Stramenopile

The stramenopiles, also called heterokonts, are protists distinguished by the presence of stiff tripartite external hairs. In most species, the hairs are attached to flagella, in some they are attached to other areas of the cellular surface, and in some they have been secondarily lost (in which case relatedness to stramenopile ancestors is evident from other shared cytological features or from genetic similarity). Stramenopiles represent one of the three major clades in the SAR supergroup, along with Alveolata and Rhizaria.

Stramenopiles are eukaryotes; most are single-celled, but some are multicellular including some large seaweeds, the brown algae. The group includes a variety of algal protists, heterotrophic flagellates, opalines and closely related proteromonad flagellates (all endobionts in other organisms); the actinophryid Heliozoa, and oomycetes. The tripartite hairs characteristic of the group have been lost in some of the included taxa – for example in most diatoms.

Many stramenopiles are unicellular flagellates, and most others produce flagellated cells at some point in their lifecycles, for instance as gametes or zoospores. Most flagellated heterokonts have two flagella; the anterior flagellum has one or two rows of stiff hairs or mastigonemes, and the posterior flagellum is without such embellishments, being smooth, usually shorter, or in a few cases not projecting from the cell.

The term 'heterokont' is used both as an adjective – indicating that a cell has two dissimilar flagella, and as the name of a taxon. The groups included in that taxon have however varied widely, creating the 'heterokont problem', now resolved by the definition of the stramenopiles.

Nomenclature

The term 'stramenopile' was introduced by D. J. Patterson in 1989, defining a group that overlapped with the ambiguously defined heterokonts.<ref>Template:Cite book</ref><ref>Template:Cite journal</ref> The name "stramenopile" has been discussed by J. C. David.<ref>Template:Cite journal</ref> Patterson's term was formalized as a taxonomic name, Stramenopiles, in 2005 by the International Society of Protistologists.<ref name="Adl 2005"/> It has since been the most widely accepted name for this group of organisms.<ref name="Adl 2019"/> Several alternative names have been proposed since Patterson's publication, such as Straminipila,<ref name="Dick, M. W. 2001"/> Straminopiles,<ref name="Vørs-1993"/> and Stramenopila,<ref name="Alexopoulos-1996"/> which is the valid name under the PhyloCode.<ref>{{#invoke:citation/CS1|citation |CitationClass=web }}</ref>

The heterokont problem

The term 'heterokont' is used as both an adjective – indicating that a cell has two dissimilar flagella – and as the name of a taxon. The taxon 'Heterokontae' was introduced in 1899 by Alexander Luther for algae that are now considered the Xanthophyceae.<ref>Template:Cite book</ref> But the same term was used for other groupings of algae. For example, in 1956, Copeland<ref>Template:Cite book</ref> used it to include the xanthophytes (using the name Vaucheriacea), a group that included what became known as the chrysophytes, the silicoflagellates, and the hyphochytrids. Copeland also included the unrelated collar flagellates (as the choanoflagellates) in which he placed the bicosoecids. He also included the not-closely related haptophytes. The consequence of associating multiple concepts to the taxon 'heterokont' is that the meaning of 'heterokont' can only be made clear by making reference to its usage: Heterokontae sensu Luther 1899; Heterokontae sensu Copeland 1956, etc. This contextual clarification is rare, such that when the taxon name is used, it is unclear how it should be understood. The term 'heterokont' has lost its usefulness in critical discussions about the identity, nature, character and relatedness of the group.<ref>Template:Cite journal</ref> The term 'stramenopile' sought to identify a clade (monophyletic and holophyletic lineage) using the approach developed by transformed cladists of pointing to a defining innovative characteristic or apomorphy.<ref>Template:Cite book</ref>

Over time, the scope of application has changed, especially when in the 1970s ultrastructural studies revealed greater diversity among the algae with chromoplasts (chlorophylls a and c) than had previously been recognized. At the same time, a protistological perspective was replacing the 19th century one based on the division of unicellular eukaryotes into animals and plants. One consequence was that an array of heterotrophic organisms, many not previously considered as 'heterokonts', were seen as related to the 'core heterokonts' (those having anterior flagella with stiff hairs). Newly recognized relatives included the parasitic opalines, proteromonads, and actinophryid Heliozoa. They joined other heterotrophic protists, such as bicosoecids, labyrinthulids, and oomycete fungi, that were included by some as heterokonts and excluded by others. Rather than continue to use a name whose meaning had changed over time and was hence ambiguous, the name 'stramenopile' was introduced to refer to the clade of protists that had tripartite stiff (usually flagellar) hairs and all their descendants. Molecular studies confirm that the genes that code for the proteins of these hairs are exclusive to stramenopiles.<ref>Template:Cite journal</ref>

