivers, streams), golden algae (Chrysophyceae) and yellow-green algae (Xanthophyceae) are common and occasionally abundant. The golden algal genus Hydrurus , in particular, can be widespread in some drainage basins and is common in cold, clear, fast-flowing mountain streams, where it attaches to a firm substrate. Xanthophycean genera commonly found in rivers include Vaucheria , Tribonema and Bumilleria , either freely floating or attached to filamentous algae and plants. ^[41] Diatoms are more diverse, with more than 60 genera commonly found in rivers. Many river diatoms have developed different strategies to attach to the substrate to avoid being displaced by water currents. The most basic strategy is to produce extracellular polymeric substances, varied carbohydrate structures formed from the cell membrane. In faster-flowing waters, some diatoms (e.g., Cocconeis ) grow directly attached to the substrate through adhesive films. Others (e.g., Eunotia , Nitzschia ) grow stalks or colonial tubes capable of reaching higher into the water column to acquire more nutrients. ^[42] Brown algae (Phaeophyceae), although highly diversified, contain only seven species present in rivers. These lack any complex multicellular thalli, and instead exist as benthic filamentous forms that have evolved independently from marine ancestors. ^[43]

Harmful algae

Two main lineages of photosynthetic stramenopiles include many toxic species. Within the class Raphidophyceae, strains of Heterosigma and Chattonella at high concentrations are responsible for fish mortality, although the nature and action of their toxins is not resolved. Freshwater Gonyostomum species are capable of mucilage secretion at high amounts detrimental to fish gills. Within the diatoms (Bacillariophyta), harmful effects can be due to physical damage or to toxin production. Centric diatoms like Chaetoceros live as colonial chains of cells with long spines (setae) that can clog fish gills, causing their death. Among diatoms, the only toxin producers have been found among pennate diatoms, almost entirely within the genus Pseudonitzschia . More than a dozen species of Pseudonitzschia are capable of producing a neurotoxin, domoic acid, the cause of amnesiac shellfish poisoning. ^[44]

Evolution

External

The ochrophytes constitute a highly diverse clade within Stramenopila, a eukaryotic supergroup that also includes several heterotrophic lineages of protists such as oomycetes, hyphochytrids, labyrinthuleans, opalines and bicosoecids. ^{[10] [45] [2]} This lineage of stramenopiles originated from an event of secondary endosymbiosis where a red alga was transformed into the chloroplast of the common ancestor of ochrophytes. ^{[45] [46] [14]}

The total group of ochrophytes is estimated to have evolved between 874 and 543 million years ago (Ma) through molecular clock inference. However, the earliest fossil remains, assigned to the billion-year-old xanthophyte Palaeovaucheria , ^[1] suggest that ochrophytes had appeared by 1000 Ma. Other early putative representatives of photosynthetic stramenopiles are Jacutianema (750 Ma), Germinosphaera (750–700 Ma) and the brown alga Miaohephyton (600–550 Ma). Scales similar to modern chrysophyte scales, and valves resembling the modern centric diatom valves, have been found in 800–700 million-years-old sediments. ^[47]

Internal

Chrysista SII Chrysophyceae Synchromophyceae Picophagea Actinophryida Olisthodiscophyceae Pinguiophyceae Eustigmatophyceae SI Raphidophyceae PX Xanthophyceae Chrysoparadoxophyceae Phaeophyceae Schizocladiophyceae Phaeosacciophyceae Aurearenophyceae Phaeothamniophyceae Diatomista Pelagophyceae Dictyochophyceae Bolidophyceae Diatomeae SIII

Evolutionary relationships between all ochrophyte classes, based on a 2025 multiprotein phylogenetic analysis. [3]

