A Hotspot of Amoebae Diversity: 8 New Naked Amoebae Associated with the Planktonic Bloom-forming Cyanobacterium Microcystis

Jeroen van Wichelen,

Sofie d’Hondt,

Myriam Claeys,

Wim Vyverman,

Cédric Berney,

David Bass,

Pieter Vanormelingen

Abstrakt

The colonies of Microcystis, one of the most common bloom-forming cyanobacteria worldwide, harbor a diverse community of microorganisms. Among these, naked amoebae feeding on Microcystis cells can strongly influence natural Microcystis population dynamics. In this study, we investigated the species diversity of these amoebae based on 26 Microcystis-associated amoebae (MAA) strains from eutrophied water bodies in Belgium and elsewhere in western Europe. A detailed morphological characterization in combination with 18S rDNA (SSU) phylogenies revealed the presence of no less than 10 species. Nine of these belonged to the known genera Vannella (2 species), Korotnevella (2), Copromyxa (2), Vexillifera (1), Cochliopodium (1) and the recently described Angulamoeba (1). Only two were previously described, the others were new to science. One taxon could not be assigned to a known genus and is here described as Schoutedamoeba gen. n., representing a new variosean lineage. The discovery of so many new species from only one very specific habitat (Microcystis colonies) from a rather restricted geographical area indicates that the diversity of planktonic naked amoebae is much higher than previously appreciated and that only a tiny fraction of the total diversity of naked amoebae is currently known.

Słowa kluczowe: Naked amoebae, Microcystis, morphology, 18S rDNA, harmful algal blooms, grazing, Europe
References

Agatha S. (2004) Evolution of ciliary patterns in the Oligotrichida (Ciliophora, Spirotricha) and its taxonomic implications. Zoology 107: 153–168

Anderson O. R. (1977) The fine structure of a marine amoeba associated with a blue-green alga in the Sargasso Sea. J. Protozool. 24: 370

Anderson O. R., Rogerson A. (1995) Annual abundances and growth-potential of Gymnamoebae in the Hudson Estuary with comparative data from the Firth of Clyde. Eur. J. Protistol. 31: 223–233

Anderson O. R., Rogerson J. A., Hannah F. (1997) Three new limax amoebae isolated from marine surface sediments: Vahlkampfia caledonica n. sp., Saccamoeba marina n. sp., and Hartmannella vacuolata n. sp. J. Euk. Microbiol. 44: 33–42

Anderson O. R. (2011) Particle-associated planktonic naked amoebae in the Hudson Estuary: size-fraction related densities, cell sizes and estimated carbon content. Acta Protozool. 50: 15–22

Anderson O. R., Tekle Y. I. (2013) A description of Cochliopodium megatetrastylus n. sp. isolated from a freshwater habitat. Acta Protozool. 52: 55–64

Arndt H. (1993) A critical review of the importance of rhizopods (naked and testate amoebae) and actinopods (heliozoa) in lake plankton. Marine Microbial Food Webs 7: 3–29

Bailey-Watts A. E., Lund J. W. G. (1973) Observations on a diatom bloom in Loch Leven, Scotland. Biol. J. Linn. Soc. 5: 235–253

Becares E., Romo S. (1994) Selective predation of Thecamoeba sphaeronucleolus (Greeff, 1891) on filamentous algae in natural conditions. J. Gen. Appl. Microbiol. 40: 15–21

BerneyC., GeisenS., Van WichelenJ., NitscheF., VanormelingenP., BonkowskiM., BassD. (2015) Expansion of the ‘reticulosphere’: diversity of novel branching and network-forming amoebae helps to define Variosea (Amoebozoa). Protist 166: 271–295

Bovee E. C. (1953) Morphological identification of free-living Amoebida. Proc. Iowa Acad. Sci. 60: 599–615

Bovee E. C. (1985) The lobose amebas III. Descriptions of nine new conopodous amebas of the genus Vexillifera Schaeffer, 1926, emd. BOVEE 1951, 1970, with comments on the genus. Arch. Protistenk. 129: 101–118

Brown M. W., Silberman J. D., Spiegel F. W. (2011) ‘Slime molds’ among the Tubulinea (Amoebozoa): molecular systematics and taxonomy of Copromyxa. Protist 162: 277–287

Brunberg A. K. (1999) Contribution of bacteria in the mucilage of Microcystis spp. (Cyanobacteria) to benthic and pelagic bacterial production in a hypereutrophic lake. FEMS Microbiol. Ecol. 29: 13–22

Cai H., Jiang H., Krumholz L. R., Yang Z. (2014) Bacterial community composition of size-fractioned aggregates within the phycosphere of cyanobacterial blooms in a eutrophic freshwater lake. PLoS ONE 9: e102879. doi:10.1371/journal.pone.0102879

Canter H. M., Lund J. W. G. (1968) The importance of Protozoa in controlling abundance of planktonic algae in lakes. P. Linn. Soc. L.
179: 203–219

Canter-Lund H. M., Lund J. W. G. (1995) Freshwater Algae, their microscopic world explored. Biopress Ltd., Bristol.

