Genus Proteomonas is not monotypic: P. agilis sp. nov. (Cryptophyceae, Geminigeraceae) from the Black Sea and hidden diversity of Proteomonas species

Antonina N. Khanaychenko; Olga V. Nikolaeva; Olga A. Rylkova; Maria Saburova; Vladimir V. Aleoshin

doi:10.1515/bot-2024-0039

Article

Genus Proteomonas is not monotypic: P. agilis sp. nov. (Cryptophyceae, Geminigeraceae) from the Black Sea and hidden diversity of Proteomonas species

Antonina N. Khanaychenko

Antonina N. Khanaychenko (PhD) is a leading researcher at the Institute of Biology of the Southern Seas. Her research has focused on the culture of various marine microalgae, rotifers, and copepods, as well as their interactions with fish larvae. Over the past 5 years, she has established a novel culture collection of cryptomonad strains isolated from the Black Sea. She is currently engaged in research on various aspects of their taxonomy and ecology.
, Olga V. Nikolaeva , Olga A. Rylkova

Olga A. Rylkova (PhD) is a senior researcher at the Institute of Biology of the Southern Seas. She has extensive experience working with a variety of microalgae and microflora associated with algal cultures. Over the past 5 years, she has focused her research on the morphological and physiological parameters of microalgae and bacteria, employing techniques such as flow cytometry, confocal laser microscopy, and scanning electron microscopy.
, Maria Saburova

Maria Saburova (PhD) is a marine biologist with over 30 years of experience in the taxonomy and ecology of planktonic and benthic microalgae from a wide geographic range. Since 2005, she has been engaged in research on marine microalgae of the Persian Gulf as a long-term scientific consultant at the Kuwait Institute for Scientific Research. Her research interests are focused on microalgal biodiversity, taxonomy, and ecology, with a particular emphasis on harmful bloom species and their impact on coastal ecosystems.
and Vladimir V. Aleoshin

Published/Copyright: November 4, 2024

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From the journal Botanica Marina Volume 67 Issue 6

Abstract

The cryptophytes of the Black Sea are a poorly studied group that has yet to be fully resolved using comprehensive taxonomic approaches, including electron microscopy and molecular genetics. This study describes Proteomonas agilis sp. nov. belonging to a marine cryptophyte genus formerly thought to be monotypic. The morphological characters of the new species align with those currently used to delineate the genus Proteomonas, and are similar to those of the haplomorph P. sulcata, the type species, with minor morphological and molecular modifications. Phylogenetic relationships inferred from nuclear-encoded SSU, LSU, and ITS2 rDNA datasets confirmed that the new species belongs to the monophyletic genus Proteomonas, which is divided into two unequal branches. The largest and relatively long branch contains 18 strains, including P. agilis sp. nov. Comparison of ITS2 rRNA secondary structures using the compensatory base changes approach confirmed the distinction of P. agilis sp. nov. from the other Proteomonas strains. Our findings revealed that the cryptophyte genus Proteomonas is not monotypic but includes a range of unstudied species besides the type species P. sulcata and P. agilis sp. nov. described in this study. Therefore, an integrated approach is required for a careful revision of the genus.

Keywords: Cryptophyceae; Proteomonas ; Black Sea; morphology; phylogeny

Corresponding author: Maria Saburova, Environment and Life Sciences Research Center, Kuwait Institute for Scientific Research, P.O. BOX 1638, Salmiya 22017, Kuwait, E-mail: msaburova@gmail.com

About the authors

Antonina N. Khanaychenko

Antonina N. Khanaychenko (PhD) is a leading researcher at the Institute of Biology of the Southern Seas. Her research has focused on the culture of various marine microalgae, rotifers, and copepods, as well as their interactions with fish larvae. Over the past 5 years, she has established a novel culture collection of cryptomonad strains isolated from the Black Sea. She is currently engaged in research on various aspects of their taxonomy and ecology.

Olga A. Rylkova

Olga A. Rylkova (PhD) is a senior researcher at the Institute of Biology of the Southern Seas. She has extensive experience working with a variety of microalgae and microflora associated with algal cultures. Over the past 5 years, she has focused her research on the morphological and physiological parameters of microalgae and bacteria, employing techniques such as flow cytometry, confocal laser microscopy, and scanning electron microscopy.

