High-resolution metagenomic reconstruction of the freshwater spring bloom
Jazyk angličtina Země Velká Británie, Anglie Médium electronic
Typ dokumentu audiovizuální média, časopisecké články, práce podpořená grantem
PubMed
36698172
PubMed Central
PMC9878933
DOI
10.1186/s40168-022-01451-4
PII: 10.1186/s40168-022-01451-4
Knihovny.cz E-zdroje
- MeSH
- Bacteria MeSH
- Eukaryota genetika MeSH
- metagenom * MeSH
- plankton MeSH
- sladká voda MeSH
- viry * genetika MeSH
- voda MeSH
- Publikační typ
- audiovizuální média MeSH
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- voda MeSH
BACKGROUND: The phytoplankton spring bloom in freshwater habitats is a complex, recurring, and dynamic ecological spectacle that unfolds at multiple biological scales. Although enormous taxonomic shifts in microbial assemblages during and after the bloom have been reported, genomic information on the microbial community of the spring bloom remains scarce. RESULTS: We performed a high-resolution spatio-temporal sampling of the spring bloom in a freshwater reservoir and describe a multitude of previously unknown taxa using metagenome-assembled genomes of eukaryotes, prokaryotes, and viruses in combination with a broad array of methodologies. The recovered genomes reveal multiple distributional dynamics for several bacterial groups with progressively increasing stratification. Analyses of abundances of metagenome-assembled genomes in concert with CARD-FISH revealed remarkably similar in situ doubling time estimates for dominant genome-streamlined microbial lineages. Discordance between quantitations of cryptophytes arising from sequence data and microscopic identification suggested the presence of hidden, yet extremely abundant aplastidic cryptophytes that were confirmed by CARD-FISH analyses. Aplastidic cryptophytes are prevalent throughout the water column but have never been considered in prior models of plankton dynamics. We also recovered the first metagenomic-assembled genomes of freshwater protists (a diatom and a haptophyte) along with thousands of giant viral genomic contigs, some of which appeared similar to viruses infecting haptophytes but owing to lack of known representatives, most remained without any indication of their hosts. The contrasting distribution of giant viruses that are present in the entire water column to that of parasitic perkinsids residing largely in deeper waters allows us to propose giant viruses as the biological agents of top-down control and bloom collapse, likely in combination with bottom-up factors like a nutrient limitation. CONCLUSION: We reconstructed thousands of genomes of microbes and viruses from a freshwater spring bloom and show that such large-scale genome recovery allows tracking of planktonic succession in great detail. However, integration of metagenomic information with other methodologies (e.g., microscopy, CARD-FISH) remains critical to reveal diverse phenomena (e.g., distributional patterns, in situ doubling times) and novel participants (e.g., aplastidic cryptophytes) and to further refine existing ecological models (e.g., factors affecting bloom collapse). This work provides a genomic foundation for future approaches towards a fine-scale characterization of the organisms in relation to the rapidly changing environment during the course of the freshwater spring bloom. Video Abstract.
Faculty of Science University of South Bohemia Branišovská 31 370 05 České Budějovice Czech Republic
Institute of Hydrobiology Biology Centre CAS Na Sádkách 7 370 05 České Budějovice Czech Republic
Limnological Station Microbial Evogenomics Lab University of Zurich Kilchberg Switzerland
Zobrazit více v PubMed
Sommer U, Gliwicz ZM, Lampert W, Duncan A. The PEG-model of seasonal succession of planktonic events in fresh waters. Arch Hydrobiol. 1986;106:433–471. doi: 10.1127/archiv-hydrobiol/106/1986/433. DOI
Sommer U, Adrian R, De Senerpont Domis L, Elser JJ, Gaedke U, Ibelings B, et al. Beyond the Plankton Ecology Group (PEG) model: mechanisms driving plankton succession. Annu Rev Ecol Evol Syst. 2012;43:429–48. doi: 10.1146/annurev-ecolsys-110411-160251. DOI
