Integrated overview of stramenopile ecology, taxonomy, and heterotrophic origin
Jazyk angličtina Země Anglie, Velká Británie Médium print
Typ dokumentu časopisecké články, přehledy
Grantová podpora
2119963
National Science Foundation
GBMF9201
Gordon and Betty Moore Foundation
CZ.02.01.01/00/22_010/0008117
VEDA FELLOWSHIPS within the Operational program Jan Amos Komensky
PubMed
39077993
PubMed Central
PMC11412368
DOI
10.1093/ismejo/wrae150
PII: 7723939
Knihovny.cz E-zdroje
- Klíčová slova
- chromalveolate hypothesis, heterotrophic flagellates, microbial ecology and evolution, plastid evolution, protistology, rhodoplex hypothesis, stramenopiles,
- MeSH
- biologická evoluce MeSH
- fylogeneze MeSH
- Heterokontophyta * klasifikace genetika MeSH
- heterotrofní procesy * MeSH
- plastidy genetika MeSH
- Publikační typ
- časopisecké články MeSH
- přehledy MeSH
Stramenopiles represent a significant proportion of aquatic and terrestrial biota. Most biologists can name a few, but these are limited to the phototrophic (e.g. diatoms and kelp) or parasitic species (e.g. oomycetes, Blastocystis), with free-living heterotrophs largely overlooked. Though our attention is slowly turning towards heterotrophs, we have only a limited understanding of their biology due to a lack of cultured models. Recent metagenomic and single-cell investigations have revealed the species richness and ecological importance of stramenopiles-especially heterotrophs. However, our lack of knowledge of the cell biology and behaviour of these organisms leads to our inability to match species to their particular ecological functions. Because photosynthetic stramenopiles are studied independently of their heterotrophic relatives, they are often treated separately in the literature. Here, we present stramenopiles as a unified group with shared synapomorphies and evolutionary history. We introduce the main lineages, describe their important biological and ecological traits, and provide a concise update on the origin of the ochrophyte plastid. We highlight the crucial role of heterotrophs and mixotrophs in our understanding of stramenopiles with the goal of inspiring future investigations in taxonomy and life history. To understand each of the many diversifications within stramenopiles-towards autotrophy, osmotrophy, or parasitism-we must understand the ancestral heterotrophic flagellate from which they each evolved. We hope the following will serve as a primer for new stramenopile researchers or as an integrative refresher to those already in the field.
Zobrazit více v PubMed
Lefèvre E, Roussel B, Amblard C et al. The molecular diversity of freshwater picoeukaryotes reveals high occurrence of putative parasitoids in the plankton. PLoS One 2008;3:e2324. 10.1371/journal.pone.0002324 PubMed DOI PMC
Singer D, Seppey CVW, Lentendu G et al. Protist taxonomic and functional diversity in soil, freshwater and marine ecosystems. Environ Int 2021;146:106262. 10.1016/j.envint.2020.106262 PubMed DOI
Seeleuthner Y, Mondy S, Lombard V et al. Single-cell genomics of multiple uncultured stramenopiles reveals underestimated functional diversity across oceans. Nat Commun 2018;9:310. 10.1038/s41467-017-02235-3 PubMed DOI PMC
Massana R, del Campo J, Sieracki ME et al. Exploring the uncultured microeukaryote majority in the oceans: reevaluation of ribogroups within stramenopiles. ISME J 2014;8:854–66. 10.1038/ismej.2013.204 PubMed DOI PMC
Thaler M, Lovejoy C. Environmental selection of marine stramenopile clades in the Arctic Ocean and coastal waters. Polar Biol 2014;37:347–57. 10.1007/s00300-013-1435-0 DOI
Xu Z, Wang M, Wu W et al. Vertical distribution of microbial eukaryotes from surface to the hadal zone of the Mariana trench. Front Microbiol 2018;9:2023. 10.3389/fmicb.2018.02023 PubMed DOI PMC
Schoenle A, Hohlfeld M, Rosse M et al. Global comparison of bicosoecid Cafeteria-like flagellates from the deep ocean and surface waters, with reorganization of the family Cafeteriaceae. Eur J Protistol 2020;73:125665. 10.1016/j.ejop.2019.125665 PubMed DOI
Park JS, Cho BC, Simpson AGB. Halocafeteria seosinensis gen. Et sp. nov. (Bicosoecida), a halophilic bacterivorous nanoflagellate isolated from a solar saltern. Extremophiles 2006;10:493–504. 10.1007/s00792-006-0001-x PubMed DOI
Schoenle A, Hohlfeld M, Rybarski A et al. Cafeteria in extreme environments: investigations on C. burkhardae and three new species from the Atacama Desert and the deep ocean. Eur J Protistol 2022;85:125905. 10.1016/j.ejop.2022.125905 PubMed DOI
Haas BJ, Kamoun S, Zody MC et al. Genome sequence and analysis of the Irish potato famine pathogen Phytophthora infestans. Nature 2009;461:393–8. 10.1038/nature08358 PubMed DOI
Lhotská Z, Jirků M, Hložková O et al. A study on the prevalence and subtype diversity of the intestinal protist Blastocystis sp. in a gut-healthy human population in the Czech Republic. Front Cell Infect Microbiol 2020;10:544335. 10.3389/fcimb.2020.544335 PubMed DOI PMC
Benoiston A-S, Ibarbalz FM, Bittner L et al. The evolution of diatoms and their biogeochemical functions. Philos Trans R Soc B Biol Sci 2017;372:20160397. 10.1098/rstb.2016.0397 PubMed DOI PMC
Nakano S, Ishii N, Manage P et al. Trophic roles of heterotrophic nanoflagellates and ciliates among planktonic organisms in a hypereutrophic pond. Aquat Microb Ecol 1998;16:153–61. 10.3354/ame016153 DOI
Sanders RW. Protists: Flagellates and amoebae. In: Mehner T and Tockner K (eds), Encyclopedia of Inland Waters, 2nd edn. Elsevier, 2022, 630–8.
Kristiansen J. Chrysophytes – Golden algae. In: Likens G.E. (ed.), Plankton of Inland Waters, 1st edn. Elsevier, 2009, 123–9.