Maria Saburova

Maria Saburova (PhD) is a marine biologist with over 30 years of experience in the taxonomy and ecology of planktonic and benthic microalgae from a wide geographic range. Since 2005, she has been engaged in research on marine microalgae of the Persian Gulf as a long-term scientific consultant at the Kuwait Institute for Scientific Research. Her research interests are focused on microalgal biodiversity, taxonomy, and ecology, with a particular emphasis on harmful bloom species and their impact on coastal ecosystems.

Acknowledgments

We are grateful to our colleagues, IBSS researchers T.V. Efimova, N.A. Moiseeva, and E.Y. Skorokhod for giving us a permission to present here part of our joint data on spectrophotometry of the cryptophyte strain IBSS-Cr-4.14M. We thank Dmitry V. Moiseenko for technical assistance in microalgae cultivation and Vyacheslav N. Lishaev (IBSS) for technical assistance with SEM. We would like to express our gratitude to the Editor in Chief, Prof. Matthew J. Dring, and the two anonymous reviewers for their valuable and constructive comments and suggestions, which have helped us to improve the quality of the manuscript.

Research ethics: All research procedures were conducted in accordance with local laws. All data were obtained and collected in accordance with local research protocols.
Informed consent: Not applicable.
Author contributions: A. N. Khanaychenko: original concept, methodology, culture establishment and maintenance, light microscopy, drafting and editing manuscript; O. V. Nikolaeva: DNA extraction and sequencing, molecular analyses, drafting and editing manuscript; O. A. Rylkova: electron microscopy; M. Saburova: visualization, review and editing manuscript; V. V. Aleoshin: methodology, analysis of molecular data, review and editing manuscript. All authors discussed the results and contributed to the final manuscript. The authors have accepted responsibility for the entire content of this manuscript and approved its submission.
Use of Large Language Models, AI and Machine Learning Tools: None declared.
Conflict of interest: The authors state no conflict of interest.
Research funding: This work was financially supported by the Research Program of the Russian Academy of Sciences grant agreement # 124022400152-1 and # 124021300070-2 at the IBSS RAS (AK, OR) and # АААА-А17-117120540067-0 (ON, VA).
Data availability: Partial nuclear encoded 18S (SSU) and 28S (LSU) rDNA and complete internal transcribed spacer (ITS) regions were deposited in the GenBank with accession number OR687719.

References

Adolf, J.E., Yeager, C.L., Miller, W.D., Mallonee, M.E., and Harding, Jr., L.W. (2006). Environmental forcing of phytoplankton floral composition, biomass, and primary productivity in Chesapeake Bay, USA. Estuar. Coast Shelf Sci. 67: 108–122, https://doi.org/10.1016/j.ecss.2005.11.030.Search in Google Scholar

Aganesova, L.O. (2021). The reproduction and development of brackish-water copepods that were fed microalgae of different species. Russ. J. Mar. Biol. 47: 114–120, https://doi.org/10.1134/s1063074021020024.Search in Google Scholar

Altenburger, A., Blossom, H.E., Garcia-Cuetos, L., Jakobsen, H.H., Carstensen, J., Lundholm, N., Hansen, P.J., Moestrup, Ø., and Haraguchi, L. (2020). Dimorphism in cryptophytes – the case of Teleaulax amphioxeia/Plagioselmis prolonga and its ecological implications. Sci. Adv. 6: 1–9, https://doi.org/10.1126/sciadv.abb1611.Search in Google Scholar PubMed PubMed Central

Andersen, R.A. (2005). Algae culturing technique. Elsevier Academic Press, New York.Search in Google Scholar

Bankevich, A., Nurk, S., Antipov, D., Gurevich, A.A., Dvorkin, M., Kulikov, A.S., Lesin, V.M., Nikolenko, S.I., Pham, S., Prjibelski, A.D., et al.. (2012). SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J. Comput. Biol. 19: 455–477, https://doi.org/10.1089/cmb.2012.0021.Search in Google Scholar PubMed PubMed Central

