Biology:Hyalospheniidae

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Short description: Family of testate amoebae

Hyalospheniidae
Temporal range: Middle Devonian[1] 370–0 Ma
Hyalosphenia papilio from Hawley Bog Massachusetts.jpg
Hyalosphenia papilio
Scientific classification e
Domain: Eukaryota
Phylum: Amoebozoa
Class: Tubulinea
Order: Arcellinida
Suborder: Glutinoconcha
Infraorder: Hyalospheniformes
Lahr et al. 2019[4]
Family: Hyalospheniidae
Schulze, 1877[2] emend. Kosakyan & Lara, 2012[3]
Type genus
Hyalosphenia
Stein 1857
Diversity
78 species
Synonyms[5]
Nebelidae
Taranek 1882[6]

Hyalospheniidae is a family of arcellinid testate amoebae and the sole family of the infraorder Hyalospheniformes. Commonly referred to as "hyalospheniids", these lobose amoebae are characterized by their ability to generate a shell composed of either organic matter or siliceous particles that may be recycled from euglyphid amoebae. They inhabit soil or freshwater habitats, and are abundant on Sphagnum mosses.

Hyalospheniid amoebae originated after the middle Devonian, around 370 million years ago. They are considered important bioindicators, and are frequently used for environmental monitoring. Their fossils are studied to investigate the paleoecology of prehistoric wetland habitats. The classification of hyalospheniids has changed several times since the 19th century based on morphological criteria. Initially classified as two separate families, Hyalospheniidae and Nebelidae, they were later proven to be synonymous through phylogenetic analyses.

Morphology

Hyalospheniidae are testate amoebae—unicellular amoeboid protists that generate mineral agglutinated shells. They are characterized by ovoid, pyriform, vase or flask-shaped shells, which are laterally compressed.[7][8] Shell construction and composition varies substantially within the family. It can be either entirely secreted by their own cells and composed of an organic matrix (e.g. Hyalosphenia), or have additional non-organic siliceous scales. These mineral scales can also be self-secreted (e.g. Quadrulella), or can be recycled from the shell plates of small euglyphid amoebae or other similar material such as diatom frustules (e.g. Apodera, Padaungiella, Nebela).[7] The trait of recycling shell plates from euglyphids is known as "kleptosquamy", and appears to be an ancestral trait within the family.[1]

Organic material (Hyalosphenia)
Siliceous elements (Planocarina)
The two main types of shell construction among hyalospheniids

Ecology

Hyalospheniid amoebae are considered important bioindicators in environmental monitoring studies. Their sensitivity to environmental changes, such as atmospheric pollution,[9] make them reliable indicators of hydrological changes. Together with the preservation of their shells over thousands of years, their environmental sensitivity gives them a prominent role in the reconstruction of the paleoclimate in peatlands, bogs and fens.[7]

This family includes several of the most common, well-studied lobose testate amoebae. Its members are especially diverse and abundant in oligotrophic wetland ecosystems, such as peatlands dominated by Sphagnum mosses. Some of them can also be found in different mosses, freshwater habitats, and soil. Although multiple hyalospheniid species have a cosmopolitan distribution, many species are restricted to the Southern hemisphere and the tropical range within the Northern hemisphere.[8]

One species, Hyalosphenia papilio, has been observed with photosynthetic endosymbionts (zoochlorellae).[10] This species is an obligate mixotroph, living in constant association with intracellular symbionts belonging to the green algal class Trebouxiophyceae, specifically algae from the family Chlorellaceae.[11]

Evolution

Arcellinida
 

Phryganellina

 
 
 

Organoconcha

 
Glutinoconcha
 

Volnustoma

 
 
 
 

Hyalospheniformes

 
 
 

Excentrosoma

 
 

Cylindrothecina

 
 
 
 
 

Longithecina

 
 

Sphaerothecina

 
 
 
 
 
 
Position of hyalosphenids in the arcellinid phylogeny.[12]

Hyalospheniidae is a family of Arcellinida, an order of lobose testate amoebae within the eukaryotic supergroup Amoebozoa. In contrast to filose testate amoebae, found within the supergroup Rhizaria (e.g. euglyphid amoebae), they present thicker pseudopods with blunt ends. It is the only family of the infraorder Hyalospheniformes, which belongs to the suborder Glutinoconcha. Glutinoconcha, which contains the majority of arcellinid species, evolved from a common ancestor with mineral agglutinated shells, in contrast to the organic shells of Organoconcha. In particular, Hyalospheniformes and Volnustoma, a different infraorder of Glutinoconcha, both evolved from ancestors with xenosomic agglutinated shells (i.e. composed of particles incorporated from an external source).[4][12]