Oborník M, Dorrell RG, Tikhonenkov DV. Editorial: mixotrophic, secondary heterotrophic, and parasitic algae. Front Plant Sci 2021;12:798555. 10.3389/fpls.2021.798555 PubMed DOI PMC
Ban H, Sato S, Yoshikawa S et al. Genome analysis of Parmales, the sister group of diatoms, reveals the evolutionary specialization of diatoms from phago-mixotrophs to photoautotrophs. Commun Biol 2023;6:697. 10.1038/s42003-023-05002-x PubMed DOI PMC
Obiol A, Muhovic I, Massana R. Oceanic heterotrophic flagellates are dominated by a few widespread taxa. Limnol Oceanogr 2021;66:4240–53. 10.1002/lno.11956 DOI
Delmont TO, Gaia M, Hinsinger DD et al. Functional repertoire convergence of distantly related eukaryotic plankton lineages abundant in the sunlit ocean. Cell Genomics 2022;2:100123. 10.1016/j.xgen.2022.100123 PubMed DOI PMC
Jamy M, Biwer C, Vaulot D et al. Global patterns and rates of habitat transitions across the eukaryotic tree of life. Nat Ecol Evol 2022;6:1458–70. 10.1038/s41559-022-01838-4 PubMed DOI PMC
Poulsen CS, Ekstrøm CT, Aarestrup FM et al. Library preparation and sequencing platform introduce bias in metagenomic-based characterizations of microbiomes. Microbiol Spectr 2022;10:e0009022. 10.1128/spectrum.00090-22 PubMed DOI PMC
McLaren MR, Willis AD, Callahan BJ. Consistent and correctable bias in metagenomic sequencing experiments. elife 2019;8:e46923. 10.7554/eLife.46923 PubMed DOI PMC
Sunagawa S, Acinas SG, Bork P et al. Tara Oceans: towards global ocean ecosystems biology. Nat Rev Microbiol 2020;18:428–45. 10.1038/s41579-020-0364-5 PubMed DOI
Sibbald SJ, Archibald JM. More protist genomes needed. Nat Ecol Evol 2017;1:0145. 10.1038/s41559-017-0145 PubMed DOI
Graupner N, Jensen M, Bock C et al. Evolution of heterotrophy in chrysophytes as reflected by comparative transcriptomics. FEMS Microbiol Ecol 2018;94:fiy039. 10.1093/femsec/fiy039 PubMed DOI PMC
Hu A, Meng F, Tanentzap AJ et al. Dark matter enhances interactions within both microbes and dissolved organic matter under global change. Environ Sci Technol 2023;57:761–9. 10.1021/acs.est.2c05052 PubMed DOI
Cavalier-Smith T, Chao EE-Y. Phylogeny and megasystematics of phagotrophic heterokonts (kingdom Chromista). J Mol Evol 2006;62:388–420. PubMed
Petersen JB. Beiträge zur Kenntnis der Flagellatengeißeln. Bot Tidsskr 1929;40:373–89.
Dodge JD. Flagella and associated structures. In: Dodge JD (ed.), The Fine Structure of Algal Cells, 1st edn. Academic Press Inc, London and New York. 1973, 57–79.
South GR, Whittick A. An Introduction to Phycology, 1st edn. Wiley, 1988, Hoboken, NJ.
Shukla SK, Mohan R, Sudhakar M. Diatoms: a potential tool to understand past oceanographic settings. Curr Sci 2009;97:1726–34.
Jirsová D, Füssy Z, Richtová J et al. Morphology, ultrastructure, and mitochondrial genome of the marine non-photosynthetic bicosoecid Cafileria marina gen. et sp. nov. Microorganisms 2019;7:240. 10.3390/microorganisms7080240 PubMed DOI PMC
Santore UJ. Flagellar and body scales in the Cryptophyceae. Br Phycol J 1983;18:239–48. 10.1080/00071618300650251 DOI
Brooker BE. Mastigonemes in a bodonid flagellate. Exp Cell Res 1965;37:300–5. 10.1016/0014-4827(65)90178-3 PubMed DOI
Fu G, Nagasato C, Oka S et al. Proteomics analysis of heterogeneous flagella in brown algae (Stramenopiles). Protist 2014;165:662–75. 10.1016/j.protis.2014.07.007 PubMed DOI
Walker CA, van West P. Zoospore development in the oomycetes. Fungal Biol Rev 2007;21:10–8. 10.1016/j.fbr.2007.02.001 DOI
Iwata I, Kimura K, Tomaru Y et al. Bothrosome formation in Schizochytrium aggregatum (Labyrinthulomycetes, Stramenopiles) during zoospore settlement. Protist 2017;168:206–19. 10.1016/j.protis.2016.12.002 PubMed DOI
Nakamura S, Tanaka G, Maeda T et al. Assembly and function of Chlamydomonas flagellar mastigonemes as probed with a monoclonal antibody. J Cell Sci 1996;109:57–62. 10.1242/jcs.109.1.57 PubMed DOI
Liu P, Lou X, Wingfield JL et al. Chlamydomonas PKD2 organizes mastigonemes, hair-like glycoprotein polymers on cilia. J Cell Biol 2020;219:e202001122. 10.1083/jcb.202001122 PubMed DOI PMC
Hee WY, Blackman LM, Hardham AR. Characterisation of Stramenopile-specific mastigoneme proteins in Phytophthora parasitica. Protoplasma 2019;256:521–35. 10.1007/s00709-018-1314-1 PubMed DOI
Sengupta S, Yang X, Higgs PG. The mechanisms of codon reassignments in mitochondrial genetic codes. J Mol Evol 2007;64:662–88. 10.1007/s00239-006-0284-7 PubMed DOI PMC
Liaud MF, Lichtlé C, Apt K et al. Compartment-specific isoforms of TPI and GAPDH are imported into diatom mitochondria as a fusion protein: evidence in favor of a mitochondrial origin of the eukaryotic glycolytic pathway. Mol Biol Evol 2000;17:213–23. 10.1093/oxfordjournals.molbev.a026301 PubMed DOI
Nakayama T, Ishida K, Archibald JM. Broad distribution of TPI-GAPDH fusion proteins among eukaryotes: evidence for glycolytic reactions in the mitochondrion? PLoS One 2012;7:e52340. 10.1371/journal.pone.0052340 PubMed DOI PMC
Río Bártulos C, Rogers MB, Williams TA et al. Mitochondrial glycolysis in a major lineage of eukaryotes. Genome Biol Evol 2018;10:2310–25. 10.1093/gbe/evy164 PubMed DOI PMC
Azuma T, Pánek T, Tice AK et al. An enigmatic stramenopile sheds light on early evolution in ochrophyta plastid organellogenesis. Mol Biol Evol 2022;39:msac065. 10.1093/molbev/msac065 PubMed DOI PMC
Cho A, Tikhonenkov DV, Hehenberger E et al. Monophyly of diverse Bigyromonadea and their impact on phylogenomic relationships within stramenopiles. Mol Phylogenet Evol 2022;171:107468. 10.1016/j.ympev.2022.107468 PubMed DOI
Khanipour Roshan S, Dumack K, Bonkowski M et al. Stramenopiles and Cercozoa dominate the heterotrophic protist community of biological soil crusts irrespective of edaphic factors. Pedobiologia - J Soil Ecol 2020;83:150673. 10.1016/j.pedobi.2020.150673 DOI
Terpis KX, Salomaki ED, Barcytė D et al. Multiple plastid losses within photosynthetic stramenopiles revealed by comprehensive phylogenomics. bioRxiv 2024; 2024.02.03.578753
Burki F, Shalchian-Tabrizi K, Minge M et al. Phylogenomics reshuffles the eukaryotic supergroups. PLoS One 2007;2:e790. 10.1371/journal.pone.0000790 PubMed DOI PMC
Burki F, Roger AJ, Brown MW et al. The new tree of eukaryotes. Trends Ecol Evol 2020;35:43–55. 10.1016/j.tree.2019.08.008 PubMed DOI
Burki F, Inagaki Y, Bråte J et al. Large-scale phylogenomic analyses reveal that two enigmatic protist lineages, Telonemia and Centroheliozoa, are related to photosynthetic Chromalveolates. Genome Biol Evol 2009;1:231–8. 10.1093/gbe/evp022 PubMed DOI PMC
Hampl V, Hug L, Leigh JW et al. Phylogenomic analyses support the monophyly of Excavata and resolve relationships among eukaryotic “supergroups”. Proc Natl Acad Sci 2009;106:3859–64. 10.1073/pnas.0807880106 PubMed DOI PMC
He D, Sierra R, Pawlowski J et al. Reducing long-branch effects in multi-protein data uncovers a close relationship between Alveolata and Rhizaria. Mol Phylogenet Evol 2016;101:1–7. 10.1016/j.ympev.2016.04.033 PubMed DOI
Sierra R, Matz MV, Aglyamova G et al. Deep relationships of Rhizaria revealed by phylogenomics: a farewell to Haeckel’s Radiolaria. Mol Phylogenet Evol 2013;67:53–9. 10.1016/j.ympev.2012.12.011 PubMed DOI
Sinha SD, Wideman JG. The persistent homology of mitochondrial ATP synthases. iScience 2023;26:106700. 10.1016/j.isci.2023.106700 PubMed DOI PMC
Patterson DJ. Stramenopiles: Chromophytes from a protistan perspective. In: Green JC, Leadbeater BSC, Diver WL (eds.), The Chromophyte Algae. Oxford University Press, Oxford UK, 1990, 357–80.