Relationships among many classes of ochrophytes remain unresolved, but three main clades (called SI, SII and SIII) are supported in most phylogenetic analyses. The SI lineage, containing the diverse and multicellular class Phaeophyceae, or brown algae, experienced an evolutionary radiation during the late Paleozoic (around 310 million years ago). The class Schizocladiophyceae is the sister lineage to brown algae, followed by a clade of closely related classes Xanthophyceae, Phaeosacciophyceae ^[28] and Chrysoparadoxophyceae. ^[23] This is in turn the sister lineage to a clade containing Aurearenophyceae and Phaeothamniophyceae, ^[45] which are sometimes treated as one class Aurophyceae. ^[14] The Raphidophyceae are the most basal within the SI. The SII lineage contains the golden algae or Chrysophyceae, as well as smaller classes Eustigmatophyceae, Pinguiophyceae, Synchromophyceae and Picophagea. Both clades, SI and SII, compose the Chrysista lineage. The remaining classes are grouped within the sister lineage Diatomista, equivalent to the SIII lineage: these are the diatoms or Diatomeae, and three closely related classes Bolidophyceae, Dictyochophyceae (including the silicoflagellates) and Pelagophyceae. ^[45] A new class of algae, Olisthodiscophyceae, was described in 2021 and recovered as part of the SII lineage. ^[34]

One group of heterotrophic heliozoan protists, Actinophryida, ^[48] is included in some classifications as the sister lineage to the raphidophytes, and both groups are treated as one class Raphidomonadea on the basis of 18S rDNA phylogenetic analyses. ^[4] However, a 2022 phylogenomic study placed one actinophryid, Actinophrys sol , as the probable sister group to ochrophytes. Although it lacks chloroplasts, plastidial genes have been found in the nuclear genome of this actinophryid, implying that its common ancestor with ochrophytes may have already begun domesticating plastids. ^[49] Later, a 2025 study recovered A. sol within the SII clade instead, implying that, much like the Picophagea, it evolved from ochrophytes that secondarily lost their chloroplasts. ^[3]

History of knowledge

Pre-Linnean

The first recorded stramenopile algae in history were the multicellular brown algae, such as kelp and other seaweeds. Their descriptions date back to early China (ca. 3000 BC), Japan (ca. 500 BC) and Greece (300 BC, such as Theophrastus). Knowledge of them likely predates recorded history, as they were potentially used by humans as a source for food, dyes, and medicine. ^[27] They likely played a role in the early dispersal of humans along seashores, ^{[16] : 220} particularly from East Asia to the Americas, where brown algae may have formed a corridor rich in aquatic resources after deglaciation. This is known as the kelp highway hypothesis. ^{[50] [51]} The remaining stramenopile algae were not included in historical works, due to being microscopic. ^[52]

The first unequivocal illustration of a diatom, Tabellaria , from 1703.

In the late 17th century, Antony van Leeuwenhoek became the first person to observe microbes, but he did not record microscopic stramenopiles. The first unmistakeable descriptions of diatoms belong to two illustrations published anonymously in England in 1703, 80 years before the first taxonomic description of a diatom. They are attributed to Charles King of Staffordshire. ^{[53] [54]}

Discovery period (1753–1882)

The first formal description of any stramenopile was by Carl Linnaeus in his 1753 work Species Plantarum , for the brown alga Fucus . In the following years, single-celled chrysophytes and diatoms were described for the first time by Otto Friedrich Müller. ^{[55] [56]} These descriptions started a century-long era of exploration, during which brown algae were described as plants, while microscopic algae were treated as animals under the name of infusoria. ^{[27] [16] : 220} Xanthophytes were first described in 1801 by Augustin Pyramus de Candolle, and raphidophytes were discovered by Karl Moriz Diesing in 1865. ^{[16] : 228}

Influential works were published around that time, such as the 1813 work by French naturalist Jean Vincent Félix Lamouroux with the use of pigment color to classify algae. ^[57] One of the most significant contributions was the 1838 publication by Christian Gottfried Ehrenberg, containing his observations of many stramenopiles under light microscopy. ^{[58] [27]} Still, these taxa remained separate from each other in the mind of taxonomists until the next period. ^{[16] : 220}