Šimek K, Nedoma J, Znachor P, Kasalický V, Jezbera J, Hornňák K, et al. A finely tuned symphony of factors modulates the microbial food web of a freshwater reservoir in spring. Limnol Oceanogr. 2014;59:1477–92. doi: 10.4319/lo.2014.59.5.1477. DOI
Zeder M, Peter S, Shabarova T, Pernthaler J. A small population of planktonic Flavobacteria with disproportionally high growth during the spring phytoplankton bloom in a prealpine lake. Environ Microbiol. 2009;11:2676–2686. doi: 10.1111/j.1462-2920.2009.01994.x. PubMed DOI
Eckert EM, Salcher MM, Posch T, Eugster B, Pernthaler J. Rapid successions affect microbial N-acetyl-glucosamine uptake patterns during a lacustrine spring phytoplankton bloom. Environ Microbiol Wiley. 2012;14:794–806. doi: 10.1111/j.1462-2920.2011.02639.x. PubMed DOI
Šimek K, Nedoma J, Znachor P, Kasalický V, Jezbera J, Hornňák K, et al. A finely tuned symphony of factors modulates the microbial food web of a freshwater reservoir in spring. Limnol Oceanogr. 2014;59:1477–1492. doi: 10.4319/lo.2014.59.5.1477. DOI
Tirok K, Gaedke U. Spring weather determines the relative importance of ciliates, rotifers and crustaceans for the initiation of the clear-water phase in a large, deep lake. J Plankton Res Oxford Academic. 2006;28:361–373. doi: 10.1093/plankt/fbi121. DOI
Frenken T, Velthuis M, de Senerpont Domis LN, Stephan S, Aben R, Kosten S, et al. Warming accelerates termination of a phytoplankton spring bloom by fungal parasites. Glob Chang Biol. 2016;22:299–309. doi: 10.1111/gcb.13095. PubMed DOI
Pradeep Ram AS, Mauduit M-E, Colombet J, Perriere F, Thouvenot A, Sime-Ngando T. Top-down controls of bacterial metabolism: a case study from a temperate freshwater lake ecosystem. Microorganisms. 2022;10. 10.3390/microorganisms10040715. PubMed PMC
Huppert A, Blasius B, Stone L. A model of phytoplankton blooms. Am Nat. 2002;159:156–171. doi: 10.1086/324789. PubMed DOI
Moreira D, López-García P. Time series are critical to understand microbial plankton diversity and ecology. Mol Ecol. 2019;28:920–922. doi: 10.1111/mec.15015. PubMed DOI PMC
Linz AM, Crary BC, Shade A, Owens S, Gilbert JA, Knight R, et al. Bacterial community composition and dynamics spanning five years in freshwater bog lakes. mSphere. 2017;2. 10.1128/mSphere.00169-17. PubMed PMC
Tromas N, Fortin N, Bedrani L, Terrat Y, Cardoso P, Bird D, et al. Characterising and predicting cyanobacterial blooms in an 8-year amplicon sequencing time course. ISME J. 2017;11:1746–1763. doi: 10.1038/ismej.2017.58. PubMed DOI PMC
Eiler A, Heinrich F, Bertilsson S. Coherent dynamics and association networks among lake bacterioplankton taxa. ISME J. nature.com. 2012;6:330–42. doi: 10.1038/ismej.2011.113. PubMed DOI PMC
Mangot J-F, Domaizon I, Taib N, Marouni N, Duffaud E, Bronner G, et al. Short-term dynamics of diversity patterns: evidence of continual reassembly within lacustrine small eukaryotes. Environ Microbiol. 2013;15:1745–1758. doi: 10.1111/1462-2920.12065. PubMed DOI
Salcher MM, Pernthaler J, Posch T. Seasonal bloom dynamics and ecophysiology of the freshwater sister clade of SAR11 bacteria “that rule the waves”(LD12). ISME J. nature.com; 2011; Available from: https://www.nature.com/articles/ismej20118 PubMed PMC
Salcher MM, Neuenschwander SM, Posch T, Pernthaler J. The ecology of pelagic freshwater methylotrophs assessed by a high-resolution monitoring and isolation campaign. ISME J. 2015;9:2442–2453. doi: 10.1038/ismej.2015.55. PubMed DOI PMC
Neuenschwander SM, Pernthaler J, Posch T, Salcher MM. Seasonal growth potential of rare lake water bacteria suggest their disproportional contribution to carbon fluxes. Environ Microbiol. 2015;17:781–795. doi: 10.1111/1462-2920.12520. PubMed DOI
Linz AM, He S, Stevens SLR, Anantharaman K, Rohwer RR, Malmstrom RR, et al. Freshwater carbon and nutrient cycles revealed through reconstructed population genomes. PeerJ. 2018;6:e6075. doi: 10.7717/peerj.6075. PubMed DOI PMC
Kavagutti VS, Andrei A-Ş, Mehrshad M, Salcher MM, Ghai R. Phage-centric ecological interactions in aquatic ecosystems revealed through ultra-deep metagenomics. Microbiome. 2019;7:135. doi: 10.1186/s40168-019-0752-0. PubMed DOI PMC
Shabarova T, Salcher MM, Porcal P, Znachor P, Nedoma J, Grossart H-P, et al. Recovery of freshwater microbial communities after extreme rain events is mediated by cyclic succession. Nat Microbiol. 2021; 10.1038/s41564-020-00852-1. PubMed
