Telonemia

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Telonemia
Telonema rivulare (contrast micrography).jpg
Telonema rivulare by interference contrast micrography
Scientific classification OOjs UI icon edit-ltr.svg
Domain: Eukaryota
Clade: Diaphoretickes
Clade: TSAR
Phylum: Telonemia
Shalchian-Tabrizi 2006 [1]
Class: Telonemea
Cavalier-Smith 1993 [2]
Order: Telonemida
Cavalier-Smith 1993 [2]
Family: Telonemidae
Cavalier-Smith 1993 [2]
Genera
Diversity
7 species
Electron micrograph of T. rivulare Telonema rivulare (electron micrography).jpg
Electron micrograph of T. rivulare

Telonemia is a phylum of microscopic eukaryotes commonly known as telonemids. They are unicellular free-living flagellates with a unique combination of cell structures, including a highly complex cytoskeleton unseen in other eukaryotes.

Contents

Telonemia shares several distinctive features with its related group, the SAR supergroup. Among these features are cortical alveoli, small sacs beneath the cell's surface that act as cushions, providing support and helping to maintain the cell's shape. Additionally, they possess tripartite mastigonemes, complex three-part hair-like structures on their flagella, the whip-like tails used for movement. These structures enhance their swimming capabilities by increasing resistance against water. Furthermore, Telonemia is equipped with filopodia, very thin, thread-like projections extending from the cell body. These projections can serve various purposes, such as aiding in movement or capturing food particles by wrapping around them. Together, the two lineages compose the TSAR clade.

This phylum is monotypic, composed of a single class Telonemea, order Telonemida and family Telonemidae. It is classified in three genera and seven species, although numerous undescribed clades of environmental DNA are known. They are detected in all marine and freshwater environments, where they prey on bacteria and small phytoplankton by engulfing them in their plasma membrane (phagotrophy).

Morphology

The phylum Telonemia comprises microscopic unicellular eukaryotes, or protists. [3] Most of the diversity of telonemids is morphologically uncharacterized. [4] The few described species are free-living predatory phagotrophic flagellates composed of pear-shaped cells with two flagella. These cells measure approximately 5–10 µm in length and 3–7 µm in width. The flagella have different lengths, with the short one measuring up to 12 µm and the long one measuring up to 16 µm. Between the flagella protrudes a short proboscis-like structure, known as a rostrum. Their mitochondrial cristae are tubular. They have a unique multi-layered cytoskeleton of high complexity, composed of layers of microfilaments and microtubules, unseen in any other eukaryote. [4] They exhibit a unique combination of cell traits that were previously believed to be exclusive to different chromalveolate groups, such as complex tripartite mastigonemes (as in stramenopiles), cortical alveoli-like structures (as in alveolates) and filopodia (as in rhizarians). [4] Despite their evolutionary proximity to chromalveolates, they lack chloroplasts. [1]

Ecology and distribution

Telonemids feed on a wide range of organisms, namely bacteria and phytoplankton ranging in size between pico- and nanoplankton. They are widely distributed and are sometimes abundant, implying they may play an important ecological role in aquatic ecosystems. [4] Around one hundred clades of environmental sequences from undescribed telonemids have been recovered in a variety of marine locations (Antarctic, Arctic and Indian Oceans; Mediterranean, Baltic, Kara, Marmara and White seas), including deep sea, and freshwater bodies from different regions (Norway, France, Antarctica, Finland, Canada, Japan). [5] [6] [4] Several telonemid clades favor open waters with lower nutrients, such as the Canada Basin and offshore the Mackenzie River, suggesting that they are able to thrive in low-productivity ecosystems (i.e. oligotrophic). [7]