Through molecular clock approximations, the age of Hyalospheniidae was estimated in 2015 to be around 370 million years old, between the Devonian and the early Carboniferous. This molecular reconstruction suggests that hyalospheniids diversified after the middle Devonian, when the diversification of land plants formed extensive forests with an abundant production of organic matter and soils. Kleptosquamy, the ability of hyalosphenid amoebae to "steal" test scales from their prey, euglyphid amoebae, is hypothesized to be an ancestral trait within the family. This working hypothesis is based on the presence of kleptosquamy on most hyalospheniids.[1] In addition to the molecular clock estimates, it has been suggested that 750–million-year-old vase-shaped microfossils could belong to this family.[13][7][14]

Systematics

History of taxonomy

There has been several attempts at classifying Hyalospheniidae among testate amoebae, as well as its internal classification. American paleontologist Joseph Leidy, in 1874, was possibly the first to notice common characteristics between the cells. He described the vase-shaped tests as composed of small siliceous particles ("discoid plates and minute rods") caught within an organic matrix, interpreted to be originated by the amoeba ("intrinsic"). He grouped those species within the genus Nebela, restricting them from the previously known genus of testate amoebae Difflugia. Instead, he described Difflugia species as having a "test composed of extraneous bodies, such as particles of quartzose sand, and diatom cases".[15][7]

In 1877, German zoologist Franz Eilhard Schulze described the families Hyalosphenidae, Arcellidae, Quadrulidae and Difflugidae. Amoebae with an organic homogenous test such as Hyalosphenia were placed in Hyalospheniidiae, while Nebela was placed in Difflugidae, and Quadrulella in Quadrulidae.[2][7]

In 1882, Taranek described the family Nebelidae to include amoebae with siliceous plates: Nebela, Lesquereusia, Quadrulella, Corythion (which was later excluded), Amphizonella, Cochliopodium, Hyalosphenia, Leptochlamys and Zonomyxa.[6] This family was redefined later in 1942 by Jung and organized into thirteen genera newly described by him: Alocodera, Apodera, Argynnia, Deflandria, Nebela, Leidyella, Penardiella, Physochila, Porosia, Pterygia, Quadrulella, Schaudinnia and Umbonaria.[16] However, Jung did not designate type species in his classification, which invalidated all genera with more than one species.[lower-alpha 1] Consequently, only monotypic genera such as Alocodera, Physochila and Porosia were recognized, and the remaining genera were absorbed by Nebela. Later, by assigning types, micropaleontologists Loeblich and Tappan validated Apodera and Certesella in 1961,[18] and Vucetich validated Argynnia in 1974.[19]

In 2002, German protozoologist Ralf Meisterfeld wrote the last review of the family based exclusively on morphological characters. He reclassified Nebela and similar genera into two families: Hyalospheniidae, composed of genera with rigid, chitinoid, organic tests (Hyalosphenia and Leptochlamys); and Nebelidae, composed of genera with tests constructed from plates of small euglyphids or diatom fragments (Apodera, Argynnia, Certesella, Nebela, Physochila, Porosia, Schoenbornia). Following a 1979 classification,[20] he excluded the genus Quadrulella into the family Lesquereusiidae along with other arcellinid genera with self-secreted siliceous rods in their tests.[21][7]

The first phylogenetic analyses of Arcellinida based on molecular data demonstrated that Nebela and Nebelidae were not monophyletic, i.e. did not form a clade or group of taxa evolved from a common ancestor without including other genera from Hyalospheniidae.[22] Species of Apodera, Porosia, Nebela and Hyalosphenia were intermingled with each other in a clade known as "core Nebelas".[8] Because of this result, and presence of distinguishing Hyalospheniidae traits within some Nebelidae, the two families were synonymised under the first name.[3] In addition, many species of the polyphyletic Nebela were separated into new monophyletic genera, namely Padaungiella in 2012,[3] Cornutheca, Gibbocarina, Longinebela, Mrabella and Planocarina in 2016,[23] and finally Alabasta in 2018.[24]

Hyalosphenid phylogeny
 
 
 
 
 
 
 

Nebela

 
 

Quadrulella

 
 
 
 

Certesella

 
 

? Porosia

 
 
 
 

Longinebela

 
 
 
 

Planocarina

 
 

Alabasta

 
 
 
 
 

Hyalosphenia

 
 
 