Lopez-Garcia P, Reboul G, David G, Jardillier L, Annenkova N, Bertolino P, et al. Environmental drivers of plankton and sediment microbial communities along latitudinal and vertical gradients in the deepest freshwater lake (Baikal, Southern Siberia) 2021. pp. EGU21–8920. PubMed
Hamilton M, Hennon GMM, Morales R, Needoba J, Peterson TD, Schatz M, et al. Dynamics of Teleaulax-like cryptophytes during the decline of a red water bloom in the Columbia River Estuary. J Plankton Res Oxford Academic. 2017;39:589–599. doi: 10.1093/plankt/fbx029. DOI
Posch T, Eugster B, Pomati F, Pernthaler J, Pitsch G, Eckert EM. Network of interactions between ciliates and phytoplankton during spring. Front Microbiol. 2015;6:1289. doi: 10.3389/fmicb.2015.01289. PubMed DOI PMC
Pitsch G, Bruni EP, Forster D, Qu Z, Sonntag B, Stoeck T, et al. Seasonality of planktonic freshwater ciliates: are analyses based on V9 regions of the 18S rRNA gene correlated with morphospecies counts? Front Microbiol. 2019;10:248. doi: 10.3389/fmicb.2019.00248. PubMed DOI PMC
Eckert EM, Baumgartner M, Huber IM, Pernthaler J. Grazing resistant freshwater bacteria profit from chitin and cell-wall-derived organic carbon. Environ Microbiol Wiley. 2013;15:2019–2030. doi: 10.1111/1462-2920.12083. PubMed DOI
Teeling H, Fuchs BM, Becher D, Klockow C, Gardebrecht A, Bennke CM, et al. Substrate-controlled succession of marine bacterioplankton populations induced by a phytoplankton bloom. Science. science.sciencemag.org. 2012;336:608–11. PubMed
Francis TB, Bartosik D, Sura T, Sichert A, Hehemann J-H, Markert S, et al. Changing expression patterns of TonB-dependent transporters suggest shifts in polysaccharide consumption over the course of a spring phytoplankton bloom. ISME J. nature.com. 2021;15:2336–50. doi: 10.1038/s41396-021-00928-8. PubMed DOI PMC
Hahnke RL, Bennke CM, Fuchs BM, Mann AJ, Rhiel E, Teeling H, et al. Dilution cultivation of marine heterotrophic bacteria abundant after a spring phytoplankton bloom in the North Sea. Environ Microbiol Wiley. 2015;17:3515–3526. doi: 10.1111/1462-2920.12479. PubMed DOI
Alejandre-Colomo C, Harder J, Fuchs BM, Rosselló-Móra R, Amann R. High-throughput cultivation of heterotrophic bacteria during a spring phytoplankton bloom in the North Sea. Syst Appl Microbiol. 2020;43:126066. doi: 10.1016/j.syapm.2020.126066. PubMed DOI
Piwosz K, Mukherjee I, Salcher MM, Grujčić V, Šimek K. CARD-FISH in the sequencing Era: opening a new universe of protistan ecology. Front Microbiol. 2021;12:640066. doi: 10.3389/fmicb.2021.640066. PubMed DOI PMC
Neuenschwander SM, Ghai R, Pernthaler J, Salcher MM. Microdiversification in genome-streamlined ubiquitous freshwater Actinobacteria. ISME J. 2018;12:185–198. doi: 10.1038/ismej.2017.156. PubMed DOI PMC
Salcher MM, Schaefle D, Kaspar M, Neuenschwander SM, Ghai R. Evolution in action: habitat transition from sediment to the pelagial leads to genome streamlining in Methylophilaceae. ISME J. 2019;13:2764–2777. doi: 10.1038/s41396-019-0471-3. PubMed DOI PMC
Šimek K, Mukherjee I, Szöke-Nagy T, Haber M, Salcher MM, Ghai R. Cryptic and ubiquitous aplastidic cryptophytes are key freshwater flagellated bacterivores. ISME J. 2022; 10.1038/s41396-022-01326-4. PubMed PMC
Raven JA, Wollenweber B, Handley LL. A comparison of ammonium and nitrate as nitrogen sources for photolithotrophs. New Phytol Wiley. 1992;121:19–32. doi: 10.1111/j.1469-8137.1992.tb01088.x. DOI
Glibert PM. Interactions of top-down and bottom-up control in planktonic nitrogen cycling. In: Tamminen T, Kuosa H, editors. Eutrophication in Planktonic Ecosystems: Food Web Dynamics and Elemental Cycling: Proceedings of the Fourth International PELAG Symposium, held in Helsinki, Finland, 26–30 August 1996. Dordrecht: Springer Netherlands; 1998. pp. 1–12.
Saba GK, Steinberg DK, Bronk DA. The relative importance of sloppy feeding, excretion, and fecal pellet leaching in the release of dissolved carbon and nitrogen by Acartia tonsa copepods. J Exp Mar Bio Ecol. 2011;404:47–56. doi: 10.1016/j.jembe.2011.04.013. DOI
Valdés VP, Fernandez C, Molina V, Escribano R, Joux F. Dissolved compounds excreted by copepods reshape the active marine bacterioplankton community composition. Front Mar Sci. 2017. 10.3389/fmars.2017.00343.