Derelle R, López-García P, Timpano H et al. A phylogenomic framework to study the diversity and evolution of stramenopiles (=heterokonts). Mol Biol Evol 2016;33:2890–8. 10.1093/molbev/msw168 PubMed DOI PMC
Riisberg I, Orr RJS, Kluge R et al. Seven gene phylogeny of Heterokonts. Protist 2009;160:191–204. 10.1016/j.protis.2008.11.004 PubMed DOI
Thakur R, Shiratori T, Ishida K. Taxon-rich multigene phylogenetic analyses resolve the phylogenetic relationship among deep-branching Stramenopiles. Protist 2019;170:125682. 10.1016/j.protis.2019.125682 PubMed DOI
Cho A, Tikhonenkov DV, Lax G et al. Phylogenomic position of genetically diverse phagotrophic stramenopile flagellates in the sediment-associated MAST-6 lineage and a potentially halotolerant placididean. Mol Phylogenet Evol 2024;190:107964. 10.1016/j.ympev.2023.107964 PubMed DOI
Cho A, Lax G, Keeling PJ. Phylogenomic analyses of ochrophytes (stramenopiles) with an emphasis on neglected lineages. Mol Phylogenet Evol 2024;198:108120. 10.1016/j.ympev.2024.108120 PubMed DOI
Moriya M, Nakayama T, Inouye I. Ultrastructure and 18S rDNA sequence analysis of Wobblia lunata gen. et sp. nov., a new heterotrophic flagellate (Stramenopiles, Incertae Sedis). Protist 2000;151:41–55. 10.1078/1434-4610-00006 PubMed DOI
Sekiguchi H, Moriya M, Nakayama T et al. Vestigial chloroplasts in heterotrophic stramenopiles Pteridomonas danica and Ciliophrys infusionum (Dictyochophyceae). Protist 2002;153:157–67. 10.1078/1434-4610-00094 PubMed DOI
Simon M, Jardillier L, Deschamps P et al. Complex communities of small protists and unexpected occurrence of typical marine lineages in shallow freshwater systems. Environ Microbiol 2015;17:3610–27. 10.1111/1462-2920.12591 PubMed DOI PMC
Adl SM, Bass D, Lane CE et al. Revisions to the classification, nomenclature, and diversity of eukaryotes. J Eukaryot Microbiol 2019;66:4–119. 10.1111/jeu.12691 PubMed DOI PMC
Sibbald SJ, Archibald JM. Genomic insights into plastid evolution. Genome Biol Evol 2020;12:978–90. 10.1093/gbe/evaa096 PubMed DOI PMC
Kamikawa R, Moog D, Zauner S et al. A non-photosynthetic diatom reveals early steps of reductive evolution in plastids. Mol Biol Evol 2017;34:2355–66. 10.1093/molbev/msx172 PubMed DOI
Kamikawa R, Azuma T, Ishii K et al. Diversity of organellar genomes in non-photosynthetic diatoms. Protist 2018;169:351–61. 10.1016/j.protis.2018.04.009 PubMed DOI
Dorrell RG, Azuma T, Nomura M et al. Principles of plastid reductive evolution illuminated by nonphotosynthetic chrysophytes. Proc Natl Acad Sci 2019;116:6914–23. 10.1073/pnas.1819976116 PubMed DOI PMC
Kayama M, Maciszewski K, Yabuki A et al. Highly reduced plastid genomes of the non-photosynthetic dictyochophyceans Pteridomonas spp. (Ochrophyta, SAR) are retained for tRNA-Glu-based organellar heme biosynthesis. Front Plant Sci 2020;11:602455. 10.3389/fpls.2020.602455 PubMed DOI PMC
Barcytė D, Jaške K, Pánek T et al. The net-like heterotrophic amoeba Leukarachnion salinum sp. nov. (Ochrophyta, Stramenopiles) has a cryptic plastid. bioRxiv 2022;2003–5.