Cornutheca

 
 
 

Mrabella

 
 

Gibbocarina

 
 
 
 
 
 
 

Apodera

 
 
 

Alocodera

 
 

Padaungiella

 
 
 
 
Based on a 2018 phylogenetic analysis of most genera,[24] and a 2021 analysis that recovered Apodera as the sister group to Alocodera and Padaungiella.[25] Porosia, excluded from the analyses, is considered a close relative of Certesella.[26]

Classification

The current taxonomy of the family recognizes 14 genera,[4][12] with a total of 78 species:

  • Alabasta Duckert, Blandenier, Kosakyan & Singer 2018 — 3 species.[24]
  • Alocodera Jung, 1942[27] — 1 species.[28]
  • Cornutheca Kosakyan, Lahr, Mulot, Meisterfeld, Mitchell & Lara, 2016 — 3 species.[23]
  • Gibbocarina Kosakyan, Lahr, Mulot, Meisterfeld, Mitchell & Lara, 2016 (=Umbonaria Jung 1942)[31] — 3 species.[23][31]
  • Hyalosphenia (Stein, 1857) Schulze, 1877 — 17 species.[7]
  • Longinebela Kosakyan, Lahr, Mulot, Meisterfeld, Mitchell & Lara, 2016 — 5 species.[23][32]
  • Mrabella Kosakyan, Lahr, Mulot, Meisterfeld, Mitchell & Lara, 2016 — 2 species.[23]
  • Nebela Leidy, 1874 em. Kosakyan, Lahr, Mulot, Meisterfeld, Mitchell & Lara, 2016 — 13 species.[23]
  • Padaungiella Lara et Todorov, 2012 — 5 species.[3]
  • Planocarina Kosakyan, Lahr, Mulot, Meisterfeld, Mitchell & Lara, 2016 — 4 species.[23]
  • Quadrulella Cockerell, 1909 em. Kosakyan, Lahr, Mulot, Meisterfeld, Mitchell & Lara, 2016 — 11 species.[23]

Notes

  1. ↑ Due to article 13.3 of the International Code of Zoological Nomenclature,[7] genera described after 1930 can only be validated if there is a type species designated to them.[17]