First synthesis period (1882–1914)

The 1882 work by M.J. Rostafinski ^[59] was the first to hypothesize an evolutionary link between the diatoms, golden algae, and brown algae. Several authors later developed this idea through various publications, such as Carl Correns, Georg Klebs, and Ernst Lemmermann, and phylogenetic relationships between very different algal groups were discussed. ^[27] This culminated in the 1900 phylogenetic study by Frederick Blackman, ^{[16] : 221} who hypothesized that complex multicellular algae evolved from simple flagellated algae, and that this happened independently in green algae (giving rise to plants) and golden algae (giving rise to brown algae and diatoms). ^[60] In 1914, Adolf Pascher published a synthesis where he did not fully accept the evolutionary relationships between stramenopile algae. Pascher instead separated the Chrysophyta (including golden algae, xanthophytes and diatoms) and the Phaeophyta (brown algae alone).

Floristic period (1914–1950)

During the following period, evolutionary discussions were mostly abandoned, because characters observed under light microscopy were insufficient to resolve evolutionary relationships. But many species were described.

During the 20th century, evolutionary and phylogenetic discussions began including heterokont algae. Transmission electron microscopy and molecular phylogenetic analysis led to the description of many new groups and several classes well into the 21st century. The sequencing of the first ochrophyte genome, belonging to Thalassiosira pseudonana , began in 2002. ^[27]

Notes

1. The name 'Heterokontophyta', as established in 1978 by van den Hoek, was not validly published. Before 2011, under the International Code of Botanical Nomenclature, a valid publication of a taxon required a description in Latin. Although after 2011 this was no longer a requirement, the change was not retroactive. In 2023, phycologists Michael Guiry, Øjvind Moestrup and Robert Andersen validated it. ^[7]
2. The only known exception is Chrysoparadoxa , which contains chloroplasts surrounded by two membranes as opposed to four. ^{[23] [24]}
3. Since 2019, diatoms do not form a single class, but numerous classes to reflect the phylogenetic advances over the previous decade. ^{[2] [33]}