McKie-Krisberg ZM, Sanders RW, Gast RJ. Evaluation of mixotrophy-associated gene expression in two species of polar marine algae. Front Mar Sci 2018;5:273. 10.3389/fmars.2018.00273 DOI
Li M, Chen Y, Zhang F et al. A three-dimensional mixotrophic model of Karlodinium veneficum blooms for a eutrophic estuary. Harmful Algae 2022;113:102203. 10.1016/j.hal.2022.102203 PubMed DOI
Koppelle S, López-Escardó D, Brussaard CPD et al. Mixotrophy in the bloom-forming genus Phaeocystis and other haptophytes. Harmful Algae 2022;117:102292. 10.1016/j.hal.2022.102292 PubMed DOI
Ptacnik R, Gomes A, Royer S-J et al. A light-induced shortcut in the planktonic microbial loop. Sci Rep 2016;6:29286. 10.1038/srep29286 PubMed DOI PMC
Wilken S, Yung CCM, Hamilton M et al. The need to account for cell biology in characterizing predatory mixotrophs in aquatic environments. Philos Trans R Soc B Biol Sci 2019;374:20190090. 10.1098/rstb.2019.0090 PubMed DOI PMC
Barbaglia GS, Paight C, Honig M et al. Environment-dependent metabolic investments in the mixotrophic chrysophyte Ochromonas. J Phycol 2024;60:170–84. 10.1111/jpy.13418 PubMed DOI
Green BR. After the primary endosymbiosis: an update on the chromalveolate hypothesis and the origins of algae with Chl c. Photosynth Res 2011;107:103–15. 10.1007/s11120-010-9584-2 PubMed DOI
Streckaite S, Gardian Z, Li F et al. Pigment configuration in the light-harvesting protein of the xanthophyte alga Xanthonema debile. Photosynth Res 2018;138:139–48. 10.1007/s11120-018-0557-1 PubMed DOI
Jeffrey S, Wright SW, Zapata M. Microalgal classes and their signature pigments. In: Roy S, Llewellyn C, Skarstad E, Johnsen G (eds). Phytoplankton Pigments: Characterization, Chemotaxonomy and Applications in Oceanography. 2011. Cambridge University Press, Cambridge, UK. pp. 3–77.
Pierella Karlusich JJ, Bowler C, Biswas H. Carbon dioxide concentration mechanisms in natural populations of marine diatoms: insights from Tara Oceans. Front Plant Sci 2021;12:657821. 10.3389/fpls.2021.657821 PubMed DOI PMC
Tokushima H, Inoue-Kashino N, Nakazato Y et al. Advantageous characteristics of the diatom Chaetoceros gracilis as a sustainable biofuel producer. Biotechnol Biofuels 2016;9:235. 10.1186/s13068-016-0649-0 PubMed DOI PMC
Zeni V, Baliota GV, Benelli G et al. Diatomaceous earth for arthropod pest control: back to the future. Molecules 2021;26:7487. 10.3390/molecules26247487 PubMed DOI PMC
Piotrowski K, Romanowska-Duda Z, Messyasz B. Cultivation of energy crops by ecological methods under the conditions of global climate and environmental changes with the use of diatom extract as a natural source of chemical compounds. Acta Physiol Plant 2020;42:146. 10.1007/s11738-020-03135-8 DOI
Kroth PG, Bones AM, Daboussi F et al. Genome editing in diatoms: achievements and goals. Plant Cell Rep 2018;37:1401–8. 10.1007/s00299-018-2334-1 PubMed DOI
Huang W, Daboussi F. Genetic and metabolic engineering in diatoms. Philos Trans R Soc B Biol Sci 2017;372:20160411. 10.1098/rstb.2016.0411 PubMed DOI PMC
Vergés A, Campbell AH. Kelp forests. Curr Biol 2020;30:R919–20. 10.1016/j.cub.2020.06.053 PubMed DOI
Smale DA. Impacts of ocean warming on kelp forest ecosystems. New Phytol 2020;225:1447–54. 10.1111/nph.16107 PubMed DOI
Neushul M. Studies on the giant kelp, macrocystis.II.Reproduction. Am J Bot 1963;50:354–9. 10.1002/j.1537-2197.1963.tb07203.x DOI
B-Béres V, Stenger-Kovács C, Buczkó K et al. Ecosystem services provided by freshwater and marine diatoms. Hydrobiologia 2023;850:2707–33. 10.1007/s10750-022-04984-9 DOI
Kim MJ, Yun HY, Shin K-H et al. Evaluation of food web structure and complexity in the process of kelp bed recovery using stable isotope analysis. Front Mar Sci 2022;9:885676. 10.3389/fmars.2022.885676 DOI
Taucher J, Bach LT, Prowe AEF et al. Enhanced silica export in a future ocean triggers global diatom decline. Nature 2022;605:696–700. 10.1038/s41586-022-04687-0 PubMed DOI PMC
Pernice MC, Giner CR, Logares R et al. Large variability of bathypelagic microbial eukaryotic communities across the world’s oceans. ISME J 2016;10:945–58. 10.1038/ismej.2015.170 PubMed DOI PMC
Nicholls KH, Wujek DE. Chrysophyceae and Phaeothamniophyceae. In: Wehr JD, Sheath RG, Kociolek JP (eds.), Freshwater Algae of North America, 2nd edn. Academic Press Inc Hoboken, NJ, 2015, 537–86.
Lie AAY, Liu Z, Terrado R et al. A tale of two mixotrophic chrysophytes: insights into the metabolisms of two Ochromonas species (Chrysophyceae) through a comparison of gene expression. PLoS One 2018;13:e0192439. 10.1371/journal.pone.0192439 PubMed DOI PMC
Wilken S, Choi CJ, Worden AZ. Contrasting mixotrophic lifestyles reveal different ecological niches in two closely related marine protists. J Phycol 2020;56:52–67. 10.1111/jpy.12920 PubMed DOI PMC
Holen DA, Boraas ME. The feeding behavior of Spumella sp. as a function of particle size: implications for bacterial size in pelagic systems. Hydrobiologia 1991;220:73–88. 10.1007/BF00017493 DOI
Meyer N, Rydzyk A, Pohnert G. Pronounced uptake and metabolism of organic substrates by diatoms revealed by pulse-labeling metabolomics. Front Mar Sci 2022;9:821167. 10.3389/fmars.2022.821167 DOI
Mitra A, Caron DA, Faure E et al. The Mixoplankton Database (MDB): diversity of photo-phago-trophic plankton in form, function, and distribution across the global ocean. J Eukaryot Microbiol 2023;70:e12972. 10.1111/jeu.12972 PubMed DOI