Systematics

History

The first telonemid genus and species, Telonema subtile , was described by Karl Griessmann in 1913 from crude cultures of the green alga Ulva and of red algae off the coast of Roscoff and Naples. [8] Eighty years later, in 1993, American protistologist Thomas Cavalier-Smith created a family Telonemidae, order Telonemida and class Telonemea to contain this protist. Initially, this group was included within the now obsolete phylum Opalozoa, along with other unrelated groups of flagellates such as apusomonads, jakobids, cercomonads, spongomonads, katablepharids, ebriids, proteomyxids and so on. In this scheme, the class Telonemea was distinguished by the presence of two posterior cilia of equal length (isokont cilia). It contained an additional order besides Telonemida, Nephromycida, which comprised the genus Nephromyces [2] (later treated as an apicomplexan). [9] In 2005 a second species of telonemid was described, T. antarcticum, from the surface waters of the Oslofjord. [10]

Since 2006, Telonemea was separated into a new eukaryotic phylum Telonemia by protistologist Kamran Shalchian-Tabrizi and coauthors, on the basis of phylogenetic analyses that placed it near chromalveolate groups such as Haptista and Cryptista. [1] However, in 2015, Cavalier-Smith and coauthors rejected their treatment as an independent phylum and transferred Telonemea to the phylum Cryptista, under the obsolete subphylum Corbihelia. This subphylum included other protists with a pharyngeal basket or radiating axopodia [11] such as Picomonas (later classified as a separate phylum Picozoa closely related to red algae) [12] and Microheliella (now proposed as the sister group to Cryptista). [13] In addition, they transferred T. antarcticum to a new genus Lateronema , on the basis of phylogenetic distance from Telonema. [11]

Numerous phylogenetic analyses in the following years solidified the position of Telonemia as the sister clade to the SAR supergroup, both collectively composing the TSAR clade (Telonemia, Stramenopila, Alveolata and Rhizaria), [14] which lead Cavalier-Smith to finally consider Telonemia a separate phylum in 2022. [15] In the same year, five more species and a third genus, Arpakorses , were described by protistologist Denis Victorovich Tikhonenkov and coauthors. [4]

Classification

Until 2019, only two species had been formally described, [14] although DNA sequences collected from seawater suggested there were many more species not yet described. [16] In 2022, five additional species were described along with a third new genus, bringing the total number of species to seven. [4]

Evolution

Telonemia on the eukaryote tree of life
  Eukaryotes  
Diaphoretickes   
  TSAR  
  SAR  

Stramenopila

Alveolata

Rhizaria

Telonemia

Haptista

Cryptista

Archaeplastida

  Amorphea  

Amoebozoa

Obazoa

CRuMs

Excavates

Hemimastigophora

Cladogram of eukaryotes based on revisions of the 2020 decade, showing in bold the position of Telonemia. [17] [18]

Telonemia is a clade of protists that branch independently from other eukaryotic supergroups groups as their own 'micro-kingdom'. [19] Early molecular analyses of Telonemia placed them as an independent branch within the SAR supergroup, a diverse clade of eukaryotes that contain Rhizaria, Alveolata and Stramenopila. [20] Other analyses proposed a close relationship with centrohelids, katablepharids, cryptomonads and haptophytes. [21] [11] At this time, they were suggested to have evolutionary significance in being a possible transitional form between ecologically important heterotrophic and photosynthetic species among chromalveolates. [1]

The present phylogenetic analyses place them as sister to the SAR supergroup in a clade commonly known as TSAR, [14] [4] which is widely accepted by the scientific community. [17] [18] As the sister clade to SAR, Telonemia has a key position in the tree of eukaryotic life. They are morphologically complex organisms that combine characteristics of different SAR lineages. The main trait uniting each SAR lineage has been described in at least one genus of Telonemia: tripartite mastigonemes in the flagella, typical of stramenopiles and described in Lateronema ; cortical alveoli underneath the plasma membrane, typical of alveolates and described in Lateronema; and fine pseudopodia (filopodia), typical of rhizarians and described in Telonema . Moreover, Arpakorses presents a kinetid structure similar to that seen in Rhizaria, and Telonema subtile presents microtubules in a formation superficially resembling the apical complex of apicomplexans. [4]

All telonemid genera possess a highly intricate multi-layered cytoskeleton, whose complexity is not found in any other eukaryote. This finding may indicate that telonemids have retained an ancestral cytoskeleton organization that has been lost in other eukaryotes. [4]

Related Research Articles

<span class="mw-page-title-main">Centrohelid</span> Group of algae

The centrohelids or centroheliozoa are a large group of heliozoan protists. They include both mobile and sessile forms, found in freshwater and marine environments, especially at some depth.