Müller H, Schöne A, Pinto-Coelho RM, Schweizer A, Weisse T. Seasonal succession of ciliates in lake constance. Microb Ecol. 1991;21:119–138. doi: 10.1007/BF02539148. PubMed DOI
Simek K, Jürgens K, Nedoma J, Comerma M, Armengol J. Ecological role and bacterial grazing of Halteria spp.: small freshwater oligotrichs as dominant pelagic ciliate bacterivores. Aquat Microb Ecol. Inter-Research Science Center. 2000;22:43–56. doi: 10.3354/ame022043. DOI
Salcher MM, Pernthaler J, Posch T. Spatiotemporal distribution and activity patterns of bacteria from three phylogenetic groups in an oligomesotrophic lake. Limnol Oceanogr. 2010;55:846–856. doi: 10.4319/lo.2010.55.2.0846. DOI
Newton RJ, Jones SE, Eiler A, McMahon KD, Bertilsson S. A guide to the natural history of freshwater lake bacteria. Microbiol Mol Biol Rev. 2011;75:14–49. doi: 10.1128/MMBR.00028-10. PubMed DOI PMC
Ghai R, McMahon KD, Rodriguez-Valera F. Breaking a paradigm: cosmopolitan and abundant freshwater actinobacteria are low GC. Environ Microbiol Rep. 2012;4:29–35. doi: 10.1111/j.1758-2229.2011.00274.x. PubMed DOI
Andrei A-Ş, Salcher MM, Mehrshad M, Rychtecký P, Znachor P, Ghai R. Niche-directed evolution modulates genome architecture in freshwater Planctomycetes. ISME J. 2019;13:1056–1071. doi: 10.1038/s41396-018-0332-5. PubMed DOI PMC
Moss JA, Xiao J, Dungan CF, Reece KS. Description of Perkinsus beihaiensis n. sp., a new Perkinsus sp. parasite in oysters of Southern China. J Eukaryot Microbiol. 2008;55:117–30. doi: 10.1111/j.1550-7408.2008.00314.x. PubMed DOI
Jeon BS, Park MG. Tuberlatum coatsi gen. n., sp. n. (Alveolata, Perkinsozoa), a new parasitoid with short germ tubes infecting marine dinoflagellates. Protist. 2019:82–103. 10.1016/j.protis.2018.12.003 PubMed
Jobard M, Wawrzyniak I, Bronner G, Marie D, Vellet A, Sime-Ngando T, et al. Freshwater Perkinsea: diversity, ecology and genomic information. J Plankton Res Oxford Academic. 2019;42:3–17. doi: 10.1093/plankt/fbz068. DOI
Karlsbakk E, Nystøyl CF, Plarre H, Nylund A. A novel protist parasite, Salmoxcellia vastator n. gen., n. sp. (Xcelliidae, Perkinsozoa), infecting farmed salmonids in Norway. Parasit Vectors. 2021;14:431. doi: 10.1186/s13071-021-04886-0. PubMed DOI PMC
Mangot J-F, Debroas D, Domaizon I. Perkinsozoa, a well-known marine protozoan flagellate parasite group, newly identified in lacustrine systems: a review. Hydrobiologia. 2011;659:37–48. doi: 10.1007/s10750-010-0268-x. DOI
Lepère C, Domaizon I, Debroas D. Unexpected importance of potential parasites in the composition of the freshwater small-eukaryote community. Appl Environ Microbiol. American Society for Microbiology. 2008;74:2940–9. doi: 10.1128/AEM.01156-07. PubMed DOI PMC
Mukherjee I, Hodoki Y, Nakano S. Seasonal dynamics of heterotrophic and plastidic protists in the water column of Lake Biwa, Japan. Aquat Microb Ecol. int-res.com; 2017; Available from: https://www.int-res.com/abstracts/ame/v80/n2/p123-137/
Lepère C, Masquelier S, Mangot JF, Debroas D, Domaizon I. Vertical structure of small eukaryotes in three lakes that differ by their trophic status: a quantitative approach. ISME J. 2010;4:1509–19. doi: 10.1038/ismej.2010.83. PubMed DOI
Brugerolle G. Cryptophagus subtilis: a new parasite of cryptophytes affiliated with the Perkinsozoa lineage. Eur J Protistol Elsevier. 2002;37:379–390. doi: 10.1078/0932-4739-00837. DOI
Vincent F, Sheyn U, Porat Z, Schatz D, Vardi A. Visualizing active viral infection reveals diverse cell fates in synchronized algal bloom demise. Proc Natl Acad Sci U S A. 2021;118. 10.1073/pnas.2021586118 PubMed PMC
Nagata T, Inoue K. Rhodopsins at a glance. J Cell Sci. 2021;134. 10.1242/jcs.258989 PubMed
Fuhrman JA, Schwalbach MS, Stingl U. Proteorhodopsins: an array of physiological roles? Nat Rev Microbiol. 2008;6:488–494. doi: 10.1038/nrmicro1893. PubMed DOI
Man D, Wang W, Sabehi G, Aravind L, Post AF, Massana R, et al. Diversification and spectral tuning in marine proteorhodopsins. EMBO J. 2003;22:1725–1731. doi: 10.1093/emboj/cdg183. PubMed DOI PMC