References

1. Butterfield NJ (2004). "A Vaucheriacean Alga from the Middle Neoproterozoic of Spitsbergen: Implications for the Evolution of Proterozoic Eukaryotes and the Cambrian Explosion". Paleobiology. 30 (2): 231–252. Bibcode:2004Pbio...30..231B. doi:10.1666/0094-8373(2004)030<0231:AVAFTM>2.0.CO;2. JSTOR   4096845.
2. Adl, Sina M.; Bass, David; Lane, Christopher E.; Lukeš, Julius; Schoch, Conrad L.; et al. (26 September 2018). "Revisions to the Classification, Nomenclature, and Diversity of Eukaryotes". The Journal of Eukaryotic Microbiology. 66 (1): 4–119. doi: 10.1111/JEU.12691 . PMC   6492006 . PMID   30257078.
3. Terpis, Kristina X.; Salomaki, Eric D.; Barcytė, Dovilė; Pánek, Tomáš; Verbruggen, Heroen; et al. (9 January 2025). "Multiple plastid losses within photosynthetic stramenopiles revealed by comprehensive phylogenomics". Current Biology. 35 (3): 483–499.e8. Bibcode:2025CBio...35..483T. doi: 10.1016/j.cub.2024.11.065 . PMID   39793566.
4. Cavalier-Smith, Thomas; Scoble, Josephine Margaret (2013-08-01). "Phylogeny of Heterokonta: Incisomonas marina, a uniciliate gliding opalozoan related to Solenicola (Nanomonadea), and evidence that Actinophryida evolved from raphidophytes" . European Journal of Protistology. 49 (3): 328–353. doi:10.1016/j.ejop.2012.09.002. ISSN   0932-4739. PMID   23219323.
5. Michael D. Guiry (21 January 2024). "How many species of algae are there? A reprise. Four kingdoms, 14 phyla, 63 classes and still growing". Journal of Phycology . 00: 1–15. doi:10.1111/JPY.13431. ISSN   0022-3646. PMID   38245909. Wikidata   Q124684077.
6. H.S. Yoon; R.A. Andersen; S.M. Boo; D. Bhattacharya (17 February 2009). "Stramenopiles" . Encyclopedia of Microbiology (Third ed.). pp. 721–731. doi:10.1016/B978-012373944-5.00253-4. ISBN   978-0-12-373944-5 . Retrieved 2 March 2024.
7. Michael D. Guiry; Øjvind Moestrup; Robert A. Andersen (11 October 2023). "Validation of the phylum name Heterokontophyta" (PDF). Notulae Algarum. 2023 (297).
8. Cavalier-Smith, T. (1986). The kingdom Chromista, origin and systematics. In: Round, F.E. and Chapman, D.J. (eds.). Progress in Phycological Research. 4: 309–347.
9. Reviers, B. de. (2006). Biologia e Filogenia das Algas . Editora Artmed, Porto Alegre, p. 157.
10. Ingvild Riisberga; Russell J. S. Orr; Ragnhild Kluge; Kamran Shalchian-Tabrizi; Holly A. Bowers; Vishwanath Patil; Bente Edvardsen; Kjetill S. Jakobsen (2009). "Seven gene phylogeny of heterokonts". Protist . 160 (2): 191–204. doi:10.1016/j.protis.2008.11.004. PMID   19213601.
11. Cavalier-Smith, T. (1986). "The Kingdom Chromista: Origin and Systematics" (PDF). In Round, F.E.; Chapman, D.J. (eds.). Progress in Phycological Research. Vol. 4. Bristol: Biopress. pp. 309–347. ISBN   094873700X. OL   15332140M.
12. T. Cavalier-Smith; E. E. Chao (November 1996). "18S rRNA sequence of Heterosigma carterae (Raphidophyceae), and the phylogeny of heterokont algae (Ochrophyta)". Phycologia. 35 (6): 500–510. doi:10.2216/I0031-8884-35-6-500.1. ISSN   0031-8884. Wikidata   Q54493514.
13. Thomas Cavalier-Smith & Ema E.-Y. Chao (2006). "Phylogeny and megasystematics of phagotrophic heterokonts (kingdom Chromista)". Journal of Molecular Evolution . 62 (4): 388–420. Bibcode:2006JMolE..62..388C. doi:10.1007/s00239-004-0353-8. PMID   16557340. S2CID   29567514.