<span class="mw-page-title-main">Chromista</span> Eukaryotic biological kingdom

Chromista is a proposed but polyphyletic biological kingdom, refined from the Chromalveolata, consisting of single-celled and multicellular eukaryotic species that share similar features in their photosynthetic organelles (plastids). It includes all eukaryotes whose plastids contain chlorophyll c and are surrounded by four membranes. If the ancestor already possessed chloroplasts derived by endosymbiosis from red algae, all non-photosynthetic Chromista have secondarily lost the ability to photosynthesise. Its members might have arisen independently as separate evolutionary groups from the last eukaryotic common ancestor.

<span class="mw-page-title-main">Cercozoa</span> Group of single-celled organisms

Cercozoa is a phylum of diverse single-celled eukaryotes. They lack shared morphological characteristics at the microscopic level, and are instead united by molecular phylogenies of rRNA and actin or polyubiquitin. They were the first major eukaryotic group to be recognized mainly through molecular phylogenies. They are the natural predators of many species of bacteria. They are closely related to the phylum Retaria, comprising amoeboids that usually have complex shells, and together form a supergroup called Rhizaria.

<span class="mw-page-title-main">Opisthokont</span> Group of eukaryotes which includes animals and fungi, among other groups

The opisthokonts are a broad group of eukaryotes, including both the animal and fungus kingdoms. The opisthokonts, previously called the "Fungi/Metazoa group", are generally recognized as a clade. Opisthokonts together with Apusomonadida and Breviata comprise the larger clade Obazoa.

<span class="mw-page-title-main">Rhizaria</span> Infrakingdom of protists

The Rhizaria are a diverse and species-rich supergroup of mostly unicellular eukaryotes. Except for the Chlorarachniophytes and three species in the genus Paulinella in the phylum Cercozoa, they are all non-photosynthethic, but many foraminifera and radiolaria have a symbiotic relationship with unicellular algae. A multicellular form, Guttulinopsis vulgaris, a cellular slime mold, has been described. This group was used by Cavalier-Smith in 2002, although the term "Rhizaria" had been long used for clades within the currently recognized taxon. Being described mainly from rDNA sequences, they vary considerably in form, having no clear morphological distinctive characters (synapomorphies), but for the most part they are amoeboids with filose, reticulose, or microtubule-supported pseudopods. In the absence of an apomorphy, the group is ill-defined, and its composition has been very fluid. Some Rhizaria possess mineral exoskeletons, which are in different clades within Rhizaria made out of opal, celestite, or calcite. Certain species can attain sizes of more than a centimeter with some species being able to form cylindrical colonies approximately 1 cm in diameter and greater than 1 m in length. They feed by capturing and engulfing prey with the extensions of their pseudopodia; forms that are symbiotic with unicellular algae contribute significantly to the total primary production of the ocean.

<span class="mw-page-title-main">Amorphea</span> Members of the Unikonta, a taxonomic group proposed by Thomas Cavalier-Smith

Amorphea is a taxonomic supergroup that includes the basal Amoebozoa and Obazoa. That latter contains the Opisthokonta, which includes the Fungi, Animals and the Choanomonada, or Choanoflagellates. The taxonomic affinities of the members of this clade were originally described and proposed by Thomas Cavalier-Smith in 2002.

<span class="mw-page-title-main">Bikont</span> Group of eukaryotes

A bikont is any of the eukaryotic organisms classified in the group Bikonta. Many single-celled and multi-celled organisms are members of the group, and these, as well as the presumed ancestor, have two flagella.