Ghai R, Mehrshad M, Mizuno CM, Rodriguez-Valera F. Metagenomic recovery of phage genomes of uncultured freshwater actinobacteria. ISME J. 2017;11:304–308. doi: 10.1038/ismej.2016.110. PubMed DOI PMC
Mendler K, Chen H, Parks DH, Lobb B, Hug LA, Doxey AC. AnnoTree: visualization and exploration of a functionally annotated microbial tree of life. Nucleic Acids Res Oxford Academic. 2019;47:4442–4448. doi: 10.1093/nar/gkz246. PubMed DOI PMC
Sawa N, Tatsuke T, Ogawa A, Hirokawa Y, Osanai T, Hanai T. Modification of carbon metabolism in Synechococcus elongatus PCC 7942 by cyanophage-derived sigma factors for bioproduction improvement. J Biosci Bioeng. 2019;127:256–264. doi: 10.1016/j.jbiosc.2018.07.019. PubMed DOI
Kasalický V, Jezbera J, Hahn MW, Šimek K. The diversity of the Limnohabitans genus, an important group of freshwater bacterioplankton, by characterization of 35 isolated strains. PLoS ONE. 2013;8:e58209. doi: 10.1371/journal.pone.0058209. PubMed DOI PMC
Jezberová J, Jezbera J, Znachor P, Nedoma J, Kasalický V, Šimek K. The limnohabitans genus harbors generalistic and opportunistic subtypes: evidence from spatiotemporal succession in a canyon-shaped reservoir. Appl Environ Microbiol . 2017;83. 10.1128/AEM.01530-17 PubMed PMC
Salcher MM, Pernthaler J, Posch T. Seasonal bloom dynamics and ecophysiology of the freshwater sister clade of SAR11 bacteria “that rule the waves” (LD12) ISME J Nature Publishing Group. 2011;5:1242–1252. PubMed PMC
Heinrich F, Eiler A, Bertilsson S. Seasonality and environmental control of freshwater SAR11 (LD12) in a temperate lake (Lake Erken, Sweden) Aquat Microb Ecol Inter-Research Science Center. 2013;70:33–44. doi: 10.3354/ame01637. DOI
Henson MW, Lanclos VC, Faircloth BC, Thrash JC. Cultivation and genomics of the first freshwater SAR11 (LD12) isolate. ISME J. 2018;12:1846–1860. doi: 10.1038/s41396-018-0092-2. PubMed DOI PMC
Kim S, Kang I, Lee J-W, Jeon CO, Giovannoni SJ, Cho J-C. Heme auxotrophy in abundant aquatic microbial lineages. Proc Natl Acad Sci U S A. 2021;118. 10.1073/pnas.2102750118 PubMed PMC
Kirchman DL. Growth rates of microbes in the oceans. Ann Rev Mar Sci. 2016;8:285–309. doi: 10.1146/annurev-marine-122414-033938. PubMed DOI
Ram ASP, Palesse S, Colombet J, Thouvenot A, Sime-Ngando T. The relative importance of viral lysis and nanoflagellate grazing for prokaryote mortality in temperate lakes. Freshw Biol Wiley. 2014;59:300–311. doi: 10.1111/fwb.12265. DOI
Weissman JL, Hou S, Fuhrman JA. Estimating maximal microbial growth rates from cultures, metagenomes, and single cells via codon usage patterns. Proc Natl Acad Sci U S A. National Academy of Sciences; 2021;118. Available from: https://www.pnas.org/content/118/12/e2016810118/tab-article-info. [Cited 2021 May 28]. PubMed PMC
Giovannoni SJ, Tripp HJ, Givan S, Podar M, Vergin KL, Baptista D, et al. Genome streamlining in a cosmopolitan oceanic bacterium. Science. 2005;309:1242–1245. doi: 10.1126/science.1114057. PubMed DOI
Delmont TO, Gaia M, Hinsinger DD, Frémont P, Vanni C, Fernandez-Guerra A, et al. Functional repertoire convergence of distantly related eukaryotic plankton lineages abundant in the sunlit ocean. Cell Genomics. 2022;2:100123. doi: 10.1016/j.xgen.2022.100123. PubMed DOI PMC
Dahl E, Bagøien E, Edvardsen B, Stenseth NC. The dynamics of Chrysochromulina species in the Skagerrak in relation to environmental conditions. J Sea Res. 2005;54:15–24. doi: 10.1016/j.seares.2005.02.004. DOI
Seoane S, Eikrem W, Pienaar R, Edvardsen B. Chrysochromulina palpebralis sp. nov. (Prymnesiophyceae): a haptophyte, possessing two alternative morphologies. Phycologia. 2009;48:165–76. doi: 10.2216/08-63.1. DOI
Søgaard DH, Sorrell BK, Sejr MK, Andersen P, Rysgaard S, Hansen PJ, et al. An under-ice bloom of mixotrophic haptophytes in low nutrient and freshwater-influenced Arctic waters. Sci Rep. 2021;11:2915. doi: 10.1038/s41598-021-82413-y. PubMed DOI PMC
Hansen PJ, Nielsen TG, Kaas H. Distribution and growth of protists and mesozooplankton during a bloom of Chrysochromulina spp. (Prymnesiophyceae, Prymnesiales). Phycologia. 1995:409–16. 10.2216/i0031-8884-34-5-409.1.