Barkhatov, Y.V., Khromechek, E.B., Zykov, V.V., and Rogozin, D.Y. (2022). Cryptophytes of Lake Shira (Khakassia, Russia): explosive growth during breakdown of meromixis. Hydrobiologia 849: 3373–3387, https://doi.org/10.1007/s10750-022-04939-0.Search in Google Scholar

Bermúdez, J., Rosales, N., Loreto, C., Briceño, B., and Morales, E. (2004). Exopolysaccharide, pigment and protein production by the marine microalga Chroomonas sp. in semicontinuous cultures. World J. Microbiol. Biotechnol. 20: 179–183, https://doi.org/10.1023/b:wibi.0000021754.59894.4a.10.1023/B:WIBI.0000021754.59894.4aSearch in Google Scholar

Bistricki, T. and Munawar, M. (1978). A rapid preparation method for scanning electron microscopy of Lugol preserved algae. J. Microsc. 114: 215–218, https://doi.org/10.1111/j.1365-2818.1978.tb00131.x.Search in Google Scholar

Bolger, A.M., Lohse, M., and Usadel, B. (2014). Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30: 2114–2120, https://doi.org/10.1093/bioinformatics/btu170.Search in Google Scholar PubMed PubMed Central

Butcher, R.W. (1967). An introductory account of the smaller algae of British coastal waters. Part IV: Cryptophyceae. Fishery Investigations. Ministry of Agriculture, Fisheries & Food, Ser. IV, London, pp. 1–54.Search in Google Scholar

Cerino, F. and Zingone, A. (2006). A survey of cryptomonad diversity and seasonality at a coastal Mediterranean site. Eur. J. Phycol. 41: 363–378, https://doi.org/10.1080/09670260600839450.Search in Google Scholar

Clay, B.L., Kugrens, P., and Lee, R.E. (1999). A revised classification of Cryptophyta. Bot. J. Linn. Soc. 131: 131–151.10.1111/j.1095-8339.1999.tb01845.xSearch in Google Scholar

Cloern, J.E. and Dufford, R. (2005). Phytoplankton community ecology: principles applied in San Francisco Bay. Mar. Ecol. Prog. Ser. 285: 11–28, https://doi.org/10.3354/meps285011.Search in Google Scholar

Coleman, A.W. (2000). The significance of a coincidence between evolutionary landmarks found in mating affinity and a DNA sequence. Protist 151: 1–9, https://doi.org/10.1078/1434-4610-00002.Search in Google Scholar PubMed

Coleman, A.W. (2007). Pan-eukaryote ITS2 homologies revealed by RNA secondary structure. Nucleic Acids Res. 35: 3322–3329, https://doi.org/10.1093/nar/gkm233.Search in Google Scholar PubMed PubMed Central

Coutinho, P., Ferreira, M., Freire, I., and Otero, A. (2020). Enriching rotifers with “premium” microalgae: Rhodomonas lens. Mar. Biotechnol. 22: 118–129, https://doi.org/10.1007/s10126-019-09936-4.Search in Google Scholar PubMed

Daugbjerg, N., Norlin, A., and Lovejoy, C. (2018). Baffinella frigidus gen. et sp. nov. (Baffinellaceae fam. nov., Cryptophyceae) from Baffin Bay: Morphology, pigment profile, phylogeny, and growth rate response to three abiotic factors. J. Phycol. 54: 665–680, https://doi.org/10.1111/jpy.12766.Search in Google Scholar PubMed

Deane, J.A., Strachan, I.M., Saunders, G.W., Hill, D.R., and McFadden, G.I. (2002). Cryptomonad evolution: nuclear 18S rDNA phylogeny versus cell morphology and pigmentation. J. Phycol. 38: 1236–1244, https://doi.org/10.1046/j.1529-8817.2002.01250.x.Search in Google Scholar

Dolgin, A. and Adolf, J. (2019). Scanning electron microscopy of phytoplankton: achieving high quality images through the use of safer alternative chemical fixatives. J. Young Investig. 37: 1–9.10.22186/jyi.37.1.1-9Search in Google Scholar