Characteristics

The presumed apomorphy of tripartite flagellar hairs in stramenopiles is well characterized. The basal part of the hair is flexible and inserts into the cell membrane; the second part is dominated by a long stiff tube (the 'straw' or 'stramen'); and finally the tube is tipped by many delicate hairs called mastigonemes.<ref name="Bouck 1971">Template:Cite journal</ref> The proteins that code for the mastigonemes appear to be exclusive to the stramenopile clade, and are present even in taxa (such as diatoms) that no longer have such hairs.<ref name="Blackman Arikawa Yamada Suzaki 2011">Template:Cite journal</ref>

Most stramenopiles have two flagella near the apex.<ref name="Yoon Andersen Boo Bhattacharya 2009 pp. 721–731">Template:Cite book</ref> They are usually supported by four microtubule roots in a distinctive pattern. There is a transitional helix inside the flagellum where the beating axoneme with its distinctive geometric pattern of nine peripheral couplets around two central microtubules changes into the nine-triplet structure of the basal body.<ref name="Fu Nagasato Oka Cock 2014 pp. 662–675">Template:Cite journal</ref>

Plastids

Many stramenopiles have plastids which enable them to photosynthesise, using light to make their own food. Those plastids are coloured off-green, orange, golden or brown because of the presence of chlorophyll a, chlorophyll c, and fucoxanthin. This form of plastid is called a stramenochrome or chromoplast.Template:Efn The most significant autotrophic stramenopiles are the brown algae (wracks and many other seaweeds), and the diatoms. The latter are among the most significant primary producers in marine and freshwater ecosystems.<ref name="Leipe Wainright Gunderson Porter 1994">Template:Cite journal</ref> Most molecular analyses suggest that the most basal stramenopiles lacked plastids and were accordingly colourless heterotrophs, feeding on other organisms. This implies that the stramenopiles arose as heterotrophs, diversified, and then some of them acquired chromoplasts. Some lineages (such as the axodine lineage that included the chromophytic pedinellids, colourless ciliophryids, and colourless actinophryid heliozoa) have secondarily reverted to heterotrophy.<ref name="Leyland Leu Boussiba 2017">Template:Cite journal</ref><ref name="Derelle López-García Timpano Moreira 2016">Template:Cite journal</ref>

Ecology

File:Kelp-forest-Monterey.jpg

Giant kelp, Macrocystis pyrifera, an example of a multicellular stramenopile, is a large seaweed, up to Template:Convert long, in the Phaeophyceae, within the Gyrista.

Some stramenopiles are significant as autotrophs and as heterotrophs in natural ecosystems; others are parasitic. Blastocystis is a gastrointestinal parasite of humans;<ref name="Roberts Stark Harkness Ellis 2014 p=17">Template:Cite journal</ref> opalines and proteromonads live in the intestines of cold-blooded vertebrates and have been described as parasitic;<ref name="Olsen 1986">Template:Cite book</ref> oomycetes include some significant plant pathogens such as the cause of potato blight, Phytophthora infestans.<ref name= "PlDis2011">Template:Cite journal</ref> Diatoms are major contributors to global carbon cycles because they are the most important autotrophs in most marine habitats.<ref name="BGCC1">Template:Cite journal</ref> The brown algae, including familiar seaweeds like wrack and kelp, are major autotrophs of the intertidal and subtidal marine habitats.<ref name="Cock Peters Coelho 2011">Template:Cite journal</ref> Some of the bacterivorous stramenopiles, such as Cafeteria, are common and widespread consumers of bacteria, and thus play a major role in recycling carbon and nutrients within microbial food webs.<ref>{{#invoke:citation/CS1|citation |CitationClass=web }}</ref><ref>Template:Cite journal</ref>