Liu H, Probert I, Uitz J, Claustre H, Aris-Brosou S, Frada M, et al. Extreme diversity in noncalcifying haptophytes explains a major pigment paradox in open oceans. Proc Natl Acad Sci U S A. 2009;106:12803–12808. doi: 10.1073/pnas.0905841106. PubMed DOI PMC
Nicholls KH, Beaver JL, Estabrook RH. Lakewide odours in Ontario and New Hampshire caused by Chrysochromulina breviturrita Nich. (Prymnesiophyceae). Hydrobiologia. 1982:91–5. 10.1007/bf00006281.
Kolmogorov M, Yuan J, Lin Y, Pevzner PA. Assembly of long, error-prone reads using repeat graphs. Nat Biotechnol. 2019;37:540–546. doi: 10.1038/s41587-019-0072-8. PubMed DOI
Hovde BT, Deodato CR, Hunsperger HM, Ryken SA, Yost W, Jha RK, et al. Genome sequence and transcriptome analyses of chrysochromulina tobin: metabolic tools for enhanced algal fitness in the prominent order prymnesiales (Haptophyceae) PLoS Genet. 2015;11:e1005469. doi: 10.1371/journal.pgen.1005469. PubMed DOI PMC
Hovde BT, Deodato CR, Andersen RA, Starkenburg SR, Barlow SB, Cattolico RA. Chrysochromulina: genomic assessment and taxonomic diagnosis of the type species for an oleaginous algal clade. Algal Research Elsevier. 2019;37:307–319. doi: 10.1016/j.algal.2018.11.023. DOI
Armbrust EV, Berges JA, Bowler C, Green BR, Martinez D, Putnam NH, et al. The genome of the diatom Thalassiosira pseudonana: ecology, evolution, and metabolism. Science. 2004;306:79–86. doi: 10.1126/science.1101156. PubMed DOI
Lommer M, Specht M, Roy A-S, Kraemer L, Andreson R, Gutowska MA, et al. Genome and low-iron response of an oceanic diatom adapted to chronic iron limitation. Genome Biol. 2012;13:R66. doi: 10.1186/gb-2012-13-7-r66. PubMed DOI PMC
Saros JE, Anderson NJ. The ecology of the planktonic diatom Cyclotella and its implications for global environmental change studies. Biol Rev Camb Philos Soc. 2015;90:522–541. doi: 10.1111/brv.12120. PubMed DOI
La Scola B, Audic S, Robert C, Jungang L, de Lamballerie X, Drancourt M, et al. A giant virus in amoebae. Science. 2003;299:2033. doi: 10.1126/science.1081867. PubMed DOI
Raoult D, Audic S, Robert C, Abergel C, Renesto P, Ogata H, et al. The 1.2-megabase genome sequence of Mimivirus. Science. 2004;306:1344–50. doi: 10.1126/science.1101485. PubMed DOI
Deeg CM, Chow C-ET, Suttle CA. The kinetoplastid-infecting Bodo saltans virus (BsV), a window into the most abundant giant viruses in the sea. Elife 2018;7.10.7554/eLife.33014 PubMed PMC
Fischer MG, Allen MJ, Wilson WH, Suttle CA. Giant virus with a remarkable complement of genes infects marine zooplankton. Proc Natl Acad Sci U S A. 2010;107:19508–19513. doi: 10.1073/pnas.1007615107. PubMed DOI PMC
Laber CP, Hunter JE, Carvalho F, Collins JR, Hunter EJ, Schieler BM, et al. Coccolithovirus facilitation of carbon export in the North Atlantic. Nat Microbiol. 2018;3:537–547. doi: 10.1038/s41564-018-0128-4. PubMed DOI
Moniruzzaman M, Weinheimer AR, Martinez-Gutierrez CA, Aylward FO. Widespread endogenization of giant viruses shapes genomes of green algae. Nature. 2020;588:141–145. doi: 10.1038/s41586-020-2924-2. PubMed DOI
Aylward FO, Moniruzzaman M, Ha AD, Koonin EV. A phylogenomic framework for charting the diversity and evolution of giant viruses. PLoS Biol. 2021;19:e3001430. doi: 10.1371/journal.pbio.3001430. PubMed DOI PMC
Schulz F, Roux S, Paez-Espino D, Jungbluth S, Walsh DA, Denef VJ, et al. Giant virus diversity and host interactions through global metagenomics. Nature Nature Publishing Group. 2020;578:432–436. PubMed PMC
Bratbak G, Egge JK, Heldal M. Viral mortality of the marine alga Emiliania huxleyi (Haptophyceae) and termination of algal blooms. Mar Ecol Prog Ser. 1993;93:39–48. doi: 10.3354/meps093039. DOI
Rosenwasser S, Ziv C, Van Creveld SG, Vardi A. Virocell metabolism: metabolic innovations during host–virus interactions in the ocean. Trends Microbiol. Elsevier; 2016; Available from: https://www.sciencedirect.com/science/article/pii/S0966842X16300695 PubMed