Dunstan, G.A., Brown, M.R., and Volkman, J.K. (2005). Cryptophyceae and rhodophyceae; chemotaxonomy, phylogeny, and application. Phytochemistry 66: 2557–2570, https://doi.org/10.1016/j.phytochem.2005.08.015.Search in Google Scholar PubMed

Efimova, T., Churilova, T., and Mukhanov, V. (2020). The influence of light of different spectral qualities on the photosynthetic characteristics of C-phycocyanine-containing cyanobacteria Synechococcus sp. WH5701. Russ. J. Mar. Biol. 46: 105–112, https://doi.org/10.1134/s1063074020020042.Search in Google Scholar

Gervais, F. (1998). Ecology of cryptophytes coexisting near a freshwater chemocline. Freshw. Biol. 39: 61–78, https://doi.org/10.1046/j.1365-2427.1998.00260.x.Search in Google Scholar

Greenwold, M.J., Cunningham, B.R., Lachenmyer, E.M., Pullman, J.M., Richardson, T.L., and Dudycha, J.L. (2019). Diversification of light capture ability was accompanied by the evolution of phycobiliproteins in cryptophyte algae. Proc. Biol. Sci. 286: 20190655, https://doi.org/10.1098/rspb.2019.0655.Search in Google Scholar PubMed PubMed Central

Greenwold, M.J., Merritt, K., Richardson, T.L., and Dudycha, J.L. (2023). A three-genome ultraconserved element phylogeny of Cryptophytes. Protist 174: 125994, https://doi.org/10.1016/j.protis.2023.125994.Search in Google Scholar PubMed

Gusev, E., Podunay, Y., Martynenko, N., Shkurina, N., and Kulikovskiy, M. (2020). Taxonomic studies of Cryptomonas lundii clade (Cryptophyta: Cryptophyceae) with description of a new species from Vietnam. Fottea 20: 137–143, https://doi.org/10.5507/fot.2020.004.Search in Google Scholar

Hammer, A., Schumann, R., and Schubert, H. (2002). Light and temperature acclimation of Rhodomonas salina (Cryptophyceae): photosynthetic performance. Aquat. Microb. Ecol. 29: 287–296, https://doi.org/10.3354/ame029287.Search in Google Scholar

Han, M.S. and Furuya, K. (2000). Size and species-specific primary productivity and community structure of phytoplankton in Tokyo Bay. J. Plank. Res. 22: 1221–1235.10.1093/plankt/22.7.1221Search in Google Scholar

He, X. and Peng, X. (2012). Spatial variability of summer and autumn phytoplankton community structure in Xiamen Western Bay based on pigment analysis. Acta Oceanol. Sin. 31: 165–175, https://doi.org/10.1007/s13131-012-0246-4.Search in Google Scholar

Hill, D.R.A. and Wetherbee, R. (1986). Proteomonas sulcata gen. et sp. nov. (Cryptophyceae), a cryptomonad with two morphologically distinct and alternating forms. Phycologia 25: 521–543, https://doi.org/10.2216/i0031-8884-25-4-521.1.Search in Google Scholar

Hoef-Emden, K. (2018). Revision of the genus Chroomonas Hansgirg: the benefits of DNA-containing specimens. Protist 169: 662–681, https://doi.org/10.1016/j.protis.2018.04.005.Search in Google Scholar PubMed

Hoef-Emden, K. and Archibald, J.M. (2017) Cryptophyta (cryptomonads). In: Archibald, J.M., Simpson, A.G.B., and Slamovits, C.H. (Eds.). Handbook of the protists. Springer International Publishing, Cham, Switzerland, pp. 851–891.10.1007/978-3-319-28149-0_35Search in Google Scholar

Hoef-Emden, K. and Melkonian, M. (2003). Revision of the genus Cryptomonas (Cryptophyceae): a combination of molecular phylogeny and morphology provides insights into a long-hidden dimorphism. Protist 154: 371–409, https://doi.org/10.1078/143446103322454130.Search in Google Scholar PubMed

Hoef-Emden, K., Marin, B., and Melkonian, M. (2002). Nuclear and nucleomorph SSU rDNA phylogeny in the cryptophyta and the evolution of cryptophyte diversity. J. Mol. Evol. 55: 161–179, https://doi.org/10.1007/s00239-002-2313-5.Search in Google Scholar PubMed

