Triangulopteris lacunata gen. et sp. nov. (Centroplasthelida), a New Centrohelid Heliozoan from Soil †
Abstract
:1. Introduction
2. Materials and Methods
2.1. Clone Isolation
2.2. Light and Electron Microscopy
2.3. Molecular Phylogeny
3. Results
3.1. Cell Morphology of Triangulopteris lacunata gen. et sp. nov.
Type Strain: HF-25 (Kolyma Lowland)
3.2. Spicules-Bearing Stage
3.3. Phylogenetic Analysis
4. Discussion
Taxonomic Summary
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Mikrjukov, K.A. Centrohelid Heliozoans (Centroheliozoa); KMK Scientific Press: Moscow, Russia, 2002; 136p. [Google Scholar]
- Burki, F.; Kaplan, M.; Tikhonenkov, D.V.; Zlatogursky, V.; Minh, B.Q.; Radaykina, L.V.; Smirnov, A.; Mylnikov, A.P.; Keeling, P.J. Untangling the early diversification of eukaryotes: A phylogenomic study of the evolutionary origins of Centrohelida, Haptophyta and Cryptista. Proc. R. Soc. B 2016, 283, 20152802. [Google Scholar] [CrossRef] [Green Version]
- Bardele, C.F. The fine structure of the centrohelidian heliozoan Heterophrys marina. Cell Tissue Res. 1975, 161, 85–102. [Google Scholar] [CrossRef] [PubMed]
- Bardele, C.F. Comparative study of axopodial microtubule patterns and possible mechanisms of pattern control in the centrohelidian heliozoa Acanthocystis, Raphidiophrys and Heterophrys. J. Cell Sci. 1977, 25, 205–232. [Google Scholar] [CrossRef] [PubMed]
- Febvre-Chevalier, C.; Febvre, J. Axonemal microtubule pattern of Cienkowskya mereschkovskyi and a revision of heliozoan taxonomy. Orig. Life 1984, 13, 315–338. [Google Scholar] [CrossRef]
- Siemensma, F.J. Klasse Heliozoa Haeckel, 1866. In Nackte Rhizopoda und Heliozoea. Protozoenfauna, Bd 2; Gustav Fischer Verlag, Stuttgart: New York, NY, USA, 1991; pp. 171–297. [Google Scholar]
- Zlatogursky, V.V.; Drachko, D.; Klimov, V.I.; Shɨshkin, Y. On the phylogenetic position of the genus Raphidocystis (Haptista: Centroplasthelida) with notes on the dimorphism in centrohelid life cycle. Eur. J. Protistol. 2018, 64, 82–90. [Google Scholar] [CrossRef]
- Drachko, D.; Shishkin, Y.; Zlatogursky, V.V. Phenotypic masquerade: Polymorphism in the life cycle of the centrohelid heliozoan Raphidiophrys heterophryoidea (Haptista: Centroplasthelida). Eur. J. Protistol. 2020, 73, 125686. [Google Scholar] [CrossRef] [PubMed]
- Cavalier-Smith, T.; Chao, E.E. Oxnerella micra sp. n. (Oxnerellidae fam. n.), a tiny naked centrohelid, and the diversity and evolution of heliozoan. Protist 2012, 163, 574–601. [Google Scholar] [CrossRef] [PubMed]
- Cavalier-Smith, T.; von der Heyden, S. Molecular phylogeny, scale evolution and taxonomy of centrohelid heliozoan. Mol. Phylogenet. Evol. 2007, 44, 1186–1203. [Google Scholar] [CrossRef]
- Triadó-Margarit, X.; Casamayor, E.O. High genetic diversity and novelty in planktonic protists inhabiting inland and coastal high salinity water bodies. FEMS Microbiol. Ecol. 2013, 85, 27–36. [Google Scholar] [CrossRef] [Green Version]
- Gerasimova, E.A.; Plotnikov, A.O.; Khlopko, Y.A.; Zlatogursky, V.V. Multiple euryhaline lineages of centrohelids (Haptista: Centroplasthelida) in inland saline waters revealed with metabarcoding. J. Eukaryot. Microbiol. 2020, 67, 223–231. [Google Scholar] [CrossRef]