14. Thomas Cavalier-Smith (5 September 2017). "Kingdom Chromista and its eight phyla: a new synthesis emphasising periplastid protein targeting, cytoskeletal and periplastid evolution, and ancient divergences". Protoplasma . 255 (1): 297–357. doi:10.1007/S00709-017-1147-3. ISSN   0033-183X. PMC   5756292 . PMID   28875267. Wikidata   Q47194626.
15. Luther, Alexander (1899). "Über Chlorosaccus, eine neue Gattung der Süsserwasseralgen, nebst einigen bemerkungen zur Systematik verwandter Algen" [On Chlorosaccus, a new genus of freshwater algae, with some remarks on the systematics of related algae]. Bihang till Klongl. Svenska Vetenskaps-akademiens Handlingar (in German). 24, Afd. III (13): 1–22. ISSN   0284-7280. OCLC   7646576.
16. Graf, Louis (2024). "Heterokontophyta—Photosynthetic Stramenopiles". In Büdel, Burkhard; Friedl, Thomas; Beyschlag, Wolfram (eds.). Biology of Algae, Lichens and Bryophytes. Springer Spektrum. pp. 220–279. doi:10.1007/978-3-662-65712-6_5. ISBN   978-3-662-65712-6.
17. C. van den Hoek; D. G. Mann; H. M. Jahns (1995). Algae: an introduction to phycology. Cambridge: University Press. ISBN   0-521-30419-9.
18. Graham LE, Graham JM, Wilcox LW, Cook ME (2022). "Photosynthetic Stramenopiles I: Introduction to Photosynthetic Stramenopiles". Algae (4th ed.). LJLM Press. pp. 12-2 –12-4. ISBN   978-0-9863935-4-9.
19. John A Raven (15 December 2020). "Determinants, and implications, of the shape and size of thylakoids and cristae". Journal of Plant Physiology . 257: 153342. doi:10.1016/J.JPLPH.2020.153342. ISSN   0176-1617. PMID   33385618. Wikidata   Q104691547.
20. Denis Tikhonenkov; Mahwash Jamy; Anastasia S Borodina; et al. (16 March 2022). "On the origin of TSAR: morphology, diversity and phylogeny of Telonemia". Open Biology . 12 (3): 210325. doi:10.1098/RSOB.210325. ISSN   2046-2441. PMC   8924772 . PMID   35291881. Wikidata   Q112636995.
21. Lee RE (2018). Phycology (5th ed.). Cambridge University Press. doi:10.1017/9781316407219. ISBN   978-1-107-55565-5.
22. Dorrell RG, Bowler C (2017). "Chapter Three - Secondary Plastids of Stramenopiles". Advances in Botanical Research. 84: 57–103. doi:10.1016/bs.abr.2017.06.003.
23. Wetherbee R, Jackson CJ, Repetti SI, Clementson LA, Costa JF, van de Meene A, Crawford S, Verbruggen H (April 2019). "The golden paradox - a new heterokont lineage with chloroplasts surrounded by two membranes". J Phycol. 55 (2): 257–278. Bibcode:2019JPcgy..55..257W. doi:10.1111/jpy.12822. hdl: 11343/233613 . PMID   30536815. S2CID   54477112.
24. Marek Eliáš (7 June 2021). "Protist diversity: Novel groups enrich the algal tree of life". Current Biology . 31: R733 –R735. doi:10.1016/J.CUB.2021.04.025. ISSN   0960-9822. Wikidata   Q124822461.
25. Flori S, Jouneau PH, Finazzi G, Maréchal E, Falconet D (2016). "Ultrastructure of the Periplastidial Compartment of the Diatom Phaeodactylum tricornutum". Protist. 167 (1): 254–267. doi:10.1016/j.protis.2016.04.001. PMID   27179349.
26. Stadnichuk, I.N.; Kusnetsov, V.V. (2021). "Endosymbiotic Origin of Chloroplasts in Plant Cells' Evolution". Russian Journal of Plant Physiology. 68 (1): 1–16. Bibcode:2021RuJPP..68....1S. doi:10.1134/S1021443721010179. S2CID   255012748.