Evolution

External

Stramenopiles are most closely related to alveolates and Rhizaria, all of which have tubular mitochondrial cristae and collectively form the SAR supergroup, whose name is formed from their initials.<ref>Krylov, M. V.; Dobrovolskii, A. A.; Issi, I. V.; Michaelevich, B. I.; Podlipaev, S. A.; Reshetnyak, V. V.; Seravin, L. N.; et al. 1980. New concepts for the system of unicellular organisms. Trudy Zoologischkei Institut Akademiya Nayuk, SSSR 94:122–132.</ref><ref name="Derelle López-García Timpano Moreira 2016"/><ref name=Burki2008a>Template:Cite journal</ref> The ancestor of the SAR supergroup appears to have captured a unicellular photosynthetic red alga, and many stramenopiles, as well as members of other SAR groups such as the Rhizaria, still have plastids which retain the double membrane of the red alga and a double membrane surrounding it, for a total of four membranes.<ref name="Oborník Lukeš 2013 pp. 333–369">Template:Cite book</ref> In addition, species of Telonemia, the sister group to SAR, exhibit heterokont flagella with tripartite mastigonemes, implying a more ancient origin of stramenopile characteristics.<ref name="Arpakorses">Template:Cite journal</ref>

Internal

The following cladogram summarizes the evolutionary relationships between stramenopiles. The phylogenetic relationships of Bigyra vary greatly from one analysis to the next: it has been recovered as either monophyletic<ref name="Incisomonas">Template:Cite journal</ref><ref name="THAKUR_2019"/> or paraphyletic. When paraphyletic, the branching order of the bigyran groups also varies: in some studies, Sagenista is the most basal-branching clade,<ref name="Incisomonas"/><ref name="firstMAST6"/><ref name="Kaonashia">Template:Cite Q</ref> while in others Opalozoa is the most basal.<ref name="CHO_2023">Template:Cite Q</ref> Nonetheless, Platysulcea is consistently recovered as the sister clade to all other stramenopiles.<ref name="THAKUR_2019"/><ref name="firstMAST6"/> In addition, a flagellate species discovered in 2023, Kaonashia insperata, remains in an uncertain phylogenetic position, but more closely related to Gyrista than to other clades.<ref name="Kaonashia"/>

Classification

File:Paraphysomonas butcheri whole mount.jpg

Electron micrograph of the protist Paraphysomonas butcheri. It illustrates the stramenopile property – of having stiff hairs. The hairs attach to one longer flagellum, the other is without hairs (an arrangement also called 'heterokont', meaning "unequal"). The body of the flagellate is coated with delicate scales. Paraphysomonas feeds on bacteria, two of which lie near the hairy flagellum.

The classification of the stramenopiles according to Adl et al. (2019), with additions from newer research:<ref name="Adl 2019">Template:Cite journal</ref><ref name="8phyla"/>

• Platysulcea Template:Au<ref name="THAKUR_2019">Template:Cite journal</ref>
• Bigyra Template:Au
  • Opalozoa Template:Au
    • Nanomonadea Template:Au
    • Opalinata Template:Au [=Slopalinida Template:Au]
    • Bicosoecida Template:Au
  • Sagenista Template:Au
    • Labyrinthulomycetes Template:Au
    • Pseudophyllomitidae Template:Au<ref name="firstMAST6">Template:Cite journal</ref>
• Gyrista Template:Au
  • Bigyromonada Template:Au
    • Developea Template:Au
    • Pirsoniales Template:Au
  • Pseudofungi Template:Au
    • Hyphochytriales Template:Au
    • Peronosporomycetes Template:Au [=Oomycetes Template:Au]
  • Actinophryidae Template:Au
  • Ochrophyta Template:Au
    • Chrysista Template:Au
      • Chrysoparadoxophyceae Template:Au<ref name="Chrysoparadoxophyceae">Template:Cite journal</ref>
      • Chrysophyceae Template:Au
      • Chloromorophyceae (nomen dubium)<ref>Template:Cite journal</ref>
      • Eustigmatophyceae Template:Au
      • Olisthodiscophyceae Template:Au<ref name="Graf_2021">Template:Cite journal</ref><ref name="Bacryté_2021">Template:Cite journal</ref>
      • Phaeophyceae Template:Au
      • Phaeosacciophyceae Template:Au<ref name="Phaeosacciophyceae">Template:Cite journal</ref>
      • Phaeothamniophyceae Template:Au
      • Raphidophyceae Template:Au
      • Schizocladiophyceae Template:Au
      • Synchromophyceae Template:Au [=Picophagea Template:Au]
      • Xanthophyceae Template:Au [Heterokontae Template:Au; Heteromonadea Template:Au; Xanthophyta Template:Au]
    • Diatomista Template:Au
      • Bolidophyceae Template:Au
      • Diatomeae Template:Au [=Bacillariophyta Template:Au]
      • Dictyochophyceae Template:Au
      • Pelagophyceae Template:Au
      • Pinguiophyceae Template:Au

External links

• Tree of Life Web Project: Stramenopiles