- Shatilovich, A.V.; Mylnikov, A.P.; Stoupin, D.V. The fauna and morphology of heterotrophic flagellates and heliozoans from Late Pleistocene fossil rodent burrows (Kolyma Lowland). Zool. Zhurn. 2010, 89, 387–397, (In Russian with Englich summary). [Google Scholar]
- Geisen, S.; Tveit, A.T.; Clark, I.M.; Richter, A.; Svenning, M.M.; Bonkowski, M.; Urich, T. Metatranscriptomic census of active protists in soils. ISME J. 2015, 9, 2178–2190. [Google Scholar] [CrossRef] [PubMed]
- Singer, D.; Seppey, C.V.W.; Lentendu, G.; Dunthorn, M.; Bass, D.; Belbahri, L.; Blandenier, Q.; Debroas, D.; de Groot, G.A.; de Vargas, C.; et al. Protist taxonomic and functional diversity in soil, freshwater and marine ecosystems. Environ. Int. 2021, 146, 106262. [Google Scholar] [CrossRef]
- Leonov, M.M. New species of centrohelid heliozoa of the genus Acanthocystis (Centroheliozoa). Zool. Zhurn. 2010, 89, 507–513, (in Russian with English summary). [Google Scholar]
- Leonov, M.M.; Mylnikov, A.P. Centroheliozoa from Southern Karelia. Zool. Zhurn. 2012, 91, 515–523, (In Russian with English summary). [Google Scholar]
- Tikhonenkov, D.V.; Mylnikov, A.P. Choanocystis antarctica sp. n., a new heliozoan (Centrohelida) species from the littoral zone of King George Island, South Shetland Islands, Antarctica. Biol. Bull. 2011, 38, 663–666. [Google Scholar] [CrossRef]
- Zlatogursky, V.V. Three new freshwater species of centrohelid heliozoans: Acanthocystis crescenta sp. nov., A. kirilli sp. nov., and Choanocystis minima sp. nov. Eur. J. Protistol. 2010, 46, 159–163. [Google Scholar] [CrossRef] [PubMed]
- Zlatogursky, V.V. Raphidiophrys heterophryoidea sp. nov. (Centrohelida: Raphidiophryidae), the first heliozoan species with a combination of siliceous and organic skeletal elements. Eur. J. Protistol. 2012, 48, 9–16. [Google Scholar] [CrossRef]
- Zlatogursky, V.V. Two new species of centrohelid heliozoans: Acanthocystis costata sp. nov. and Choanocystis symna sp. nov. Acta Protozool 2014, 53, 313–324. [Google Scholar]
- Zlatogursky, V.V.; Gerasimova, E.A.; Plotnikov, A.O. A new species of centrohelid heliozoan Acanthocystis amura n. sp. isolated from two remote locations in Russia. J. Eukaryot. Microbiol. 2017, 64, 434–439. [Google Scholar] [CrossRef] [PubMed]
- Zlatogursky, V.V.; Gerasimova, E.A.; Drachko, D.; Klimov, V.I.; Shɨshkin, Y.; Plotnikov, A.O. Pinjata ruminata gen. et sp. n.—A new member of centrohelid family Yogsothothidae (Haptista: Centroplasthelida) from the brackish river. J. Eukaryot. Microbiol. 2019, 66, 862–868. [Google Scholar] [CrossRef]
- Gerasimova, E.A.; Plotnikov, A.O. New freshwater species of centrohelids Acanthocystis lyra sp. nov. and Acanthocystis siemensmae sp. nov. (Haptista, Heliozoa, Centrohelea) from the South Urals, Russia. Acta Protozool. 2016, 55, 231–237. [Google Scholar]
- Prokina, K.I.; Zagumyonnyi, D.G.; Mylnikov, A.P. Marine Centrohelid heliozoans (Centroplasthelida Febvre-Chevalier et Febvre, 1984) from bays of Sevastopol (The Black Sea shore). Russ. J. Mar. Biol. 2019, 45, 377–384. [Google Scholar] [CrossRef]
- Prokina, K.I.; Radaykina, L.V.; Mylnikov, A.P. Centrohelid Heliozoans (Centroplasthelida Febvre-Chevalier et Febvre 1984) from Vietnam. Biol. Bull. 2020, 47, 29–40. [Google Scholar] [CrossRef]