Caron D. A., Swanberg N. R. (1990) The ecology of planktonic sarcodines. Rev. Aquat. Sci. 3: 147–180

Cook W. L., Ahearn D. G. (1976) Natural control of Anabaena blooms by the amoeba Asterocaelum anabaenophilum sp. nov.In:The distributional History of the Biota of the Southern Appalachians. Part IV. Algae and Fungi. Biogeography, Systematics, and Ecology, (Eds. B. C. Parker, M. K. Roane). University Press of Virginia, Charlottesville, 71–80

Corsaro D., Michel R., Walochnik J., Müller K. D., Greub G. (2010) Saccamoeba lacustris, sp. nov. (Amoebozoa: Lobosea: Hartmannellidae), a new lobose amoeba, parasitized by the novel chlamydia ‘Candidatus Metachlamydia lacustris’ (Chlamydiae: Parachlamydiaceae). Eur. J. Protistol. 46: 86–95

Corsaro D., Müller K.-D., Wingender J., Michel R. (2013) ‘Candidatus Mesochlamydia elodea’ (Chlamydiae: Parachlamydiaceae), a novel Chlamydia parasite of free-living amoebae. Parasitol. Res. 112: 829–838

Darling K. F., Kucera M., Pudsey C. J., Wade C. M. (2004) Molecular evidence links cryptic diversification in polar planktonic protists to Quaternary climate dynamics. PNAS 101: 7657–7662

Darling K. F., Wade C. M. (2008) The genetic diversity of planktic foraminifera and the global distribution of ribosomal RNA genotypes. Mar. Micropaleontol. 67: 216–238

Deng L., Hayes P. (2008) Evidence for cyanophages active against bloom-forming freshwater cyanobacteria. Freshw. Biol. 53: 1240–1252

de Queiroz K. (2007) Species concepts and species delimitation. Systematic Biol. 56: 879–886

Douglas T. E., Kronforst M. R., Queller D. C., Strassmann J. E. (2011) Genetic diversity in the social amoeba Dictyostelium discoideum: population differentiation and cryptic species. Mol. Phylogenet. Evol. 60: 455–462

Dyková I., Kostka M., Pecková H. (2011) Three new species of the Amoebozoan genus Vexillifera Schaeffer, 1926. Acta Protozool. 50: 55–63

Finlay B. J., Esteban G. F. (1998) Freshwater protozoa: biodiversity and ecological function. Biodivers. Conserv. 7: 1163–1186

Foissner W., Stoeck T., Agatha S., Dunthorn M. (2011) Intraclass evolution and classification of the Colpodea (Ciliophora). J. Eukaryot. Microbiol. 58: 397–415

Garstecki T., Arndt H. (2000) Seasonal abundances and community structure of benthic rhizopods in shallow lagoons of the southern Baltic Sea. Eur. J. Protistol. 36: 103–115

Geisen S., Kudryavtsev A., Bonkowski M., Smirnov A. (2014) Discrepancy between species borders at morphological and molecular levels in the genus Cochliopodium (Amoebozoa, Himatismenida), with the description of Cochliopodium plurinucleolum n. sp. Protist 165: 364–383

Guillard R. R. L., Lorenzen C. L. (1972) Yellow-green algae with chlorophyllide C. J. Phycol. 8: 10–14

Hall T. A. (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl. Acid. S. 41: 95–98

Heger T. J., Mitchell E. A. D., Leander B. S. (2013) Holarctic phylogeography of the testate amoeba Hyalosphenia papilio (Amoebozoa: Arcellinida) reveals extensive genetic diversity explained more by environment than dispersal limitation. Mol. Ecol. 22: 5172–5184

Hebert P. D. N., Cywinska A., Ball S. L., deWaard J. R. (2003) Biological identifications through DNA barcodes. Proc. R. Soc. Lond. B Biol. Sci. 270: 313–321