27. Andersen, Robert A. (2004). "Biology and systematics of heterokont and haptophyte algae". American Journal of Botany. 91 (10): 1508–1522. Bibcode:2004AmJB...91.1508A. doi:10.3732/ajb.91.10.1508. ISSN   0002-9122. PMID   21652306.
28. Graf L, Yang EC, Han KY, Küpper FC, Benes KM, Oyadomari JK, Herbert RJH, Verbruggen H, Wetherbee R, Andersen RA, Yoon HS (December 2020). "Multigene Phylogeny, Morphological Observation and Re-examination of the Literature Lead to the Description of the Phaeosacciophyceae Classis Nova and Four New Species of the Heterokontophyta SI Clade" (PDF). Protist. 171 (6) 125781. doi: 10.1016/j.protis.2020.125781 . PMID   33278705. S2CID   227315556.
29. Kai A, Yoshii Y, Nakayama T, Inouye I (2008). "Aurearenophyceae classis nova, a New Class of Heterokontophyta Based on a New Marine Unicellular Alga Aurearena cruciata gen. et sp. nov. Inhabiting Sandy Beaches" . Protist. 159 (3): 435–457. doi:10.1016/j.protis.2007.12.003. ISSN   1434-4610. PMID   18358776.
30. Kuwata, Akira; Yamada, Kazumasa; Ichinomiya, Mutsuo; Yoshikawa, Shinya; Tragin, Margot; Vaulot, Daniel; Lopes dos Santos, Adriana (29 October 2018). "Bolidophyceae, a Sister Picoplanktonic Group of Diatoms – A Review". Frontiers in Marine Science. 5 370. Bibcode:2018FrMaS...5..370K. doi: 10.3389/fmars.2018.00370 . ISSN   2296-7745.
31. Kim, Eunsoo; Yubuki, Naoji; Leander, Brian S.; Graham, Linda E. (2010). "Ultrastructure and 18S rDNA Phylogeny of Apoikia lindahlii comb. nov. (Chrysophyceae) and its Epibiontic Protists, Filos agilis gen. et sp. nov. (Bicosoecida) and Nanos amicus gen. et sp. nov. (Bicosoecida)". Protist. 161 (2): 177–196. doi:10.1016/j.protis.2009.09.003. PMID   20022300.
32. Kristiansen, Jørgen; Škaloud, Pavel (2017). "Chrysophyta". In Archibald, John M.; Simpson, Alastair G.B.; Slamovits, Claudio H. (eds.). Handbook of the Protists (PDF). Vol. 1 (2nd ed.). Cham: Springer International Publishing. pp. 331–366. doi:10.1007/978-3-319-28149-0_43. ISBN   978-3-319-28149-0. LCCN   2017945328.
33. Friedl, Thomas (2024), Büdel, Burkhard; Friedl, Thomas; Beyschlag, Wolfram (eds.), "Algae from Secondary Endosymbiosis" , Biology of Algae, Lichens and Bryophytes, Berlin, Heidelberg: Springer, pp. 219–383, doi:10.1007/978-3-662-65712-6_5, ISBN   978-3-662-65712-6 , retrieved 2025-10-17
34. Dovilė Barcytė; Wenche Eikrem; Anette Engesmo; Sergio Seoane; Jens Wohlmann; Aleš Horák; Tatiana Yurchenko; Marek Eliáš (2 March 2021). "Olisthodiscus represents a new class of Ochrophyta". Journal of Phycology. 57 (4): 1094–1118. Bibcode:2021JPcgy..57.1094B. doi: 10.1111/jpy.13155 . hdl: 10852/86515 . PMID   33655496.
35. Wetherbee, Richard; Bringloe, Trevor T.; van de Meene, Allison; Andersen, Robert A.; Verbruggen, Heroen (2023). "Structure and formation of the perforated theca defining the Pelagophyceae (Heterokonta), and three new genera that substantiate the diverse nature of the class". Journal of Phycology. 59 (1): 126–151. Bibcode:2023JPcgy..59..126W. doi: 10.1111/jpy.13294 . ISSN   0022-3646. PMID   36326615.
36. Bringloe, Trevor T.; Starko, Samuel; Wade, Rachael M.; Vieira, Christophe; Kawai, Hiroshi; et al. (27 Jul 2020). "Phylogeny and Evolution of the Brown Algae" (PDF). Critical Reviews in Plant Sciences. 39 (4): 281–321. Bibcode:2020CRvPS..39..281B. doi: 10.1080/07352689.2020.1787679 . Retrieved 22 August 2025.