- Zagumyonnyi, D.G.; Prokina, K.I.; Tikhonenkov, D.V. First findings of сentrohelid heliozoans (Haptista: Centroplasthelida) from marine and freshwater environments of South Korea. Protistology 2020, 14, 227–245. [Google Scholar] [CrossRef]
- Shishkin, Y.; Drachko, D.; Zlatogursky, V.V. Clypifer cribrifer gen. nov., sp. nov. (Clypiferidae fam. nov., Pterocystida, Centroplasthelida), with notes on evolution of centrohelid siliceous coverings. Int. J. Syst. Evol. Microbiol. 2021, 71. [Google Scholar] [CrossRef] [PubMed]
- Drachko, D.; Mikhailovskii, V.; Shishkin, Y.; Zlatogursky, V.V. Phylogenetic position and morphology of Raphidiophrys elongata sp. nov. (Haptista: Centroplasthelida) with notes on cyst wall structure and evolution. Eur. J. Protistol. 2021, 81, 125836. [Google Scholar] [CrossRef] [PubMed]
- Prokina, K.I.; Zagumyonnyi, D.G.; Tikhonenkov, D.V. Centrohelid heliozoans (Centroplasthelida Febvre-Chevalier et Febvre, 1984) from different types of freshwater bodies in the Middle Russian forest-steppe. Acta Protozool. 2018, 57, 243–266. [Google Scholar] [CrossRef]
- Vørs, N. Heterotrophic amoebae, flagellates and Heliozoa from the Tvärminne area, Gulf of Finland, in 1988–1990. Ophelia 1992, 36, 1–109. [Google Scholar] [CrossRef]
- Schneider, C.A.; Rasband, W.S.; Eliceiri, K.W. NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 2012, 9, 671–675. [Google Scholar] [CrossRef]
- Gile, G.H.; James, E.R.; Scheffrahn, R.H.; Carpenter, K.J.; Harper, J.T.; Keeling, P.J. Molecular and morphological analysis of the family Calonymphidae with a description of Calonympha chia sp. nov., Snyderella kirbyi sp. nov., Snyderella swezyae sp. nov. and Snyderella yamini sp. nov. Int. J. Syst. Evol. Microbiol. 2011, 61, 2547–2558. [Google Scholar] [CrossRef] [PubMed]
- Katoh, K.; Kuma, K.; Toh, H.; Miyata, T. MAFFT version 5: Improvement in accuracy of multiple sequence alignment. Nucleic Acids Res. 2005, 33, 511–518. [Google Scholar] [CrossRef] [PubMed]
- Katoh, K.; Standley, D.M. MAFFT multiple sequence alignment software version 7: Improvements in performance and usability. Mol. Biol. Evol. 2013, 30, 772–780. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Capella-Gutierrez, S.; Silla-Martinez, J.M.; Gabaldon, T. TrimAl: A tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 2009, 25, 1972–1973. [Google Scholar] [CrossRef]
- Ronquist, F.; Huelsenbeck, J.P. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 2003, 19, 1572–1574. [Google Scholar] [CrossRef] [Green Version]
- Nguyen, L.T.; Schmidt, H.A.; Haeseler, A.; Minh, B.Q. IQ-TREE: A fast and effective stochastic algorithm for estimating maximum likelihood phylogenies. Mol. Biol. Evol. 2015, 32, 268–274. [Google Scholar] [CrossRef] [PubMed]
- Dürrschmidt, M. An electron microscopical study of freshwater Heliozoa (genus Acanthocystis, Centrohelidia) from Chile, New Zealand, Malaysia and Sri Lanka. II. Arch. Protistenkunde. 1987, 133, 21–48. [Google Scholar] [CrossRef]
- Wujek, D.E. Freshwater heliozoa from Florida. Fla. Sci. 2006, 69, 177–191. [Google Scholar]
- Simon, M.; López-García, P.; Deschamps, P.; Moreira, D.; Restoux, G.; Bertolino, P.; Jardillier, L. Marked seasonality and high spatial variability of protist communities in shallow freshwater systems. ISME J. 2015, 9, 1941–1953. [Google Scholar] [CrossRef] [Green Version]
