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Telonemia

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Telonemia
Telonema rivulare by interference contrast micrography
Scientific classification Edit this classification
Domain: Eukaryota
Clade: Diaphoretickes
Clade: TSAR
Phylum: Telonemia
Shalchian-Tabrizi 2006[2]
Class: Telonemea
Cavalier-Smith 1993[1]
Order: Telonemida
Cavalier-Smith 1993[1]
Family: Telonemidae
Cavalier-Smith 1993[1]
Genera
Diversity
7 species
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.

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

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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.[2]

Ecology and distribution

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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

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History

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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[1] (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.[2] 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

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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

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Telonemia on the eukaryote tree of life
 Eukaryotes 
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.[2]

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]

References

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  1. ^ a b c d 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.
  2. ^ a b c d 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.
  3. ^ Vogt, Yngve (February 1, 2012). "Found Unknown Group of Oceanic Life Forms". Apollon.
  4. ^ a b c d e f g h i j k l m n o p 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. 12 (3). The Royal Society. 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. PMC 4345384.
  8. ^ a b 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. ^ a b 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. 55. The Microbiology Society: 2595–2604. doi:10.1099/ijs.0.63652-0.
  11. ^ a b c d e 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. ^ a b c 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. ^ a b 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. ^ a b 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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