Godrijan J, Drapeau D, Balch WM. Mixotrophic uptake of organic compounds by coccolithophores. Limnol Oceanogr 2020;65:1410–21. 10.1002/lno.11396 DOI
Balch WM, Drapeau DT, Poulton N et al. Osmotrophy of dissolved organic compounds by coccolithophore populations: fixation into particulate organic and inorganic carbon. Sci Adv 2023;9:eadf6973. 10.1126/sciadv.adf6973 PubMed DOI PMC
Kamikawa R, Mochizuki T, Sakamoto M et al. Genome evolution of a nonparasitic secondary heterotroph, the diatom Nitzschia putrida. Sci Adv 2022;8:eabi5075. 10.1126/sciadv.abi5075 PubMed DOI PMC
Maberly SC, Ball LA, Raven JA et al. Inorganic carbon acquisition by chrysophytes. J Phycol 2009;45:1052–61. 10.1111/j.1529-8817.2009.00734.x PubMed DOI
Terrado R, Pasulka AL, Lie AAY et al. Autotrophic and heterotrophic acquisition of carbon and nitrogen by a mixotrophic chrysophyte established through stable isotope analysis. ISME J 2017;11:2022–34. 10.1038/ismej.2017.68 PubMed DOI PMC
Terrado R, Monier A, Edgar R et al. Diversity of nitrogen assimilation pathways among microbial photosynthetic eukaryotes. J Phycol 2015;51:490–506. 10.1111/jpy.12292 PubMed DOI
Kamjunke N, Henrichs T, Gaedke U. Phosphorus gain by bacterivory promotes the mixotrophic flagellate Dinobryon spp. during re-oligotrophication. J Plankton Res 2006;29:39–46. 10.1093/plankt/fbl054 DOI
Rothhaupt KO. Utilization of substitutable carbon and phosphorus sources by the mixotrophic chrysophyte Ochromonas sp. Ecology 1996;77:706–15. 10.2307/2265495 DOI
Johnson WM, Alexander H, Bier RL et al. Auxotrophic interactions: a stabilizing attribute of aquatic microbial communities? FEMS Microbiol Ecol 2020;96:fiaa115. 10.1093/femsec/fiaa115 PubMed DOI PMC
Faure E, Not F, Benoiston A-S et al. Mixotrophic protists display contrasted biogeographies in the global ocean. ISME J 2019;13:1072–83. 10.1038/s41396-018-0340-5 PubMed DOI PMC
Leles SG, Mitra A, Flynn KJ et al. Oceanic protists with different forms of acquired phototrophy display contrasting biogeographies and abundance. Proc R Soc B Biol Sci 2017;284:20170664. 10.1098/rspb.2017.0664 PubMed DOI PMC
Tanaka R, Tanaka A. Tetrapyrrole biosynthesis in higher plants. Annu Rev Plant Biol 2007;58:321–46. 10.1146/annurev.arplant.57.032905.105448 PubMed DOI
López G, Yate C, Ramos FA et al. Production of polyunsaturated fatty acids and lipids from autotrophic, mixotrophic and heterotrophic cultivation of Galdieria sp. strain USBA-GBX-832. Sci Rep 2019;9:10791. 10.1038/s41598-019-46645-3 PubMed DOI PMC
Boëchat IG, Weithoff G, Krüger A et al. A biochemical explanation for the success of mixotrophy in the flagellate Ochromonas sp. Limnol Oceanogr 2007;52:1624–32. 10.4319/lo.2007.52.4.1624 DOI
Brown JW, Sorhannus U. A molecular genetic timescale for the diversification of autotrophic stramenopiles (Ochrophyta): substantive underestimation of putative fossil ages. PLoS One 2010;5:e12759. 10.1371/journal.pone.0012759 PubMed DOI PMC
Burki F, Kaplan M, Tikhonenkov DV et al. Untangling the early diversification of eukaryotes: a phylogenomic study of the evolutionary origins of Centrohelida, Haptophyta and Cryptista. Proc R Soc B Biol Sci 2016;283:20152802. 10.1098/rspb.2015.2802 PubMed DOI PMC
Keeling PJ. Chromalveolates and the evolution of plastids by secondary endosymbiosis. J Eukaryot Microbiol 2009;56:1–8. 10.1111/j.1550-7408.2008.00371.x PubMed DOI
Ševčíková T, Horák A, Klimeš V et al. Updating algal evolutionary relationships through plastid genome sequencing: did alveolate plastids emerge through endosymbiosis of an ochrophyte? Sci Rep 2015;5:10134. 10.1038/srep10134 PubMed DOI PMC
Cavalier-Smith T. Principles of protein and lipid targeting in secondary symbiogenesis: euglenoid, dinoflagellate, and sporozoan plastid origins and the eukaryote family tree. J Eukaryot Microbiol 1999;46:347–66. 10.1111/j.1550-7408.1999.tb04614.x PubMed DOI
Khan H, Parks N, Kozera C et al. Plastid genome sequence of the cryptophyte alga Rhodomonas salina CCMP1319: lateral transfer of putative DNA replication machinery and a test of chromist plastid phylogeny. Mol Biol Evol 2007;24:1832–42. 10.1093/molbev/msm101 PubMed DOI
Dorrell RG, Gile G, McCallum G et al. Chimeric origins of ochrophytes and haptophytes revealed through an ancient plastid proteome. elife 2017;6:e23717. 10.7554/eLife.23717 PubMed DOI PMC
Baurain D, Brinkmann H, Petersen J et al. Phylogenomic evidence for separate acquisition of plastids in cryptophytes, haptophytes, and stramenopiles. Mol Biol Evol 2010;27:1698–709. 10.1093/molbev/msq059 PubMed DOI
Yoon HS, Hackett JD, Pinto G et al. The single, ancient origin of chromist plastids. Proc Natl Acad Sci 2002;99:15507–12. 10.1073/pnas.242379899 PubMed DOI PMC
Fast NM, Kissinger JC, Roos DS et al. Nuclear-encoded, plastid-targeted genes suggest a single common origin for apicomplexan and dinoflagellate plastids. Mol Biol Evol 2001;18:418–26. 10.1093/oxfordjournals.molbev.a003818 PubMed DOI
Tyler BM, Tripathy S, Zhang X et al. Phytophthora genome sequences uncover evolutionary origins and mechanisms of pathogenesis. Science 2006;313:1261–6. 10.1126/science.1128796 PubMed DOI
Sargent JR, Bell M V., Henderson RJ. Protists as sources of (n-3) polyunsaturated fatty acids for vertebrate development. In: Brugerolle G, Mignot JP (eds). Proceedings of the Second European Congress of Protistology. 1995. Clermont-Ferrand, pp. 54–64.