Hu, H.-J., Li, Y.-G., Wu, L.-P., and Qi, Y.-Z. (2002). Studies on genus Cryptomonas from China Sea. Acta Oceanol. Sin. 21: 535–540.Search in Google Scholar

Huang, B., Liu, Y., Xiang, W., Tian, H., Liu, H., Cao, Z., and Hong, H. (2008). Grazing impact of microzooplankton on phytoplankton in the Xiamen Bay using pigment-specific dilution technique. Acta Oceanol. Sin. 27: 147–162.Search in Google Scholar

Johnson, M.D., Beaudoin, D.J., Laza-Martínez, A., Dyhrman, S.T., Fensin, E., Lin, S., Merculief, A., Nagai, S., Pompeu, M., Setälä, O., et al.. (2016). The genetic diversity of Mesodinium and associated cryptophytes. Front. Microbiol. 7: 2017, https://doi.org/10.3389/fmicb.2016.02017.Search in Google Scholar PubMed PubMed Central

Khanaychenko, A., Mukhanov, V., Aganesova, L., Besiktepe, S., and Gavrilova, N. (2018). Grazing and feeding selectivity of Oithona davisae in the Black Sea: importance of cryptophytes. Turk. J. Fish. Aquat. Sci. 18: 937–949, https://doi.org/10.4194/1303-2712-v18_8_02.Search in Google Scholar

Khanaychenko, A.N., Rylkova, O.A., Aganesova, L.O., Popova, O.V., Aleoshin, V.V., and Saburova, M. (2022). Rhodomonas storeatuloformis sp. nov.(Cryptophyceae, Pyrenomonadaceae), a new cryptomonad from the Black Sea: morphology versus molecular phylogeny. Fottea 22: 122–136, https://doi.org/10.5507/fot.2021.019.Search in Google Scholar

Kim, H.S., Kim, J.H., Jo, S.G., Rho, J.R., and Yih, W. (2020). Amino acids and fatty acids composition in mass-cultured Teleaulax amphioxeia strains with notable potential for rotifer (Brachionus plicatilis) enrichment. J. World Aquacult. Soc. 51: 712–728, https://doi.org/10.1111/jwas.12698.Search in Google Scholar

Kjer, K.M., Blahnik, R.J., and Holzenthal, R.W. (2001). Phylogeny of Trichoptera (Caddisflies): characterization of signal and noise within multiple datasets. Syst. Biol. 50: 781–816, https://doi.org/10.1080/106351501753462812.Search in Google Scholar PubMed

Klaveness, D. (1989). Biology and ecology of the Cryptophyceae: status and challenges. Biol. Oceanogr. 6: 257–270.Search in Google Scholar

Krasnova, E.D., Pantyulin, A.N., Matorin, D.N., Todorenko, D.A., Belevich, T.A., Milyutina, I.A., and Voronov, D.A. (2014). Cryptomonad alga Rhodomonas sp. (Cryptophyta, Pyrenomonadaceae) bloom in the redox zone of the basins separating from the White Sea. Microbiology 83: 270–277, https://doi.org/10.1134/s0026261714030102.Search in Google Scholar

Latsos, C., van Houcke, J., Blommaert, L., Verbeeke, G.P., Kromkamp, J., and Timmermans, K.R. (2021). Effect of light quality and quantity on productivity and phycoerythrin concentration in the cryptophyte Rhodomonas sp. J. Appl. Phycol. 33: 729–741, https://doi.org/10.1007/s10811-020-02338-3.Search in Google Scholar

Laza-Martínez, A. (2012). Urgorri complanatus gen. et sp. nov. (Cryptophyceae), a red-tide-forming species in brackish waters. J. Phycol. 48: 423–435, https://doi.org/10.1111/j.1529-8817.2012.01130.x.Search in Google Scholar PubMed

Laza-Martínez, A., Arluzea, J., Miguel, I., and Orive, E. (2012). Morphological and molecular characterization of Teleaulax gracilis sp. nov. and T. minuta sp. nov. (Cryptophyceae). Phycologia 51: 649–661, https://doi.org/10.2216/11-044.1.Search in Google Scholar