Hindák F., Hindáková A. (1995) Chlorangiopsis flos-aquae (Tetrasporales, Chlorophyceae), a new species colonizing cyanophycean water blooms. Biologia 50: 309–313

Honjo M., Matsui K., Ueki M., Nakamura R., Fuhrman J. A., Kawabata Z. (2006) Diversity of virus-like agents killing Microcystis aeruginosa in a hyper-eutrophic pond. J. Plankton Res. 28: 407–412

Huelsenbeck J. P., Ronquist F. (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17: 754–755

Huss V. A. R., Frank C., Hartmann E. C., Hirmer M., Kloboucek A., Seidel B. M., Wenzeler P., Kessler E. (1999) Biochemical taxonomy and molecular phylogeny of the genus Chlorella sensu lato (Chlorophyta). J. Phycol. 35: 587–598

Janse I., Meima M., Kardinaal W. E. A., Zwart G. (2003) High-resolution differentiation of Cyanobacteria by using rRNA-Internal Transcribed Spacer Denaturing Gradient Gel Electrophoresis. Appl. Environ. Microb. 69: 6634–6643

Jumpponen A., Jones K. L., Mattox J. D., Yaege C. (2010) Massively parallel 454-sequencing of fungal communities in Quercus spp. ectomycorrhizas indicates seasonal dynamics in urban and rural sites. Mol. Ecol. 19 (S1): 41–53

Kermarrec L., Bouchez A., Rimet F., Humbert J.-F. (2013) First evidence of the existence of semi-cryptic species and of a phylogeographic structure in the Gomphonema parvulum (Kützing) Kützing complex (Bacillariophyta), Protist 164: 686–705

Kudryavtsev A. (2005) Redescription of Cochliopodium vestitum (Archer, 1871), a freshwater spine-bearing Cochliopodium. Acta Protozool. 44: 123–128

Kudryavtsev A. (2006) ‘Minute’ species of Cochliopodium (Himatismenida): Description of three new fresh- and brackish-water species with a new diagnosis for Cochliopodium minus Page, 1976. Eur. J. Protistol. 42: 77–89

Kudryavtsev A., Pawlowski J. (2015) Cunea n. g. (Amoebozoa, Dactylopodida) with two cryptic species isolated from different areas of the ocean. Eur. J. Protistol. 51: 197–209

Kumar S., Tamura K., Nei M. (1994) MEGA: Molecular Evolutionary Genetics Analysis software for microcomputers. Comput. Appl. Biosci. 10: 189–191

Lambrecht E., Baré J., Claeys M., Chavatte N., Bert W., Sabbe K., Houf K. (2015) Transmission electron microscopy sample preparation protocols for ultrastructural study of cysts of free-living protozoa. Biotechniques 58: 181–188

Laybourn-Parry J., Jones K., Holdich J. P. (1987) Grazing by Mayorella sp. (Protozoa: Sarcodina) on Cyanobacteria. Funct. Ecol. 1: 99–104

Leliaert F., Verbruggen H., Vanormelingen P., Steen F., López-Bautista J. M., Zuccarello G. C., De Clerck O. (2014) DNA-based species delimitation in algae. Eur. J. Phycol. 49: 179–196

Li N., Zhang L., Li F., Wang Y., Zhu Y., Kang H., Wang S., Qin S. (2011) Metagenome of microorganisms associated with the toxic Cyanobacteria Microcystis aeruginosa analyzed using the 454 sequencing platform. Chin. J. Oceanol. Limn. 29: 505–513

Manage P. M. (2009) Seasonal changes in the abundance of biological agents killing Microcystis aeruginosa in a hypereutrophic pond. Vidyodaya J. of Sci. 14: 85–101

Mann D. G., Sato S., Trobajo R., Vanormelingen P., Souffreau C. (2010) DNA barcoding for species identification and discovery in diatoms.Cryptogamie Algol. 31: 557–577

Maruyama T., Kato K., Yokoyama A., Tanaka T., Hiraishi A., Park H. D. (2003) Dynamics of microcystin-degrading bacteria in mucilage of Microcystis. Microb. Ecol. 46: 279–288

Medinger R., Nolte V., Pandey R. V., Jost S., Ottenwälder B., Schlötterer C., Boenigk J. (2010) Diversity in a hidden world: potential and limitation of next-generation sequencing for surveys of molecular diversity of eukaryotic microorganisms. Mol. Ecol. 19 (S1): 32–40