References

  1. ↑ 1.0 1.1 1.2 Lahr, Daniel JG; Bosak, Tanja; Lara, Enrique; Mitchell, Edward AD (September 2015). "The Phanerozoic diversification of silica-cycling testate amoebae and its possible links to changes in terrestrial ecosystems". PeerJ 3: e1234. doi:10.7717/peerj.1234. PMID 26734499. 
  2. ↑ 2.0 2.1 "Rhizopodenstudien VI". Archiv für Mikroskopische Anatomie 13: 9–30. 1877. doi:10.1007/BF02933929. https://www.biodiversitylibrary.org/item/49005#page/7/mode/1up. Retrieved 2023-09-24. 
  3. ↑ 3.0 3.1 3.2 3.3 "COI Barcoding of Nebelid Testate Amoebae (Amoebozoa: Arcellinida): Extensive Cryptic Diversity and Redefinition of the Hyalospheniidae Schultze". Protist 163 (3): 415–434. 2012. doi:10.1016/j.protis.2011.10.003. PMID 22130576. 
  4. ↑ 4.0 4.1 4.2 "Phylogenomics and Morphological Reconstruction of Arcellinida Testate Amoebae Highlight Diversity of Microbial Eukaryotes in the Neoproterozoic". Current Biology 29 (6): 991–1001. 2019. doi:10.1016/j.cub.2019.01.078. PMID 30827918. 
  5. ↑ Kosakyan, Anush; Gomaa, Fatma; Lara, Enrique; Lahr, Daniel J.G. (2016). "Current and future perspectives on the systematics, taxonomy and nomenclature of testate amoebae". European Journal of Protistology 55B (Pt B): 105–117. doi:10.1016/j.ejop.2016.02.001. PMID 27004416. 
  6. ↑ 6.0 6.1 "Monographie der Nebeliden Böhmens. Ein Beitrag zur Kenntnis der Süsswasser Monothalamien" (in German). Abhandlungen der Königlichen Böhmischen Gesellschaft der Wissenschaften VI: 1–56. 1882. 
  7. ↑ 7.0 7.1 7.2 7.3 7.4 7.5 7.6 7.7 7.8 7.9 Kosakyan, Anush (16 April 2014). Phylogeny, systematics and ecology of free living protists. Case study: family Hyalospheniidae (Thesis). University of Neuchâtel. Archived from the original on 29 September 2023. Retrieved 24 September 2023.
  8. ↑ 8.0 8.1 8.2 "Ribosomal RNA genes challenge the monophyly of the Hyalospheniidae (Amoebozoa: Arcellinida)". Protist 159 (2): 165–176. 2008. doi:10.1016/j.protis.2007.09.003. PMID 18023614. http://infoscience.epfl.ch/record/109481. Retrieved 2023-10-22. 
  9. ↑ "Can pollution bias peatland paleoclimate reconstruction?". Quaternary Research 78 (2): 170–173. 2012. doi:10.1016/j.yqres.2012.05.004. Bibcode: 2012QuRes..78..170P. 
  10. ↑ "Changes in Testate Amoeba Assemblages in a Series of Different Types of Aquatic and Terrestrial Habitats of Wetland and Forest Ecosystems". Biology Bulletin 50: 1719–1737. 2023. doi:10.1134/S1062359023080332. 
  11. ↑ Gomaa, Fatma; Kosakyan, Anush; Heger, Thierry J.; Corsaro, Daniele; Mitchell, Edward A.D.; Lara, Enrique (2014). "One Alga to Rule them All: Unrelated Mixotrophic Testate Amoebae (Amoebozoa, Rhizaria and Stramenopiles) Share the Same Symbiont (Trebouxiophyceae)". Protist 165 (2): 161–176. doi:10.1016/j.protis.2014.01.002. 
  12. ↑ 12.0 12.1 12.2 González-Miguéns, Rubén; Todorov, Milcho; Blandenier, Quentin; Duckert, Clément; Porfirio-Sousa, Alfredo L.; Ribeiro, Giulia M.; Ramos, Diana; Lahr, Daniel J.G. et al. (2022). "Deconstructing Difflugia: The tangled evolution of lobose testate amoebae shells (Amoebozoa: Arcellinida) illustrates the importance of convergent evolution in protist phylogeny". Molecular Phylogenetics and Evolution 175: 107557. doi:10.1016/j.ympev.2022.107557. PMID 35777650. 
  13. ↑ "Vase-shaped microfossils from the Neoproterozoic Chuar Group, Grand Canyon: a classification guided by modern testate amoebae". Journal of Paleontology 77 (3): 409–429. May 2003. doi:10.1666/0022-3360(2003)077<0409:VMFTNC>2.0.CO;2. http://www.geol.ucsb.edu/faculty/porter/Papers/Porteretal2003_VSMs.pdf. Retrieved 2023-09-24. 
  14. ↑ "Organic preservation of vase-shaped microfossils from the late Tonian Chuar Group, Grand Canyon, Arizona, USA". Geobiology 21 (3): 290–309. 2023. doi:10.1111/gbi.12544. PMID 36651474. 
  15. ↑ "Notice of some new freshwater rhizopods". Annals and Magazine of Natural History 14 (83): 383–385. 1874. doi:10.1080/00222937408680997. https://ia800708.us.archive.org/view_archive.php?archive=/22/items/crossref-pre-1909-scholarly-works/10.1080%252F00222937408680992.zip&file=10.1080%252F00222937408680997.pdf. 
  16. ↑ "Illustrierte Thekamöben-Bestimmungstabellen I. Die Systematik der Nebelinen" (in German). Archiv für Protistenkunde 95: 357–390. 1942. 
  17. ↑ "ICZN Code Art. 13". https://code.iczn.org/chapter-4-criteria-of-availability/article-13-names-published-after-1930/. 