Harper JT, Keeling PJ. Nucleus-encoded, plastid-targeted glyceraldehyde-3-phosphate dehydrogenase (GAPDH) indicates a single origin for chromalveolate plastids. Mol Biol Evol 2003;20:1730–5. 10.1093/molbev/msg195 PubMed DOI
Wang Q, Sun H, Huang J. Re-analyses of “algal” genes suggest a complex evolutionary history of oomycetes. Front Plant Sci 2017;8:1540. 10.3389/fpls.2017.01540 PubMed DOI PMC
Santos HJ, Nozaki T. The mitosome of the anaerobic parasitic protist Entamoeba histolytica: a peculiar and minimalist mitochondrion-related organelle. J Eukaryot Microbiol 2022;69:e12923. 10.1111/jeu.12923 PubMed DOI PMC
Muñoz-Gómez SA. Energetics and evolution of anaerobic microbial eukaryotes. Nat Microbiol 2023;8:197–203. 10.1038/s41564-022-01299-2 PubMed DOI
Karnkowska A, Vacek V, Zubáčová Z et al. A eukaryote without a mitochondrial organelle. Curr Biol 2016;26:1274–84. 10.1016/j.cub.2016.03.053 PubMed DOI
Hjort K, Goldberg AV, Tsaousis AD et al. Diversity and reductive evolution of mitochondria among microbial eukaryotes. Philos Trans R Soc B Biol Sci 2010;365:713–27. 10.1098/rstb.2009.0224 PubMed DOI PMC
Salomaki E, Kolisko M. There is treasure everywhere: reductive plastid evolution in apicomplexa in light of their close relatives. Biomol Ther 2019;9:378. 10.3390/biom9080378 PubMed DOI PMC
Makiuchi T, Nozaki T. Highly divergent mitochondrion-related organelles in anaerobic parasitic protozoa. Biochimie 2014;100:3–17. 10.1016/j.biochi.2013.11.018 PubMed DOI
Zhu G, Marchewka MJ, Keithly JS. Cryptosporidium parvum appears to lack a plastid genome. Microbiology 2000;146:315–21. 10.1099/00221287-146-2-315 PubMed DOI
Gornik SG, Febrimarsa CAM, MacRae JI et al. Endosymbiosis undone by stepwise elimination of the plastid in a parasitic dinoflagellate. Proc Natl Acad Sci USA 2015;112:5767–72. 10.1073/pnas.1423400112 PubMed DOI PMC
Schön ME, Zlatogursky VV, Singh RP et al. Single cell genomics reveals plastid-lacking Picozoa are close relatives of red algae. Nat Commun 2021;12:6651. 10.1038/s41467-021-26918-0 PubMed DOI PMC
Burki F. The eukaryotic tree of life from a global phylogenomic perspective. Cold Spring Harb Perspect Biol 2014;6:a016147–7. 10.1101/cshperspect.a016147 PubMed DOI PMC
Adl SM, Simpson AGB, Lane CE et al. The revised classification of eukaryotes. J Eukaryot Microbiol 2012;59:429–514. 10.1111/j.1550-7408.2012.00644.x PubMed DOI PMC
Petersen J, Ludewig A-K, Michael V et al. Chromera velia, endosymbioses and the rhodoplex hypothesis—plastid evolution in cryptophytes, alveolates, stramenopiles, and haptophytes (CASH lineages). Genome Biol Evol 2014;6:666–84. 10.1093/gbe/evu043 PubMed DOI PMC
Hempel F, Bullmann L, Lau J et al. ERAD-derived preprotein transport across the second outermost plastid membrane of diatoms. Mol Biol Evol 2009;26:1781–90. 10.1093/molbev/msp079 PubMed DOI
Felsner G, Sommer MS, Gruenheit N et al. ERAD components in organisms with complex red plastids suggest recruitment of a preexisting protein transport pathway for the periplastid membrane. Genome Biol Evol 2011;3:140–50. 10.1093/gbe/evq074 PubMed DOI PMC
Kienle N, Kloepper TH, Fasshauer D. Shedding light on the expansion and diversification of the Cdc48 protein family during the rise of the eukaryotic cell. BMC Evol Biol 2016;16:215. 10.1186/s12862-016-0790-1 PubMed DOI PMC
Sommer MS, Gould SB, Lehmann P et al. Der1-mediated preprotein import into the periplastid compartment of chromalveolates? Mol Biol Evol 2007;24:918–28. 10.1093/molbev/msm008 PubMed DOI
Bolte K, Gruenheit N, Felsner G et al. Making new out of old: recycling and modification of an ancient protein translocation system during eukaryotic evolution. BioEssays 2011;33:368–76. 10.1002/bies.201100007 PubMed DOI
Stiller JW, Schreiber J, Yue J et al. The evolution of photosynthesis in chromist algae through serial endosymbioses. Nat Commun 2014;5:5764. 10.1038/ncomms6764 PubMed DOI PMC
Bodył A, Stiller JW, Mackiewicz P. Chromalveolate plastids: direct descent or multiple endosymbioses? Trends Ecol Evol 2009;24:119–21. PubMed
Strassert JFH, Irisarri I, Williams TA et al. A molecular timescale for eukaryote evolution with implications for the origin of red algal-derived plastids. Nat Commun 2021;12:1879. 10.1038/s41467-021-22044-z PubMed DOI PMC
Kim JI, Moore CE, Archibald JM et al. Evolutionary dynamics of cryptophyte plastid genomes. Genome Biol Evol 2017;9:1859–72. 10.1093/gbe/evx123 PubMed DOI PMC
Karnkowska A, Yubuki N, Maruyama M et al. Euglenozoan kleptoplasty illuminates the early evolution of photoendosymbiosis. Proc Natl Acad Sci 2023;120:e2220100120. 10.1073/pnas.2220100120 PubMed DOI PMC
Shiratori T, Nakayama T, Ishida K. A new deep-branching stramenopile, Platysulcus tardus gen. Nov., sp. nov. Protist 2015;166:337–48. 10.1016/j.protis.2015.05.001 PubMed DOI
Leonard G, Labarre A, Milner DS et al. Comparative genomic analysis of the ‘pseudofungus’ Hyphochytrium catenoides. Open Biol 2018;8:170184. 10.1098/rsob.170184 PubMed DOI PMC
Spanu PD, Panstruga R. Editorial: biotrophic plant-microbe interactions. Front Plant Sci 2017;8:192. PubMed PMC
Martin F, Kohler A, Murat C et al. Unearthing the roots of ectomycorrhizal symbioses. Nat Rev Microbiol 2016;14:760–73. 10.1038/nrmicro.2016.149 PubMed DOI
Van der Auwera G, De Baere R, Van de Peer Y et al. The phylogeny of the Hyphochytriomycota as deduced from ribosomal RNA sequences of Hyphochytrium catenoides. Mol Biol Evol 1995;12:671–8. PubMed
Lévesque CA. Fifty years of oomycetes—from consolidation to evolutionary and genomic exploration. Fungal Divers 2011;50:35–46. 10.1007/s13225-011-0128-7 DOI
Lévesque CA, Brouwer H, Cano L et al. Genome sequence of the necrotrophic plant pathogen Pythium ultimum reveals original pathogenicity mechanisms and effector repertoire. Genome Biol 2010;11:R73. 10.1186/gb-2010-11-7-r73 PubMed DOI PMC
Richards TA, Soanes DM, Jones MDM et al. Horizontal gene transfer facilitated the evolution of plant parasitic mechanisms in the oomycetes. Proc Natl Acad Sci 2011;108:15258–63. 10.1073/pnas.1105100108 PubMed DOI PMC
Savory F, Leonard G, Richards TA. The role of horizontal gene transfer in the evolution of the oomycetes. PLoS Pathog 2015;11:e1004805. 10.1371/journal.ppat.1004805 PubMed DOI PMC
Aleoshin VV, Mylnikov AP, Mirzaeva GS et al. Heterokont predator Develorapax marinus gen. et sp. nov. – a model of the ochrophyte ancestor. Front Microbiol 2016;7:1194. PubMed PMC