Mizuta S., Imai H., Chang K.-H., Doi H., Nishibe Y., Nakano S.-I.
(2011) Grazing on Microcystis (Cyanophyceae) by testate amoebae with special reference to cyanobacterial abundance and physiological state. Limnology 12: 205–211

Nassonova E., Smirnov A., Fahrni J., Pawlowski J. (2010) Barcoding amoebae: comparison of SSU, ITS and COI genes as tools for molecular identification of naked lobose amoebae. Protist 161: 102–115

Nishibe Y., Manage P. M., Kawabata Z., Nakano S. (2004) Trophic coupling of a testate amoeba and Microcystis species in a hypertrophic pond. Limnology 5: 71–76

O’Kelly C. J., Peglar M. T., Black M. N. D., Sawyer T. K., Nerad T. A.
(2001) Korotnovella hemistylolepis n. sp. and Korotnevella monacantholepis n. sp. (Paramoebidae), two new scale-covered mesohaline amoebae. J. Eukaryot. Microbiol. 48: 655–662

Özen A., Šorf M., Trochine C., Liboriussen L., Beklioglu M., Søndergaard M., Lauridsen T. L., Johansson L. S., Jeppesen E. (2013) Long-term effects of warming and nutrients on microbes and other plankton in mesocosms. Freshwater Biol. 58: 483–493

Page F. C. (1980) A light- and electron-microscopical comparison of limax and flabellate marine amoebae belonging to four genera. Protistologica 16: 57–78

Page F. C. (1981) Mayorella Schaeffer, 1926, and Hollandella n.g. (Gymnamoebia), distinguished by surface structure and other characters, with comparisons of three species. Protistologica 17: 543–562

Page F. C. (1988) A New Key to Freshwater and Soil Gymnamoebae. Freshwater Biol. Ass., Ambleside

Pankow H. (1986) About endophytic and epiphytic algae in or on the mucilage envelope of Microcystis colonies. Arch. Protistenkd.
132: 377–380

Pawlowski J., Burki F. (2009) Untangling the phylogeny of amoeboid protists. J. Eukaryot. Microbiol. 56: 16–25

Pawlowski J., Audic S., Adl S., Bass D., Belbahri L., et al. (2012) CBOL Protist Working Group: barcoding eukaryotic richness beyond the Animal, Plant, and Fungal Kingdoms. PLoS Biol. 10:
e1001419. doi:10.1371/journal.pbio.1001419

Penard E. (1902) Faune Rhizopodique du Bassin du Leman. Henry Kündig, Geneva

Piganeau G., Eyre-Walker A., Grimsley N., Moreau H. (2011) How and why DNA barcodes underestimate the diversity of microbial eukaryotes. PLoS ONE 6: e16342. doi:10.1371/journal.pone.0016342

Raper K. B., Worley A. C., Kurzynski T. A. (1978) Copromyxella: a new genus of Acrasidae. Amer. J. Bot. 65: 1011–1026

Reid N. M., Carstens B. C. (2012) Phylogenetic estimation error can decrease the accuracy of species delimitation: a Bayesian implementation of the general mixed Yule-coalescent model. BMC Evol. Biol. 12: 196

Rodríguez-Zaragoza S. (1994) Ecology of free-living amoebae. Crit. Rev. Microbiol. 20: 225–241

Rogerson A., Gwaltney C. (2000) High numbers of naked amoebae in the planktonic waters of a mangrove stand in Southern Florida, USA. J. Eukaryot. Microbiol. 47: 235–241

Rogerson A., Anderson O. R., Vogel C. (2003) Are planktonic naked amoebae predominately floc associated or free in the water column? J. Plankton Res. 25: 1359–1365

Ronquist F., Teslenko M., van der Mark P., Ayres D. L., Darling A., Hohna S., Larget B., Liu L., Suchard M. A., Huelsenbeck J. P. (2012) MrBayes 3.2: Efficient Bayesian phylogenetic inference and model choice across a large model space. Syst. Biol.61: 539–542

Savolainen V., Cowan R. S., Vogler A. P., Roderick G. K., Lane R. (2005) Towards writing the encyclopaedia of life: an introduction to DNA barcoding. Phil. Trans. R. Soc. B 360: 1805–1811

Schouteden H. (1905a) Notes sur quelques Amibes et Choanoflagellates. Arch. Protistk. 5: 322–338

Schouteden H. (1905b) Notes sur les Organismes Inférieurs. Ann. Soc. Roy. Zoöl. Malacol. de Belgique 40: 4–16