<span class="mw-page-title-main">Chromalveolata</span> Group of eukaryotic organisms

Chromalveolata was a eukaryote supergroup present in a major classification of 2005, then regarded as one of the six major groups within the eukaryotes. It was a refinement of the kingdom Chromista, first proposed by Thomas Cavalier-Smith in 1981. Chromalveolata was proposed to represent the organisms descended from a single secondary endosymbiosis involving a red alga and a bikont. The plastids in these organisms are those that contain chlorophyll c.

<span class="mw-page-title-main">SAR supergroup</span> Eukaryotes superphylum

SAR or Harosa is a highly diverse clade of eukaryotes, often considered a supergroup, that includes stramenopiles (heterokonts), alveolates, and rhizarians. It is a node-based taxon, including all descendants of the three groups' last common ancestor, and comprises most of the now-rejected Chromalveolata. Their sister group has been found to be telonemids, with which they make up the TSAR clade.

<span class="mw-page-title-main">Hacrobia</span> Group of algae

The cryptomonads-haptophytes assemblage is a proposed but disputed monophyletic grouping of unicellular eukaryotes that are not included in the SAR supergroup. Several alternative names have been used for the group, including Hacrobia ; CCTH ; and "Eukaryomonadae".

<span class="mw-page-title-main">Holozoa</span> Clade containing animals and some protists

Holozoa is a clade of organisms that includes animals and their closest single-celled relatives, but excludes fungi and all other organisms. Together they amount to more than 1.5 million species of purely heterotrophic organisms, including around 300 unicellular species. It consists of various subgroups, namely Metazoa and the protists Choanoflagellata, Filasterea, Pluriformea and Ichthyosporea. Along with fungi and some other groups, Holozoa is part of the Opisthokonta, a supergroup of eukaryotes. Choanofila was previously used as the name for a group similar in composition to Holozoa, but its usage is discouraged now because it excludes animals and is therefore paraphyletic.

Telonema is a genus of single-celled organisms.

<span class="mw-page-title-main">Diaphoretickes</span> Taxon of eukaryotes

Diaphoretickes is a major group of eukaryotic organisms, with over 400,000 species. The majority of the earth's biomass that carries out photosynthesis belongs to Diaphoretickes.

<span class="mw-page-title-main">Halvaria</span> Infrakingdom of protists

Halvaria is a taxonomic grouping of protists that includes Alveolata and Stramenopiles (Heterokonta).

<span class="mw-page-title-main">Cryptista</span> Phylum of algae

Cryptista is a clade of alga-like eukaryotes. It is most likely related to Archaeplastida which includes plants and many algae, within the larger group Diaphoretickes.

<span class="mw-page-title-main">Haptista</span> Group of protists

Haptista is a proposed group of protists made up of centrohelids and haptophytes. Phylogenomic studies indicate that Haptista, together with Ancoracysta twista, forms a sister clade to the SAR+Telonemia supergroup, but it may also be sister to the Cryptista (+Archaeplastida). It is thus one of the earliest diverging Diaphoretickes.

Endohelea is a proposed clade of eukaryotes that are related to Archaeplastida and the SAR supergroup. They used to be considered heliozoans, but phylogenetically they belong to a group of microorganisms known as Cryptista.

Corbihelia is a proposed phylum of eukaryotes.

Mantamonads are a group of free-living heterotrophic flagellates that move primarily by gliding on surfaces. They are classified as one genus Mantamonas in the monotypic family Mantamonadidae, order Mantamonadida and class Glissodiscea. Previously, they were classified in Apusozoa as sister of the Apusmonadida on the basis of rRNA analyses. However, mantamonads are currently placed in CRuMs on the basis of phylogenomic analyses that identify their closest relatives as the Diphylleida and Rigifilida.

A supergroup, in evolutionary biology, is a large group of organisms that share one common ancestor and have important defining characteristics. It is an informal, mostly arbitrary rank in biological taxonomy that is often greater than phylum or kingdom, although some supergroups are also treated as phyla.