- Simon, M.; Jardillier, L.; Deschamps, P.; Moreira, D.; Restoux, G.; Bertolino, P.; López-García, P. Complex communities of small protists and unexpected occurrence of typical marine lineages in shallow freshwater systems. Environ. Microbiol. 2015, 17, 3610–3627. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Geisen, S.; Mitchell, E.A.D.; Adl, S.; Bonkowski, M.; Dunthorn, M.; Ekelund, F.; Fernández, L.D.; Jousset, A.; Krashevska, V.; Singer, D.; et al. Soil protists: A fertile frontier in soil biology research. FEMS Microbiol. Rev. 2018, 42, 293–323. [Google Scholar] [CrossRef]
- Oliverio, A.M.; Geisen, S.; Delgado-Baquerizo, M.; Maestre, F.T.; Turner, B.L.; Fierer, N. The global-scale distributions of soil protists and their contributions to belowground systems. Sci. Adv. 2020, 6, eaax8787. [Google Scholar] [CrossRef] [Green Version]
- Shatilovich, A.V.; Shmakova, L.A.; Mylnikov, A.P.; Gilichinsky, D.A. Ancient Protozoa isolated from permafrost. In Permafrost Soils; Margesin, R., Ed.; Springer: Berlin/Heidelberg, Germany, 2009; pp. 97–115. [Google Scholar]
- Stoupin, D.; Kiss, A.K.; Arndt, H.; Shatilovich, A.V.; Gilichinsky, D.A.; Nitsche, F. Cryptic diversity within the choanoflagellate morphospecies complex Codosiga botrytis—phylogeny and morphology of ancient and modern isolates. Eur. J. Protistol. 2012, 48, 263–273. [Google Scholar] [CrossRef]
- Shmakova, L.A.; Rivkina, E.M. Viable eukaryotes of the phylum Amoebozoa from the Arctic permafrost. Paleontol. J. 2015, 49, 572–577. [Google Scholar] [CrossRef]
- Shatilovich, A.; Stoupin, D.; Rivkina, E. Ciliates from ancient permafrost: Assessment of cold resistance of the resting cysts. Eur. J. Protistol. 2015, 51, 230–240. [Google Scholar] [CrossRef] [PubMed]
- Shmakova, L.; Bondarenko, N.; Smirnov, A. Viable species of Flamella (Amoebozoa: Variosea) isolated from ancient arctic permafrost sediments. Protist 2016, 167, 13–30. [Google Scholar] [CrossRef]
- Malavin, S.; Shmakova, L.; Claverie, J.-M.; Rivkina, E. Frozen Zoo: A collection of permafrost samples containing viable protists and their viruses. Biodivers. Data J. 2020, 8, e51586. [Google Scholar] [CrossRef]
- Fyodorov-Davydov, D.G.; Kholodov, A.L.; Ostroumov, V.E.; Kraev, G.N.; Sorokovikov, V.A.; Davydov, S.P.; Merekalova, A.A. Seasonal thaw of soils in the North Yakutian ecosystems. In Proceedings of the 9th International Conference on Permafrost, Fairbanks, AK, USA, 29 June–3 July 2008; Kane, D.L., Hinkel, K.M., Eds.; Institute of Northern Engineering, University of Alaska: Fairbanks, AK, USA, 2008; pp. 481–486. [Google Scholar] [CrossRef]
- Biskaborn, B.K.; Smith, S.L.; Noetzli, J.; Matthes, H.; Vieira, G.; Streletskiy, D.A.; Schoeneich, P.; Romanovsky, V.E.; Lewkowicz, A.G.; Abramov, A.; et al. Permafrost is warming at a global scale. Nat. Commun. 2019, 10, 264. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Inglese, C.N.; Christiansen, C.T.; Lamhonwah, D.; Moniz, K.; Montross, S.N.; Lamoureux, S.; Lafrenière, M.; Grogan, P.; Walker, V.K. Examination of soil microbial communities after permafrost thaw subsequent to an active layer detachment in the high Arctic. Arct. Antarct. Alp. Res. 2017, 49, 455–472. [Google Scholar] [CrossRef] [Green Version]