Sen B. (1988) Fungal parasitism of planktonic algae in Shearwater UK IV. Parasitic occurrence of a new chytrid species on the blue-green algae Microcystis aeruginosa Kuetz. emend. Elenkin. Archiv fuer Hydrobiologie Suppl. 3: 177–184

Shadwick L. L., Spiegel F. W., Shadwick J. D. L., Brown M. W., Silberman J. D. (2009) Eumycetozoa =Amoebozoa?: SSUrDNA phylogeny of protosteloid slime molds and its significance for the Amoebozoan supergroup. PLoS ONE 4: e6754. doi:10.1371/journal.pone.0006754

Sheridan C. C., Steinberg D. K, Kling G. W. (2002) The microbial and metazoan community associated with colonies of Trichodesmium spp.: a quantitative survey. J. Plankton Res. 24: 913–922

Shi L. M., Cai Y. F., Yang H. L., Xing P., Li P. F., Kong L. D., Kong F. X. (2009) Phylogenetic diversity and specificity of bacteria associated with Microcystis aeruginosa and other cyanobacteria. J. Environ. Sci.-China 21: 1581–1590

Shi L., Cai Y., Kong F., Yu Y. (2012) Specific association between bacteria and buoyant Microcystis colonies compared with other bulk bacterial communities in the eutrophic Lake Taihu, China. Environ. Microbiol. Reports 4: 669–678

Sims G. P., Aitken R., Rogerson A. (2002) Identification and phylogenetic analysis of morphologically similar naked amoebae using small subunit ribosomal RNA. J. Eukaryot. Microbiol. 49: 478–484

Smirnov A. V. (1996/97) Two new species of marine amoebae: Hartmannella lobifera n. sp. and Korotnevella nivo n. sp. (Lobosea, Gymnamoebida). Arch. Protistenkd. 147: 283–292

Smirnov A. V. (1999)Korotnevella diskophora n. sp. (Gymnamoebia, Paramoebidae) – small freshwater amoeba with peculiar scales. Protistology 1: 30–33

Smirnov A.V., Goodkov A.V (1999) An illustrated list of basic morphotypes of Gymnamoebia (Rhizopoda, Lobosea). Protistology 1: 20–29

Smirnov A. V., Nassonova E., Holzmann M., Pawlowski J. (2002) Morphological, ecological and molecular studies of Vannella simplex Wohlfarth-Bottermann 1960 (Lobosea, Gymnamoebia), with a new diagnosis of this species. Protist 153: 367–377

Smirnov A. V., Brown S. (2004) Guide to the methods of study and identification of soil gymnamoebae. Protistology 3: 148–190

Smirnov A., Nassonova E., Berney C., Fahrni J., Bolivar I., Pawlowski J. (2005) Molecular phylogeny and classification of the lobose amoebae. Protist 156: 129–142

Smirnov A. V., Nassonova E. S., Chao E., Cavalier-Smith T. (2007) Phylogeny, evolution and taxonomy of vannellid amoebae. Protist 158: 295–324

Smirnov A., Nassonova E., Fahrni J., Pawlowski J. (2009) Rhizamoeba neglecta n. sp. (Amoebozoa,Tubulinea) from the bottom sediments of freshwater Lake Leshevoe (Valamo Island, North-Western Russia), with notes on the phylogeny of the order Leptomyxida. Eur. J. Protistol. 45: 251–259

Smirnov A. V., Chao E., Nassonova E. S., Cavalier-Smith T.(2011) A revised classification of naked lobose amoebae (Amoebozoa: Lobosa). Protist 162: 545–570

Spurr A. R. (1969) A low-viscosity epoxy resin embedding medium for electron microscopy. J. Ultrastruct. Res. 26: 31–43

Tamura K., Stecher G., Peterson D., Filipski A., Kumar S. (2013) MEGA6: Molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol. 30: 2725–2729

Tekle Y. I., Anderson O. R., Lecky A. F., Kelly S. D. (2013) A new freshwater amoeba: Cochliopodium pentatrifurcatum n. sp. (Amoebozoa, Amorphea). J. Eukaryot. Microbiol. 60: 342–349

Tekle Y. I. (2014) DNA barcoding in Amoebozoa and challenges: the example of Cochliopodium. Protist 165: 473–484

Tekle Y. I., Anderson O. R., Lecky A. F. (2014) Evidence of parasexual activity in “asexual amoebae” Cochliopodium spp. (Amoebozoa): extensive cellular and nuclear fusion. Protist 165: 676–687