Nayfach S, Camargo AP, Schulz F, Eloe-Fadrosh E, Roux S, Kyrpides NC. CheckV assesses the quality and completeness of metagenome-assembled viral genomes. Nat Biotechnol. 2021;39:578–585. doi: 10.1038/s41587-020-00774-7. PubMed DOI PMC
Thingstad TF, Lignell R. Theoretical models for the control of bacterial growth rate, abundance, diversity and carbon demand. Aquat Microb Ecol Inter-Research. 1997;13:19–27. doi: 10.3354/ame013019. DOI
Wilhelm SW, Suttle CA. Viruses and nutrient cycles in the sea: viruses play critical roles in the structure and function of aquatic food webs. Bioscience. 1999;49:781–788. doi: 10.2307/1313569. DOI
Wilson WH, Tarran GA, Schroeder D, Cox M, Oke J, Malin G. Isolation of viruses responsible for the demise of an Emiliania huxleyi bloom in the English Channel. J Mar Biol Assoc U K. 2002;82:369–77. doi: 10.1017/S002531540200560X. DOI
Meshram AR, Vader A, Kristiansen S, Gabrielsen TM. Microbial eukaryotes in an arctic under-ice spring bloom north of Svalbard. Front Microbiol. 2017. 10.3389/fmicb.2017.01099 PubMed PMC
Kim JI, Yoon HS, Yi G, Shin W, Archibald JM. Comparative mitochondrial genomics of cryptophyte algae: gene shuffling and dynamic mobile genetic elements. BMC Genomics BioMed Central. 2018;19:1–14. PubMed PMC
Grujcic V, Nuy JK, Salcher MM, Shabarova T, Kasalicky V, Boenigk J, et al. Cryptophyta as major bacterivores in freshwater summer plankton. ISME J. 2018;12:1668–1681. doi: 10.1038/s41396-018-0057-5. PubMed DOI PMC
Šimek K, Mukherjee I, Nedoma J, de Paula CCP, Jezberová J, Sirová D, et al. CARD-FISH and prey tracer techniques reveal the role of overlooked flagellate groups as major bacterivores in freshwater hypertrophic shallow lakes. Environ Microbiol. Wiley; 2021; Available from: https://onlinelibrary.wiley.com/doi/10.1111/1462-2920.15846. PubMed DOI PMC
Piwosz K, Shabarova T, Pernthaler J, Posch T, Šimek K, Porcal P, et al. Bacterial and eukaryotic small-subunit amplicon data do not provide a quantitative picture of microbial communities, but they are reliable in the context of ecological interpretations. mSphere. 2020;5. 10.1128/mSphere.00052-20 PubMed PMC
Mukherjee I, Salcher MM, Andrei A-Ş, Kavagutti VS, Shabarova T, Grujčić V, et al. A freshwater radiation of diplonemids. Environ Microbiol Wiley. 2020;22:4658–4668. doi: 10.1111/1462-2920.15209. PubMed DOI
Cenci U, Sibbald SJ, Curtis BA, Kamikawa R, Eme L, Moog D, et al. Nuclear genome sequence of the plastid-lacking cryptomonad Goniomonas avonlea provides insights into the evolution of secondary plastids. BMC Biol. 2018;16:137. doi: 10.1186/s12915-018-0593-5. PubMed DOI PMC
Morris JJ. Black Queen evolution: the role of leakiness in structuring microbial communities. Trends Genet. 2015;31:475–482. doi: 10.1016/j.tig.2015.05.004. PubMed DOI
Znachor P, Nedoma J, Hejzlar J, Seďa J, Kopáček J, Boukal D, et al. Multiple long-term trends and trend reversals dominate environmental conditions in a man-made freshwater reservoir. Sci Total Environ. 2018;624:24–33. doi: 10.1016/j.scitotenv.2017.12.061. PubMed DOI
Znachor P, Hejzlar J, Vrba J, Nedoma J, Seda J, Simek K, et al. Brief history of long-term ecological research into aquatic ecosystems and their catchments in the Czech Republic. Part I: Manmade reservoirs. researchgate.net; 2016;1. Available from: https://www.researchgate.net/profile/Petr-Znachor/publication/311416951_Brief_history_of_long-term_ecological_research_into_aquatic_ecosystems_and_their_catchments_in_the_Czech_Republic_Part_I_Manmade_reservoirs/links/5853827808ae0c0f322282e6/Brief-history-of-long-term-ecological-research-into-aquatic-ecosystems-and-their-catchments-in-the-Czech-Republic-Part-I-Manmade-reservoirs.pdf
Beutler M, Wiltshire KH, Meyer B, Moldaenke C, Lüring C, Meyerhöfer M, et al. A fluorometric method for the differentiation of algal populations in vivo and in situ. Photosynth Res. 2002;72:39–53. doi: 10.1023/A:1016026607048. PubMed DOI
Mackereth F, Heron J, Talling J. Water analysis: some revised methods form limnologists. Kendal: Titus Wilson and Son Limited; 1989.