References

  1. 1 2 3 4 Shalchian-Tabrizi, K; Eikrem, W; Klaveness, D; Vaulot, D; Minge, M.A; Le Gall, F; Romari, K; Throndsen, J; Botnen, A; Massana, R; Thomsen, H.A; Jakobsen, K.S (28 April 2006). "Telonemia, a new protist phylum with affinity to chromist lineages". Proceedings of the Royal Society B: Biological Sciences. 273 (1595): 1833–1842. doi:10.1098/rspb.2006.3515. PMC   1634789 . PMID   16790418.
  2. 1 2 3 4 Cavalier-Smith, Thomas (1993). "The Protozoan Phylum Opalozoa". The Journal of Eukaryotic Microbiology. 40 (5): 609–615. doi:10.1111/j.1550-7408.1993.tb06117.x. S2CID   84129692.
  3. ↑ Vogt, Yngve (February 1, 2012). "Found Unknown Group of Oceanic Life Forms". Apollon.
  4. 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 Tikhonenkov, Denis V.; Jamy, Mahwash; Borodina, Anastasia S.; Belyaev, Artem O.; Zagumyonnyi, Dmitry G.; Prokina, Kristina I.; Mylnikov, Alexander P.; Burki, Fabien; Karpov, Sergey A. (2022). "On the origin of TSAR: morphology, diversity and phylogeny of Telonemia". Open Biology. The Royal Society. 12 (3). doi: 10.1098/rsob.210325 . ISSN   2046-2441. PMC   8924772 . PMID   35291881.
  5. ↑ Bråte, Jon; Klaveness, Dag; Rygh, Tellef; Jakobsen, Kjetill S; Shalchian-Tabrizi, Kamran (2010). "Telonemia-specific environmental 18S rDNA PCR reveals unknown diversity and multiple marine-freshwater colonizations". BMC Microbiology. 10 (1): 168. doi: 10.1186/1471-2180-10-168 . PMC   2891722 . PMID   20534135.
  6. ↑ Lefèvre, Emilie; Roussel, Balbine; Amblard, Christian; Sime-Ngando, Télesphore; Ibelings, Bas (11 June 2008). "The Molecular Diversity of Freshwater Picoeukaryotes Reveals High Occurrence of Putative Parasitoids in the Plankton". PLOS ONE. 3 (6): e2324. Bibcode:2008PLoSO...3.2324L. doi: 10.1371/journal.pone.0002324 . PMC   2396521 . PMID   18545660.
  7. ↑ Thaler M, Lovejoy C (2015). "Biogeography of Heterotrophic Flagellate Populations Indicates the Presence of Generalist and Specialist Taxa in the Arctic Ocean". Applied and Environmental Microbiology. 81 (6): 2137–2148. doi:10.1128/AEM.02737-14.
  8. 1 2 Grießmann, Karl (1913). Über marine Flagellaten[About marine flagellates] (Thesis) (in German). Fischer. OCLC   638176877.
  9. ↑ Muñoz-Gómez, Sergio A.; Durnin, Keira; Eme, Laura; Paight, Christopher; Lane, Christopher E.; Saffo, Mary B.; Slamovits, Claudio H. (2019). "Nephromyces Represents a Diverse and Novel Lineage of the Apicomplexa That Has Retained Apicoplasts". Genome Biology and Evolution. 11 (10): 2727–2740. doi: 10.1093/gbe/evz155 . PMC   6777426 .
  10. 1 2 Klaveness, Dag; Shalchian-Tabrizi, Kamran; Thomsen, Helge Abildhauge; Eikrem, Wenche; Jakobsen, Kjetill S. (2005). "Telonema antarcticum sp. nov., a common marine phagotrophic flagellate". International Journal of Systematic and Evolutionary Microbiology. The Microbiology Society. 55: 2595–2604. doi: 10.1099/ijs.0.63652-0 .