Leipe DD, Tong SM, Goggin CL et al. 16S-like rDNA sequences from Developayella elegans, Labyrinthuloides haliotidis, and Proteromonas lacertae confirm that the stramenopiles are a primarily heterotrophic group. Eur J Protistol 1996;32:449–58. 10.1016/S0932-4739(96)80004-6 DOI
Weiler BA, Elisabet LS, Sieracki ME et al. Mediocremonas mediterraneus, a new member within the developea. J Eukaryot Microbiol 2021;68:12825. 10.1111/jeu.12825 PubMed DOI
Silberman JD, Sogin ML, Leipe DD et al. Human parasite finds taxonomic home. Nature 1996;380:398–8. 10.1038/380398a0 PubMed DOI
Bahnweg G, Sparrow FK. Aplanochytrium kerguelensis gen. nov. spec. nov., a new phycomycete from subantarctic marine waters. Arch Mikrobiol 1972;81:45–9. 10.1007/BF00715023 PubMed DOI
Yubuki N, Pánek T, Yabuki A et al. Morphological identities of two different marine stramenopile environmental sequence clades: Bicosoeca kenaiensis (Hilliard, 1971) and Cantina marsupialis (Larsen and Patterson, 1990) gen. nov., comb. nov. J Eukaryot Microbiol 2015;62:532–42. 10.1111/jeu.12207 PubMed DOI
Labarre A, López-Escardó D, Latorre F et al. Comparative genomics reveals new functional insights in uncultured MAST species. ISME J 2021;15:1767–81. 10.1038/s41396-020-00885-8 PubMed DOI PMC
de Vargas C, Audic S, Henry N et al. Eukaryotic plankton diversity in the sunlit ocean. Science 2015;348:1261605. 10.1126/science.1261605 PubMed DOI
Wideman JG, Monier A, Rodríguez-Martínez R et al. Unexpected mitochondrial genome diversity revealed by targeted single-cell genomics of heterotrophic flagellated protists. Nat Microbiol 2019;5:154–65. 10.1038/s41564-019-0605-4 PubMed DOI
Cavalier-Smith T, Scoble JM. Phylogeny of Heterokonta: Incisomonas marina, a uniciliate gliding opalozoan related to Solenicola (Nanomonadea), and evidence that Actinophryida evolved from raphidophytes. Eur J Protistol 2013;49:328–53. 10.1016/j.ejop.2012.09.002 PubMed DOI
Shiratori T, Thakur R, Ishida K. Pseudophyllomitus vesiculosus (Larsen and Patterson 1990) lee, 2002, a poorly studied phagotrophic biflagellate is the first characterized member of Stramenopile environmental clade MAST-6. Protist 2017;168:439–51. 10.1016/j.protis.2017.06.004 PubMed DOI
Tsui CKM, Marshall W, Yokoyama R et al. Labyrinthulomycetes phylogeny and its implications for the evolutionary loss of chloroplasts and gain of ectoplasmic gliding. Mol Phylogenet Evol 2009;50:129–40. 10.1016/j.ympev.2008.09.027 PubMed DOI
Raghukumar S, Damare VS. Increasing evidence for the important role of Labyrinthulomycetes in marine ecosystems. Bot Mar 2011;54:3–11. 10.1515/bot.2011.008 DOI
Xie N, Hunt DE, Johnson ZI et al. Annual partitioning patterns of labyrinthulomycetes protists reveal their multifaceted role in marine microbial food webs. Appl Environ Microbiol 2021;87:e01652–20. 10.1128/AEM.01652-20 PubMed DOI PMC
Rubin E, Tanguy A, Pales Espinosa E et al. Differential gene expression in five isolates of the clam pathogen, quahog parasite unknown (QPX). J Eukaryot Microbiol 2017;64:647–54. 10.1111/jeu.12400 PubMed DOI
Xie N, Wang Z, Hunt DE et al. Niche partitioning of Labyrinthulomycete protists across sharp coastal gradients and their putative relationships with bacteria and fungi. Front Microbiol 2022;13:906864. 10.3389/fmicb.2022.906864 PubMed DOI PMC
Hamamoto Y, Honda D. Nutritional intake of Aplanochytrium (Labyrinthulea, Stramenopiles) from living diatoms revealed by culture experiments suggesting the new prey–predator interactions in the grazing food web of the marine ecosystem. PLoS One 2019;14:e0208941. 10.1371/journal.pone.0208941 PubMed DOI PMC
Gomaa F, Mitchell EAD, Lara E. Amphitremida (Poche, 1913) is a new major, ubiquitous labyrinthulomycete clade. PLoS One 2013;8:e53046. 10.1371/journal.pone.0053046 PubMed DOI PMC
Takahashi Y, Yoshida M, Inouye I et al. Fibrophrys columna gen. nov., sp. nov: a member of the family Amphifilidae. Eur J Protistol 2016;56:41–50. 10.1016/j.ejop.2016.06.003 PubMed DOI
Pan J, del Campo J, Keeling PJ. Reference tree and environmental sequence diversity of Labyrinthulomycetes. J Eukaryot Microbiol 2017;64:88–96. 10.1111/jeu.12342 PubMed DOI
Takahashi Y, Yoshida M, Inouye I et al. Diplophrys mutabilis sp. nov., a new member of Labyrinthulomycetes from freshwater habitats. Protist 2014;165:50–65. 10.1016/j.protis.2013.10.001 PubMed DOI
Qiu X, Xie X, Meesapyodsuk D. Molecular mechanisms for biosynthesis and assembly of nutritionally important very long chain polyunsaturated fatty acids in microorganisms. Prog Lipid Res 2020;79:101047. 10.1016/j.plipres.2020.101047 PubMed DOI
Ishibashi Y, Goda H, Hamaguchi R et al. PUFA synthase-independent DHA synthesis pathway in Parietichytrium sp. and its modification to produce EPA and n-3DPA. Commun Biol 2021;4:1378. 10.1038/s42003-021-02857-w PubMed DOI PMC
Sanders RW, Porter KG, Bennett SJ et al. Seasonal patterns of bacterivory by flagellates, ciliates, rotifers, and cladocerans in a freshwater planktonic community. Limnol Oceanogr 1989;34:673–87. 10.4319/lo.1989.34.4.0673 DOI
Hahn MW, Höfle MG. Grazing of protozoa and its effect on populations of aquatic bacteria. FEMS Microbiol Ecol 2001;35:113–21. 10.1111/j.1574-6941.2001.tb00794.x PubMed DOI
Harder CB, Ekelund F, Karpov SA. Ultrastructure and phylogenetic position of regin rotiferus and Otto terricolus genera et species novae (Bicosoecida, Heterokonta/Stramenopiles). Protist 2014;165:144–60. 10.1016/j.protis.2014.01.004 PubMed DOI
Moestrup Ø. Current status of chtysophyte ‘splinter groups’: Synurophytes, pedinellis, silicoflagellates. In: Sandgren C, Smol JP, Kristiansen J (eds). Chrysophyte Algae: Ecology, Phylogeny and Development, 1st ed. 1995. Cambridge University Press, Cambridge, pp. 1535–5, 10.1017/CBO9780511752292.005. DOI
Preisig HR. A modern concept of chrysophyte classification. In: Sandgren C, Smol JP, Kristiansen J (eds). Chrysophyte Algae: Ecology, Phylogeny, Development, 1st ed. 1995. Cambridge University Press, Cambridge, pp. 47–74, 10.1017/CBO9780511752292.004. DOI
O’Kelly CJ, Patterson DJ. The flagellar apparatus of cafeteria roenbergensis Fenchel & Patterson, 1988 (Bicosoecales = Bicosoecida). Eur J Protistol 1996;32:216–26. 10.1016/S0932-4739(96)80021-6 DOI
Millette NC, Gast RJ, Luo JY et al. Mixoplankton and mixotrophy: future research priorities. J Plankton Res 2023;45:576–96. 10.1093/plankt/fbad020 PubMed DOI PMC
Fenchel T, Patterson DJ. Cafeteria roenbergensis nov. gen., nov. sp., a heterotrophic microflagellate from marine plankton. Mar Microb Food Webs 1988;3:9–19.