37. Craig Bailey J, Bidigare RR, Christensen SJ, Andersen RA (September 1998). "Phaeothamniophyceae Classis Nova: A New Lineage of Chromophytes Based upon Photosynthetic Pigments, rbcL Sequence Analysis and Ultrastructure". Protist. 149 (3): 245–63. doi:10.1016/S1434-4610(98)70032-X. PMID   23194637.
38. Kawachi, Masanobu; Inouye, Isao; Honda, Daiske; O'Kelly, Charles J.; Bailey, J. Craig; Bidigare, Robert R.; Andersen, Robert A. (2002). "The Pinguiophyceae classis nova, a new class of photosynthetic stramenopiles whose members produce large amounts of omega-3 fatty acids". Phycological Research. 50 (1): 31–47. Bibcode:2002PhycR..50...31K. doi:10.1046/j.1440-1835.2002.00260.x. ISSN   1322-0829.
39. Engesmo, Anette; Eikrem, Wenche; Seoane, Sergio; Smith, Kirsty; Edvardsen, Bente; et al. (2016). "New insights into the morphology and phylogeny of Heterosigma akashiwo (Raphidophyceae), with the description of Heterosigma minor sp. nov ". Phycologia. 55 (3): 279–294. Bibcode:2016Phyco..55..279E. doi:10.2216/15-115.1. ISSN   0031-8884 . Retrieved 27 October 2025.
40. Kawai, Hiroshi; Maeba, Shunsuke; Sasaki, Hideaki; Okuda, Kazuo; Henry, Eric C. (2003). "Schizocladia ischiensis: A New Filamentous Marine Chromophyte Belonging to a New Class, Schizocladiophyceae" . Protist. 154 (2): 211–228. doi:10.1078/143446103322166518. ISSN   1434-4610. PMID   13677449.
41. Orlando Necchi Jr. (2016). "Chapter 7. Heterokonts (Xanthophyceae and Chrysophyceae) in Rivers". In Orlando Necchi Jr. (ed.). River Algae. Switzerland: Springer International Publishing. pp. 153–158. doi:10.1007/978-3-319-31984-1_7.
42. Ana Luiza Burliga; J. Patrick Kociolek (2016). "Chapter 5. Diatoms (Bacillariophyta) in Rivers". In Orlando Necchi Jr. (ed.). River Algae. Switzerland: Springer International Publishing. pp. 153–158. doi:10.1007/978-3-319-31984-1_5.
43. John D. Wehr (2016). "Chapter 6. Brown Algae (Phaeophyceae) in Rivers". In Orlando Necchi Jr. (ed.). River Algae. Switzerland: Springer International Publishing. pp. 153–158. doi:10.1007/978-3-319-31984-1_6.
44. Medlin LK, Cembella AD (2013). "Biodiversity of Harmful Marine Algae". In Levin SA (ed.). Encyclopedia of Biodiversity (PDF) (Second ed.). Academic Press. pp. 470–484. doi:10.1016/B978-0-12-384719-5.00404-4. ISBN   978-0-12-384720-1.
45. Bringloe, Trevor T.; Starko, Samuel; Wade, Rachael M.; Vieira, Christophe; Kawai, Hiroshi; et al. (27 Jul 2020). "Phylogeny and Evolution of the Brown Algae" (PDF). Critical Reviews in Plant Sciences. 39 (4): 281–321. Bibcode:2020CRvPS..39..281B. doi: 10.1080/07352689.2020.1787679 . Retrieved 22 August 2025.
46. Ševčíková T, Horák A, Klimeš V, et al. (2015). "Updating algal evolutionary relationships through plastid genome sequencing: did alveolate plastids emerge through endosymbiosis of an ochrophyte?". Sci Rep. 5 10134. Bibcode:2015NatSR...510134S. doi: 10.1038/srep10134 . PMC   4603697 . PMID   26017773.
47. Brown JW, Sorhannus U (2010). "A Molecular Genetic Timescale for the Diversification of Autotrophic Stramenopiles (Ochrophyta): Substantive Underestimation of Putative Fossil Ages". PLOS ONE. 5 (9) e12759. Bibcode:2010PLoSO...512759B. doi: 10.1371/journal.pone.0012759 . PMC   2940848 . PMID   20862282.