Łukaszek, M. and Hoef-Emden, K. (2017). The use of integrative taxonomy for identification of cryptophytes – first records for Poland. Phycologia 56: 122–123.Search in Google Scholar

Magalhães, K., Santos, A.L., Vaulot, D., and Oliveira, M.C. (2021). Hemiselmis aquamarina sp.nov. (Cryptomonadales, Cryptophyceae), a cryptophyte with a novel phycobiliprotein type (Cr-PC 564). Protist 172: 125832, https://doi.org/10.1016/j.protis.2021.125832.Search in Google Scholar PubMed

Majaneva, M., Remonen, I., Rintala, J.M., Belevich, I., Kremp, A., Setälä, O., Jokitalo, E., and Blomster, J. (2014). Rhinomonas nottbecki n. sp. (Cryptomonadales) and molecular phylogeny of the family Pyrenomonadaceae. J. Eukaryot. Microbiol. 61: 480–492, https://doi.org/10.1111/jeu.12128.Search in Google Scholar PubMed

Marin, B., Klingberg, M., and Melkonian, M. (1998). Phylogenetic relationships among the Cryptophyta: analyses of nuclear-encoded SSU rRNA sequences support the monophyly of extant plastid-containing lineages. Protist 149: 265–276, https://doi.org/10.1016/s1434-4610(98)70033-1.Search in Google Scholar PubMed

Martynenko, N., Kezlya, E., and Gusev, E. (2022). Description of a new species of the genus Cryptomonas (Cryptophyceae: Cryptomonadales), isolated from soils in a tropical forest. Diversity 14: 1001, https://doi.org/10.3390/d14111001.Search in Google Scholar

Medina, M., Collins, A.G., Silberman, J.D., and Sogin, M.L. (2001). Evaluating hypotheses of basal animal phylogeny using complete sequences of large and small subunit rRNA. Proc. Natl. Acad. Sci. U. S. A. 98: 9707–9712, https://doi.org/10.1073/pnas.171316998.Search in Google Scholar PubMed PubMed Central

Medlin, L., Elwood, H.J., Stickel, S., and Sogin, M.L. (1988). The characterization of enzymatically amplified eukaryotic 16S-like rRNA-coding regions. Gene 71: 491–499, https://doi.org/10.1016/0378-1119(88)90066-2.Search in Google Scholar PubMed

Medlin, L.K., Piwosz, K., and Metfies, K. (2017). Uncovering hidden biodiversity in the Cryptophyta: clone library studies at the Helgoland time series site in the Southern German Bight indentifies the cryptophycean clade potentially responsible for the majority of its genetic diversity during the spring bloom. Vie Milieu/Life Environ. 67: 27–32.Search in Google Scholar

Mikaelyan, A.S., Mosharov, S.A., Kubryakov, A.A., Pautova, L.A., Fedorov, A., and Chasovnikov, V.K. (2020). The impact of physical processes on taxonomic composition, distribution and growth of phytoplankton in the open Black Sea. J. Mar. Syst. 208: 103368, https://doi.org/10.1016/j.jmarsys.2020.103368.Search in Google Scholar

Mikaelyan, A.S., Pautova, L.A., and Fedorov, A.V. (2021). Seasonal evolution of deep phytoplankton assemblages in the Black Sea. J. Sea Res. 178: 102125, https://doi.org/10.1016/j.seares.2021.102125.Search in Google Scholar

Mitchell, B.G. and Kiefer, D.A. (1988). Chlorophyll a specific absorption and fluorescence excitation spectra for light-limited phytoplankton. Deep-Sea Res. A: Oceanogr. Res. Pap. 35: 639–663.10.1016/0198-0149(88)90024-6Search in Google Scholar

Moncheva, S., Boicenco, L., Mikaelyan, A.S., Zotov, A., Dereziuk, N., Gvarishvili, C., Slabakova, N., Mavrodieva, R., Vlas, O., Pautova, L.A., et al.. (2019) Phytoplankton. In: Black Sea state of environment report 2009-2014/5. Commission on the Protection of the Black Sea against Pollution, Istanbul, pp. 225–284.Search in Google Scholar