  18. ↑ Loeblich, Alfred Richard; Tappan, Helen Niña (1961). "Remarks on the systematics of the Sarkodina (Protozoa), renamed homonyms and new and validated genera". Proceedings of the Biological Society of Washington 74: 213–234. https://www.biodiversitylibrary.org/page/34571345#page/251/mode/1up. Retrieved 2023-09-24. 
  19. ↑ "Comentarios criticos sobre Argynnia Jung, 1942 (Rhizopoda, Testacea)" (in Spanish). Neotropica 20 (63): 126–128. 1974. 
  20. ↑ "Siliceous structures secreted by members of the subclass Lobosia (Rhizopodea, Protozoa)". Bulletin of the British Museum (Natural History) Zoology 36: 203–207. 1979. https://biostor.org/reference/107. Retrieved 2023-10-22. 
  21. ↑ "Order Arcellinida Kent, 1880". An illustrated guide to the protozoa: organisms traditionally referred to as protozoa, or newly discovered groups (2nd ed.). Lawrence, Kansas, USA: Society of protozoologists. 2002. pp. 827–860. https://protistologists.org/wp-content/uploads/2023/07/20ARCELLINIDA.pdf. Retrieved 2023-09-25. 
  22. ↑ "The testate lobose amoebae (order Arcellinida Kent, 1880) finally find their home within Amoebozoa". Protist 156 (2): 191–202. 2005. doi:10.1016/j.protis.2005.03.002. PMID 16171186. 
  23. ↑ 23.0 23.1 23.2 23.3 23.4 23.5 23.6 23.7 Kosakyan, Anush; Lahr, Daniel J. G.; Mulot, Matthieu; Meisterfeld, Ralf; Mitchell, Edward A. D.; Lara, Enrique (2016). "Phylogenetic reconstruction based on COI reshuffles the taxonomy of hyalosphenid shelled (testate) amoebae and reveals the convoluted evolution of shell plate shapes". Cladistics 32 (6): 606–623. doi:10.1111/cla.12167. PMID 34727671. 
  24. ↑ 24.0 24.1 24.2 "En garde! Redefinition of Nebela militaris (Arcellinida, Hyalospheniidae) and erection of Alabasta gen. nov.". European Journal of Protistology 66: 156–165. 2018. doi:10.1016/j.ejop.2018.08.005. PMID 30366198. http://doc.rero.ch/record/323497/files/Duckert_C.-En_garde-20181136.pdf. Retrieved 2023-01-03. 
  25. ↑ 25.0 25.1 "Superficially described and ignored for 92 years, rediscovered and emended: Apodera angatakere (Amoebozoa: Arcellinida: Hyalospheniformes) is a new flagship testate amoeba taxon from Aotearoa (New Zealand)". Journal of Eukaryotic Microbiology 68 (6): e12867. 2021. doi:10.1111/jeu.12867. PMID 34351666. 
  26. ↑ 26.0 26.1 Bobrov, Anatoly; Kosakyan, Anush. "A New Species from Mountain Forest Soils in Japan: Porosia paracarinata sp. nov., and Taxonomic Concept of the Genus Porosia Jung, 1942". Acta Protozoologica 54 (4): 289–294. doi:10.4467/16890027AP.15.024.3538. 
  27. ↑ 27.0 27.1 "Südchilenische Thekamöben". Archiv für Protistenkunde 95: 253–356. 1942. 
  28. ↑ Luketa, Stefan (2015). "Description of the family Padaungiellidae and morphological variability of Padaungiella lageniformis (Amoebozoides: Arcellinida) from the Vlasina Lake area, Serbia". Archives of Biological Sciences, Belgrade 67 (4): 1331–1337. doi:10.2298/ABS150312110L. 
  29. ↑ Bobrov, Anatoly; Duckert, Clément; Mitchell, Edward A. D. (2021). "Certesella larai (Amoebozoa: Arcellinida: Hyalospheniformes) a new soil testate amoeba species from the Dominican Republic and Chile challenges the definition of genera Certesella and Porosia". Acta Protozoologica 60: 61–75. doi:10.4467/16890027AP.21.007.15381. 
  30. ↑ Vucetich, María Cristina (1978). "Comentarios sobre el género Certesella Loeblich & Tappan, 1961 y estudio de la estéreo ultraestructura tecal de tres especies austroamericanas (Rhizopoda Testaceolobosa)" (in Spanish). Obra Centenario, Museo de la Plata, Zoología 6: 305–313. http://naturalis.fcnym.unlp.edu.ar/repositorio/_documentos/sipcyt/bfa001237.pdf. Retrieved 2023-09-23. 
  31. ↑ 31.0 31.1 Luketa, Stefan (2017). "Morphological variability of Gibbocarina galeata and G. penardiana comb. nov. (Arcellinida: Hyalospheniidae) from East Herzegovina". Protistology 11 (1): 37–47. doi:10.21685/1680-0826-2017-11-1-3. https://www.researchgate.net/publication/318949582. 
  32. ↑ Todorov, Milcho; Bankov, Nikola; Ganeva, Anna (2018). "Longinebela ampulla sp. n. (Arcellinida: Hyalospheniidae), a New Testate Amoeba from Sphagnum Peatlands in Bulgaria". Acta Zoologica Bulgarica 70 (3): 285–292. https://www.acta-zoologica-bulgarica.eu/downloads/acta-zoologica-bulgarica/2018/70-3-285-292.pdf. Retrieved 2023-10-22. 

Wikidata ☰ Q2209049 entry



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