48. Mikrjukov, Kirill A.; Patterson, David J. (2001). "Taxonomy and phylogeny of Heliozoa. III. Actinophryids" (PDF). Acta Protozoologica. 40: 3–25.
49. Azuma, Tomonori; Pánek, Tomáš; Tice, Alexander K.; Kayama, Motoki; Kobayashi, Mayumi; Miyashita, Hideaki; Suzaki, Toshinobu; Yabuki, Akinori; Brown, Matthew W.; Kamikawa, Ryoma (10 April 2022). "An Enigmatic Stramenopile Sheds Light on Early Evolution in Ochrophyta Plastid Organellogenesis". Molecular Biology and Evolution. 39 (4) msac065. doi:10.1093/molbev/msac065. PMC   9004409 . PMID   35348760.
50. Erlandson, Jon M.; Braje, Todd J.; Gill, Kristina M.; Graham, Michael H. (2 September 2015). "Ecology of the Kelp Highway: Did Marine Resources Facilitate Human Dispersal From Northeast Asia to the Americas?". The Journal of Island and Coastal Archaeology. 10 (3): 392–411. doi:10.1080/15564894.2014.1001923. ISSN   1556-4894.
51. Braje, Todd J.; Dillehay, Tom D.; Erlandson, Jon M.; Klein, Richard G.; Rick, Torben C. (3 November 2017). "Finding the first Americans". Science. 358 (6363): 592–594. Bibcode:2017Sci...358..592B. doi:10.1126/science.aao5473. ISSN   0036-8075. PMID   29097536.
53. Dolan, John R. (2019). "Unmasking "The Eldest Son of The Father of Protozoology": Charles King". Protist. 170 (4). doi:10.1016/j.protis.2019.07.002.
54. Karlusich, Juan Jose Pierella; Ibarbalz, Federico M; Bowler, Chris (30 October 2020). "Exploration of marine phytoplankton: from their historical appreciation to the omics era" (PDF). Journal of Plankton Research: 595–612. doi: 10.1093/plankt/fbaa049 . ISSN   0142-7873 . Retrieved 10 November 2025.
55. Müller, Othone Friderico (1773). Vermivm terrestrium et fluviatilium, seu, Animalium infusoriorum, helminthicorum et testaceorum, non marinorum, succincta historia [A brief history of terrestrial and aquatic worms, or, of infusorian, helminthic, and non-marine animals] (in Latin). Vol. 1. Hauniae [Copenhagen]: Nicolai Mölleri. doi: 10.5962/bhl.title.46299 . LCCN   11003700. OCLC   16831547.
56. Müller, Otho Friedricus (1786). Animalcula infusoria fluviatilia et marina [Small aquatic and marine infusoria] (in Latin). Hauniae [Copenhagen]: Heineck et Faber. doi: 10.5962/bhl.title.46299 . LCCN   11003700. OCLC   16831547.
57. Lamouroux, Jean Vincent Félix (1813). Essai sur les genres de la famille des Thalassiophytes non articulées: présenté à l'Institut, dans la séance du 3 février 1812 [Essay on the genera of the non-articulated Thalassiophyte family: presented to the Institute, in the session of February 3, 1812] (in French). Paris: G. Dufour. OCLC   165882976.
58. Ehrenberg, Christian Gottfried (1838). Die Infusionsthierchen als vollkommene Organismen. Ein Blick in das tiefere organische Leben der Natur[The infusoria animals as perfect organisms. A look into the deeper organic life of nature] (in German). Leipzig: L. Voss. pp. i–xviii, 1–547, plates I–LXIV. doi: 10.5962/bhl.title.58475 . OCLC   15015104.
59. Rostafinski, M.J. "L'Hydrurus et ses affinités". Annales des Sciences Naturelles Botanique. 14: 1–25. LCCN   89641916. OCLC   1481304.
60. Blackman, F. Frost (1900). "The Primitive Algae and the Flagellata. An Account of modern Work bearing on the Evolution of the Algae". Annals of Botany. os-14 (4): 647–688. doi: 10.1093/oxfordjournals.aob.a088798 . ISSN   1095-8290 . Retrieved 2025-11-05.