Moorhouse, H., Read, D., Mcgowan, S., Wagner, M., Roberts, C., Armstrong, L., Nicholls, D., Wickham, H., Hutchins, M., and Bowes, M. (2018). Characterisation of a major phytoplankton bloom in the River Thames (UK) using flow cytometry and high performance liquid chromatography. Sci. Total Environ. 624: 366–376, https://doi.org/10.1016/j.scitotenv.2017.12.128.Search in Google Scholar PubMed

Müller, T., Philippi, N., Dandekar, T., Schultz, J., and Wolf, M. (2007). Distinguishing species. RNA 13: 1469–1472, https://doi.org/10.1261/rna.617107.Search in Google Scholar PubMed PubMed Central

Nguyen, L.T., Schmidt, H.A., Von Haeseler, A., and Minh, B.Q. (2015). IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol. Biol. Evol. 32: 268–274, https://doi.org/10.1093/molbev/msu300.Search in Google Scholar PubMed PubMed Central

Novarino, G. (1991). Observations on some new and interesting Cryptophyceae. Nord. J. Bot. 11: 599–611, https://doi.org/10.1111/j.1756-1051.1991.tb01269.x.Search in Google Scholar

Oostlander, P.C., van Houcke, J., Wijffels, R.H., and Barbosa, M.J. (2020). Optimization of Rhodomonas sp. under continuous cultivation for industrial applications in aquaculture. Algal Res. 47: 101889, https://doi.org/10.1016/j.algal.2020.101889.Search in Google Scholar

Peltomaa, E., Johnson, M.D., and Taipale, S.J. (2018). Marine cryptophytes are great sources of EPA and DHA. Mar. Drugs 16: 1–11, https://doi.org/10.3390/md16010003.Search in Google Scholar PubMed PubMed Central

Polikarpov, I., Saburova, M., and Al-Yamani, F. (2020). Decadal changes in diversity and occurrence of microalgal blooms in the NW Arabian/Persian Gulf. Deep Sea Res. II: Top. Stud. Oceanogr. 179: 104810, https://doi.org/10.1016/j.dsr2.2020.104810.Search in Google Scholar

Rammel, T., Nagarkar, M., and Palenik, B. (2024). Temporal and spatial diversity and abundance of cryptophytes in San Diego coastal waters. J. Phycol. 60: 668–684, https://doi.org/10.1111/jpy.13451.Search in Google Scholar PubMed

Rouchijajnen, M.I. (1967). Species nova generis Cryptomonas (Pyrrophyta) e mari Nigro (Ponto Euxino). Novitates Systematicae Plantarum non Vascularium (Novosti Sistematiki Nizshikh Rastenii) 4: 71–73, (in Russian, with Latin diagnosis).Search in Google Scholar

Rouchijajnen, M.I. (1970). Species novae generum Cryptomonas (Pyrrophyta) et Platymonas (Chlorophyta, Chlamydomonadales) e mari Nigro. Novitates Systematicae Plantarum non Vascularium (Novosti Sistematiki Nizshikh Rastenii) 7: 20–23, (in Russian, with Latin diagnosis).Search in Google Scholar

Seixas, P., Coutinho, P., Ferreira, M., and Otero, A. (2009). Nutritional value of the cryptophyte Rhodomonas lens for Artemia sp. J. Exp. Mar. Biol. Ecol. 381: 1–9, https://doi.org/10.1016/j.jembe.2009.09.007.Search in Google Scholar

Shalchian-Tabrizi, K., Bråte, J., Logares, R., Klaveness, D., Berney, C., and Jakobsen, K.S. (2008). Diversification of unicellular eukaryotes: cryptomonad colonizations of marine and fresh waters inferred from revised 18S rRNA phylogeny. Environ. Microbiol. 10: 2635–2644, https://doi.org/10.1111/j.1462-2920.2008.01685.x.Search in Google Scholar PubMed

Simdyanov, T.G., Diakin, A.Y., and Aleoshin, V.V. (2015). Ultrastructure and 28S rDNA phylogeny of two gregarines: Cephaloidophora cf. communis and Heliospora cf. longissima with remarks on gregarine morphology and phylogenetic analysis. Acta Protozool. 54: 241–262.Search in Google Scholar