Baricevic A, Maric Pfannkuchen D, Smodlaka Tankovic M et al. Identification of the heterotrophic nanoflagellate Bilabrum latius in the southern Adriatic (Mediterranean Sea). Eur J Protistol 2023;90:125999. 10.1016/j.ejop.2023.125999 PubMed DOI
Burger G, O’Kelly C, Gray MW et al. Cafeteria Roenbergensis Mitochondrial DNA Complete Sequence OGMP Accession no. AF193903, 1999.
Hackl T, Martin R, Barenhoff K et al. Four high-quality draft genome assemblies of the marine heterotrophic nanoflagellate cafeteria roenbergensis. Sci Data 2020;7:29. 10.1038/s41597-020-0363-4 PubMed DOI PMC
Boegnik J, Matz C, Jürgens K et al. Confusing selective feeding with differential digestion in bacterivorous nanoflagellates. J Eukaryot Microbiol 2001;48:425–32. 10.1111/j.1550-7408.2001.tb00175.x PubMed DOI
Ishigaki T, Terazaki M. Grazing behavior of heterotrophic nanoflagellates observed with a high speed VTR system. J Eukaryot Microbiol 1998;45:484–7. 10.1111/j.1550-7408.1998.tb05104.x DOI
Jürgens K, Massana R. Protistan grazing on marine bacterioplankton. In: Kirchman D.L. (ed.), Microbial Ecology of the Oceans, 2nd edn. John Wiley & Sons, Inc., Hoboken, NJ, 2008, 383–441.
Fischer MG, Allen MJ, Wilson WH et al. Giant virus with a remarkable complement of genes infects marine zooplankton. Proc Natl Acad Sci USA 2010;107:19508–13. 10.1073/pnas.1007615107 PubMed DOI PMC
Massana R, Del Campo J, Dinter C et al. Crash of a population of the marine heterotrophic flagellate cafeteria roenbergensis by viral infection. Environ Microbiol 2007;9:2660–9. 10.1111/j.1462-2920.2007.01378.x PubMed DOI
Gómez F, Moreira D, Benzerara K et al. Solenicola setigera is the first characterized member of the abundant and cosmopolitan uncultured marine stramenopile group MAST-3. Environ Microbiol 2011;13:193–202. 10.1111/j.1462-2920.2010.02320.x PubMed DOI
Moriya M, Nakayama T, Inouye I. A new class of the stramenopiles, placididea classis nova: description of Placidia cafeteriopsis gen. Et sp. nov. Protist 2002;153:143–56. 10.1078/1434-4610-00093 PubMed DOI
Okamura T, Kondo R. Suigetsumonas clinomigrationis gen. Et sp. nov., a novel facultative anaerobic nanoflagellate isolated from the meromictic Lake Suigetsu, Japan. Protist 2015;166:409–21. 10.1016/j.protis.2015.06.003 PubMed DOI
Park JS, Simpson AGB. Characterization of halotolerant Bicosoecida and Placididea (Stramenopila) that are distinct from marine forms, and the phylogenetic pattern of salinity preference in heterotrophic stramenopiles. Environ Microbiol 2010;12:1173–84. 10.1111/j.1462-2920.2010.02158.x PubMed DOI
Rybarski AE, Nitsche F, Soo Park J et al. Revision of the phylogeny of Placididea (Stramenopiles): molecular and morphological diversity of novel placidid protists from extreme aquatic environments. Eur J Protistol 2021;81:125809. 10.1016/j.ejop.2021.125809 PubMed DOI
Kostka M. Opalinata. In: Archibald J.M., AGB S., Slamovits C.H. et al. (eds.), Handbook of the Protists, 2nd edn. Cham: Springer International Publishing, 2016, 1–23.
Corliss JO. The opalinid infusorians: flagellates or ciliates? J Protozool 1955;2:107–14. 10.1111/j.1550-7408.1955.tb02410.x DOI
Zhao W, Hu G, Ponce-Gordo F et al. Morphological description of Opalina obtrigonoidea Metcalf, 1923 (Heterokonta, Opalinea) from Duttaphrynus melanostictus and evaluation of the ITS region as a suitable genetic marker for inter-species identification in Opalina. Parasitol Int 2020;76:102103. 10.1016/j.parint.2020.102103 PubMed DOI
Wang R, Zhao W, Hu G et al. Redescription of Opalina triangulata (Heterokonta, Opalinea) from Fejervarya limnocharis based on morphological and molecular data. Eur J Protistol 2019;71:125639. 10.1016/j.ejop.2019.125639 PubMed DOI
Li M, Hu G, Zhao W et al. A revised taxonomy and phylogeny of opalinids (Stramenopiles: Opalinata) inferred from the analysis of complete nuclear ribosomal DNA genes. Zool J Linnean Soc 2023;201:269–89. 10.1093/zoolinnean/zlad150 DOI
Tan KSW. New insights on classification, identification, and clinical relevance of Blastocystis spp. Clin Microbiol Rev 2008;21:639–65. 10.1128/CMR.00022-08 PubMed DOI PMC
Burki F. The convoluted evolution of eukaryotes with complex plastids. Advances in Botanical Research, 2017;84:1–30. 10.1016/bs.abr.2017.06.001 DOI
Guillou L, Chrétiennot-Dinet M-J, Boulben S et al. Symbiomonas scintillans gen. et sp. nov. and Picophagus flagellatus gen. et sp. nov. (Heterokonta): two new heterotrophic flagellates of picoplanktonic size. Protist 1999;150:383–98. 10.1016/S1434-4610(99)70040-4 PubMed DOI