  11. 1 2 3 4 5 Cavalier-Smith, Thomas; Chao, Ema E.; Lewis, Rhodri (December 2015). "Multiple origins of Heliozoa from flagellate ancestors: New cryptist subphylum Corbihelia, superclass Corbistoma, and monophyly of Haptista, Cryptista, Hacrobia and Chromista". Molecular Phylogenetics and Evolution. 93: 331–362. doi: 10.1016/j.ympev.2015.07.004 . PMID   26234272.
  12. ↑ Schön, Max E.; Zlatogursky, Vasily V.; Singh, Rohan P.; Poirier, Camille; Wilken, Susanne; Mathur, Varsha; Strassert, Jürgen F. H.; Pinhassi, Jarone; Worden, Alexandra Z.; Keeling, Patrick J.; Ettema, Thijs J. G.; Wideman, Jeremy G.; Burki, Fabien (2021). "Single cell genomics reveals plastid-lacking Picozoa are close relatives of red algae". Nature Communications. 12: 6651. doi: 10.1038/s41467-021-26918-0 .
  13. ↑ Yazaki, Euki; Yabuki, Akinori; Imaizumi, Ayaka; Kume, Keitaro; Hashimoto, Tetsuo; Inagaki, Yuji (2022). "The closest lineage of Archaeplastida is revealed by phylogenomics analyses that include Microheliella maris". Open Biol. 12: 210376. doi:10.1098/rsob.210376. PMC   9006020 .
  14. 1 2 3 Strassert, Jürgen F H; Jamy, Mahwash; Mylnikov, Alexander P; Tikhonenkov, Denis V; Burki, Fabien; Shapiro, Beth (April 2019). "New Phylogenomic Analysis of the Enigmatic Phylum Telonemia Further Resolves the Eukaryote Tree of Life". Molecular Biology and Evolution. 36 (4): 757–765. doi: 10.1093/molbev/msz012 . PMC   6844682 . PMID   30668767.
  15. ↑ Cavalier-Smith, Thomas (2022). "Ciliary transition zone evolution and the root of the eukaryote tree: implications for opisthokont origin and classification of kingdoms Protozoa, Plantae, and Fungi". Protoplasma. 259: 487–593. doi: 10.1007/s00709-021-01665-7 . PMC   9010356 .
  16. ↑ Shalchian-Tabrizi, K; Kauserud, H; Massana, R; Klaveness, D; Jakobsen, KS (18 April 2007). "Analysis of Environmental 18S Ribosomal RNA Sequences reveals Unknown Diversity of the Cosmopolitan Phylum Telonemia". Protist. 158 (2): 173–180. doi:10.1016/j.protis.2006.10.003. PMID   17196879.
  17. 1 2 Burki, Fabien; Roger, Andrew J.; Brown, Matthew W.; Simpson, Alastair G.B. (2020). "The New Tree of Eukaryotes". Trends in Ecology & Evolution. 35 (1): 43–55. doi: 10.1016/j.tree.2019.08.008 .
  18. 1 2 Burki, Fabien; Sandin, Miguel M.; Jamy, Mahwash (2021). "Diversity and ecology of protists revealed by metabarcoding". Current Biology. 31 (19): R1267–R1280. doi: 10.1016/j.cub.2021.07.066 .
  19. ↑ Pawlowski, Jan (15 April 2013). "The new micro-kingdoms of eukaryotes". BMC Biology. 11: 40. doi: 10.1186/1741-7007-11-40 . PMC   3626909 . PMID   23587248.
  20. ↑ Reeb, Valérie C.; Peglar, Michael T.; Yoon, Hwan Su; et al. (October 2009). "Interrelationships of chromalveolates within a broadly sampled tree of photosynthetic protists". Molecular Phylogenetics and Evolution. 53 (1): 202–211. doi:10.1016/j.ympev.2009.04.012. PMID   19398025.
  21. ↑ Burki, Fabien; Inagaki, Yuji; Bråte, Jon; et al. (2009). "Large-Scale Phylogenomic Analyses Reveal That Two Enigmatic Protist Lineages, Telonemia and Centroheliozoa, Are Related to Photosynthetic Chromalveolates". Genome Biology and Evolution. 1: 231–238. doi:10.1093/gbe/evp022. PMC   2817417 . PMID   20333193.
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