- Wu, M.-H.; Chen, S.-Y.; Chen, J.-W.; Xue, K.; Chen, S.-L.; Wang, X.-M.; Chen, T.; Kang, S.C.; Rui, J.P.; Thies, J.E.; et al. Reduced microbial stability in the active layer is associated with carbon loss under alpine permafrost degradation. PNAS 2021, 118, e2025321118. [Google Scholar] [CrossRef] [PubMed]
No | Sampling Site | Date | Biotope | Coordinates |
---|---|---|---|---|
1 | Syuryu-Kaya Mt, Crimean Peninsula | 14 August 2016 | Soil of dry stream | 44°56′07.8″ N 35°12′38.7″ E |
2 | Pesiv Island, Dnieper Lowland, East European Plain | 11 October 2014 | Soil and willow leaf litter | 50°30′14.68″ N 30°31′57.16″ E |
3 | Champ Island (Franz Josef Land archipelago, Arctic Ocean | 6 August 2019 | Moss with sand in the glacier melting zone (70 m from water edge), polar desert | 80°37′46.8″ N 56°53′45.5″ E |
4 | Cape Maliy Chukochiy vicinity, Kolyma Lowland (North-Eastern Siberia) | August 2016 | Buried peat, cryoturbated soil from 40 cm depth and mineral soil from 65 depth | 70°03′53.9″ N 159°44′06.6″ E |
Parameter | Kolyma Lowland Strain | Franz Josef Land Strain | Dnieper Lowland Strain | Crimean Strain |
---|---|---|---|---|
Cell diameter, μm | 4.3–16.3 (LM) (75) | 5.0–6.9 (TEM) (7) | ~ 6–7 (SEM) (11) | ~ 7 (SEM) (2) |
Spine scale length, μm | 1.06–3.33 (61) | 2.74–4.55 (37) | 2.12–4.70 (35) | 2.81–4.17 (20) |
Basal plate width, μm | 0.60–0.92 (52) | 0.65–1.17 (26) | 0.70–0.90 (29) | 0.66–0.91 (19) |
Marginal rim of basal plate, μm | 0.05–0.07 (31) | 0.04-0.05 (7) | 0.06–0.09 (25) | 0.07-0.09 (5) |
Shaft diameter, μm | 0.08–0.12 (50) | 0.05–0.09 (28) | 0.10–0.11 (30) | 0.10–0.12 (20) |
Pocket height, μm | 0.15–0.36 (21) | 0.15–0.29 (5) | 0.18-0.35 (19) | 0.14–0.25 (8) |
Pocket width, μm | 0.06–0.13 (26) | 0.09–0.12 (6) | 0.07-0.15 (18) | 0.06–0.10 (8) |
Pocket depth, μm | 0.13–0.36 (15) | 0.26 (1) | 0.17 (1) | – |
Plate scales length, μm | 1.25–2.05 (48) | 1.76–1.86 (5) | 1.22–1.62 (22) | 1.63–2.05 (15) |
Plate scales width, μm | 0.86–1.93 (48) | 1.07–1.27 (6) | 0.69–0.97 (19) | 1.10–1.40 (15) |
Length of medial thickening of plate scales, μm | 0.47–0.77 (22) | 0.82-0.85 (6) | 0.72–0.86 (15) | 0.59–1.05 (15) |
Width of medial thickening of plate scales, μm | 0.065–0.116 (18) | 0.060–0.064 (6) | 0.072–0.085 (12) | 0.07-0.15 (15) |
Cysts diameter, μm | 5.9–7.3 (LM) (20) | – | – | – |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Zagumyonnyi, D.G.; Radaykina, L.V.; Tikhonenkov, D.V. Triangulopteris lacunata gen. et sp. nov. (Centroplasthelida), a New Centrohelid Heliozoan from Soil. Diversity 2021, 13, 658. https://doi.org/10.3390/d13120658
Zagumyonnyi DG, Radaykina LV, Tikhonenkov DV. Triangulopteris lacunata gen. et sp. nov. (Centroplasthelida), a New Centrohelid Heliozoan from Soil. Diversity. 2021; 13(12):658. https://doi.org/10.3390/d13120658
Chicago/Turabian StyleZagumyonnyi, Dmitry G., Liudmila V. Radaykina, and Denis V. Tikhonenkov. 2021. "Triangulopteris lacunata gen. et sp. nov. (Centroplasthelida), a New Centrohelid Heliozoan from Soil" Diversity 13, no. 12: 658. https://doi.org/10.3390/d13120658
APA StyleZagumyonnyi, D. G., Radaykina, L. V., & Tikhonenkov, D. V. (2021). Triangulopteris lacunata gen. et sp. nov. (Centroplasthelida), a New Centrohelid Heliozoan from Soil. Diversity, 13(12), 658. https://doi.org/10.3390/d13120658