Simdyanov, T.G., Guillou, L., Diakin, A.Y., Mikhailov, K.V., Schrével, J., and Aleoshin, V.V. (2017). A new view on the morphology and phylogeny of eugregarines suggested by the evidence from the gregarine Ancorasagittata (Leuckart, 1860) Labbé, 1899 (Apicomplexa: Eugregarinida). PeerJ 5: e3354, https://doi.org/10.7717/peerj.3354.Search in Google Scholar PubMed PubMed Central

Solarska, M., Adamski, M., and Piątek, J. (2023). Complicated family relationships, or about taxonomic problems in the family Pyrenomonadaceae (Cryptophyceae). Oceanol. Hydrobiol. Stud. 52: 299–306, https://doi.org/10.26881/oahs-2023.3.04.Search in Google Scholar

Sun, Y., Youn, S.H., Kim, Y., Kang, J.J., Lee, D., Kim, K., Jang, H.K., Jo, N., Yun, M.S., Song, S.K., et al.. (2022). Interannual variation in phytoplankton community driven by environmental factors in the northern East China Sea. Front. Mar. Sci. 9: 769497, https://doi.org/10.3389/fmars.2022.769497.Search in Google Scholar

Šupraha, L., Bosak, S., Ljubešić, Z., Mihanović, H., Olujić, G., Mikac, I., and Viličić, D. (2014). Cryptophyte bloom in a Mediterranean estuary: high abundance of Plagioselmis cf. prolonga in the Krka river estuary (eastern Adriatic Sea). Sci. Mar. 78: 329–338, https://doi.org/10.3989/scimar.03998.28c.Search in Google Scholar

Van der Auwera, G., Chapelle, S., and De Wachter, R. (1994). Structure of the large ribosomal subunit RNA of Phytophtora megasperma, and phylogeny of the oomycetes. FEBS Lett. 338: 133–136, https://doi.org/10.1016/0014-5793(94)80350-1.Search in Google Scholar PubMed

Vu, M.T., Douëtte, C., Rayner, T.A., Thoisen, C., Nielsen, S.L., and Hansen, B.W. (2016). Optimization of photosynthesis, growth, and biochemical composition of the microalga Rhodomonas salina – an established diet for live feed copepods in aquaculture. J. Appl. Phycol. 28: 1485–1500, https://doi.org/10.1007/s10811-015-0722-2.Search in Google Scholar

Wolf, M., Chen, S., Song, J., Ankenbrand, M., and Müller, T. (2013). Compensatory base changes in ITS2 secondary structures correlate with the biological species concept despite intragenomic variability in ITS2 sequences – a proof of concept. PLoS One 8: e66726, https://doi.org/10.1371/journal.pone.0066726.Search in Google Scholar PubMed PubMed Central

Xing, X.-L., Lin, X.-Y., Chen, C.-P., Gao, Y.-H., Liang, J.-R., Huang, H.-Z., Li, B.-Q., Ho, K.-C., and Qi, Y.-Z. (2008). Observations of several cryptomonad flagellates from China Sea by scanning electron microscopy. J. Systemat. Evol. 46: 205–212.Search in Google Scholar

Zhang, J., Wu, C., Pellegrini, D., Romano, G., Esposito, F., Ianora, A., and Buttino, I. (2013). Effects of different monoalgal diets on egg production, hatching success and apoptosis induction in a Mediterranean population of the calanoid copepod Acartia tonsa (Dana). Aquaculture 400: 65–72, https://doi.org/10.1016/j.aquaculture.2013.02.032.Search in Google Scholar

Zuker, M. (2003). Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res. 31: 3406–3415, https://doi.org/10.1093/nar/gkg595.Search in Google Scholar PubMed PubMed Central

Supplementary Material

This article contains supplementary material (https://doi.org/10.1515/bot-2024-0039).

Received: 2024-06-16

Accepted: 2024-09-06

Published Online: 2024-11-04

Published in Print: 2024-12-17

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Supplementary Material

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https://doi.org/10.1515/bot-2024-0039

Keywords for this article

Cryptophyceae; Proteomonas; Black Sea; morphology; phylogeny