Udalov I. A. (2015) Cyst-forming amoebae of the genus Korotnevella Goodkov, 1988 (Amoebozoa: Dactylopodida), with description of two new species. Eur. J. Protistol. 51: 480–493

van Hannen E. J., van Agterveld M. P., Gons H. J., Laanbroek H. J. (1998) Revealing genetic diversity of eukaryotic microorganisms in aquatic environments by denaturing gradient gel electrophoresis. J. Phycol. 34: 206–213

Van Oye P. (1956) Overzicht van onze kennis der rhizopodenfauna van België. Biologisch Jaarboek Dodonaea 23: 283–289

Van Wichelen J., Muylaert K., Van Der Gucht K., Vyverman W. (2006) Observations on little studied protists (chytrids and an amoeba), affecting phytoplankton populations in the upper reaches of the Schelde Estuary (Belgium). Belg. J. Bot. 139: 153–166

Van Wichelen J., van Gremberghe I., Vanormelingen P., Debeer A.-E.,
Leporcq B., Menzel D., Codd G. A., Descy J.-P., Vyverman W. (2010) Strong effects of amoebae grazing on the biomass and genetic structure of a Microcystis bloom (Cyanobacteria). Environ. Microbiol. 12: 2797–2813

Van Wichelen J., van Gremberghe I., Vanormelingen P., Vyverman W. (2012) The importance of morphological versus chemical defences for the bloom-forming cyanobacteriumMicrocystis against amoebae grazing. Aquat. Ecol. 46: 73–84

Velho L. F. M., Lansac-Toha F. A., Bini L. M. (2003) Influence of environmental heterogeneity on the structure of testate amoebae (Protozoa, Rhizopoda) assemblages in the plankton of the upper Paraná river floodplain. Brazil. Internat. Rev. Hydrobiol. 88: 154–166

Visser P. M., Ibelings B. W., Mur L. R., Walsby A. E. (2005) The eco-physiology of the harmful cyanobacterium Microcystis: features explaining its success and measures for its control. In: Harmful cyanobacteria, (Eds. J. Huisman, H. C. P. Matthijs, P. M. Visser). Springer, Berlin, 109–142

Watson P., Sorrell S. C., Brown M. W. (2014) Ptolemeba n. gen., a novel genus of hartmannellid amoebae (Tubulinea, Amoebozoa); with emphasis on the taxonomy of Saccamoeba. J. Eukaryot. Microbiol. 61: 611–619

Whitton B. A. (1973) Interactions with other organisms. In: The biology of blue-green algae, (Eds. N. G. Carr, B. G. Whitton). Botanical Monographs 9, Blackwell Scientific Publications, Oxford, UK., 415–433

Wright S. J. L., Redhead K., Maudsley H. (1981) Acanthamoeba-castellanii, a predator of cyanobacteria. J. Gen. Microbiol. 125: 293–300

Worm J., Søndergaard M. (1998) Dynamics of heterotrophic bacteria attached to Microcystis spp. (Cyanobacteria). Aquat. Microb. Ecol. 14: 19–28

Xu D., Sun P., Shin M. K., Kim Y. O. (2012) Species boundaries in tintinnid ciliates: a case study – morphometric variability, molecular characterization, and temporal distribution of Helicostomella species (Ciliophora, Tintinnina). J. Eukaryot. Microbiol. 59: 351–358

Yamamoto Y. (1981) Observation on the occurrence of microbial agents which cause lysis of blue-green algae in Lake Kasumigaura. Jap. J. Limnol. 42: 20–27

Yamamoto Y., Suzuki K. (1984) Light and electron microscope observations and prey specificities of an algophorous amoeba from Japanese freshwater. J. Gen. Appl. Microbiol. 30: 411–417

Zhang X., Hu H. Y., Hong Y., Yang J. (2008) Isolation of a Poterioochromonas capable of feeding on Microcystis aeruginosa and degrading microcystin-LR. FEMS Microbiol. Lett. 288: 241–246

Zwart G., Huismans R., Van Agterveld M. P., Van de Peer Y., De Rijk P., Eenhoorn H., Muyzer G., Van Hannen E. J., Gons H. J., Laanbroek H. J. (1998) Divergent members of the bacterial division Verrucomicrobiales in a temperate freshwater lake. FEMS Microbiol. Ecol. 25: 159–169

Czasopismo w darmowym dostępie.

Czasopismo ukazuje się w sposób ciągły on-line.
Pierwotną formą czasopisma jest wersja elektroniczna.