Murphy J, Riley JP. A modified single solution method for the determination of phosphate in natural waters. Anal Chim Acta Elsevier. 1962;27:31–36. doi: 10.1016/S0003-2670(00)88444-5. DOI
Kopáček J, Hejzlar J. Semi-micro determination of total phosphorus in fresh waters with perchloric acid digestion. Int J Environ Anal Chem. 1993;53:173–83. doi: 10.1080/03067319308045987. DOI
Procházková L. Bestimmung der Nitrate im Wasser. Fresenius’ Zeitschrift für Analytische Chemie. 1959;167:254–60. doi: 10.1007/BF00458786. DOI
Lund JWG, Kipling C, Le Cren ED. The inverted microscope method of estimating algal numbers and the statistical basis of estimations by counting. Hydrobiologia Springer Nature. 1958;11:143–170. doi: 10.1007/BF00007865. DOI
Hillebrand H, Dürselen C-D, Kirschtel D, Pollingher U, Zohary T. Biovolume calculation for pelagic and benthic microalgae. J Phycol Wiley. 1999;35:403–424. doi: 10.1046/j.1529-8817.1999.3520403.x. DOI
Posch T, Loferer-Krößbacher M, Gao G, Alfreider A, Pernthaler J, Psenner R. Precision of bacterioplankton biomass determination: a comparison of two fluorescent dyes, and of allometric and linear volume-to-carbon conversion factors. Aquat Microb Ecol. 2001;25:55–63. doi: 10.3354/ame025055. DOI
Sherr BF, Sherr EB, Fallon RD. Use of monodispersed, fluorescently labeled bacteria to estimate in situ protozoan bacterivory. Appl Environ Microbiol. 1987;53:958–965. doi: 10.1128/aem.53.5.958-965.1987. PubMed DOI PMC
Šimek K, Grujčić V, Nedoma J, Jezberová J, Šorf M, Matoušů A, et al. Microbial food webs in hypertrophic fishponds: Omnivorous ciliate taxa are major protistan bacterivores. Limnol Oceanogr Wiley. 2019;64:2295–2309. doi: 10.1002/lno.11260. DOI
Jezbera J, Hornák K, Simek K. Prey selectivity of bacterivorous protists in different size fractions of reservoir water amended with nutrients. Environ Microbiol Wiley Online Library. 2006;8:1330–1339. PubMed
Brussaard CPD. Optimization of procedures for counting viruses by flow cytometry. Appl Environ Microbiol. 2004;70:1506–1513. doi: 10.1128/AEM.70.3.1506-1513.2004. PubMed DOI PMC
Sekar R, Pernthaler A, Pernthaler J, Warnecke F, Posch T, Amann R. An improved protocol for quantification of freshwater Actinobacteria by fluorescence in situ hybridization. Appl Environ Microbiol. 2003:2928–35. 10.1128/aem.69.5.2928-2935.2003 PubMed PMC
Warnecke F, Sommaruga R, Sekar R, Hofer JS, Pernthaler J. Abundances, identity, and growth state of actinobacteria in mountain lakes of different UV transparency. Appl Environ Microbiol. 2005;71:5551–5559. doi: 10.1128/AEM.71.9.5551-5559.2005. PubMed DOI PMC
Friedrich U, Van Langenhove H, Altendorf K, Lipski A. Microbial community and physicochemical analysis of an industrial waste gas biofilter and design of 16S rRNA-targeting oligonucleotide probes. Environ Microbiol. 2003:439–439. 10.1046/j.1462-2920.2001.00169.x-i1 PubMed
Salcher MM, Pernthaler J, Frater N, Posch T. Vertical and longitudinal distribution patterns of different bacterioplankton populations in a canyon-shaped, deep prealpine lake. Limnol Oceanogr. 2011:2027–39. 10.4319/lo.2011.56.6.2027
Neuenschwander SM, Salcher MM, Pernthaler J. Fluorescence in situ hybridization and sequential catalyzed reporter deposition (2C-FISH) for the flow cytometric sorting of freshwater ultramicrobacteria. Front Microbiol. 2015;6:247. doi: 10.3389/fmicb.2015.00247. PubMed DOI PMC
Kemp PF, Cole JJ, Sherr BF, Sherr EB. Handbook of methods in aquatic microbial ecology. CRC Press; 1993.
Metfies K, Medlin LK. Refining cryptophyte identification with DNA-microarrays. J Plankton Res Oxford University Press. 2007;29:1071–1075. doi: 10.1093/plankt/fbm080. DOI
Šimek K, Grujčić V, Mukherjee I, Kasalický V, Nedoma J, Posch T, et al. Cascading effects in freshwater microbial food webs by predatory Cercozoa, Katablepharidacea and ciliates feeding on aplastidic bacterivorous cryptophytes. FEMS Microbiol Ecol. academic.oup.com; 2020;96. 10.1093/femsec/fiaa121 PubMed PMC
Seda J, Kolarova K, Petrusek A, Machacek J. Daphnia galeata in the deep hypolimnion: Spatial differentiation of a “typical epilimnetic” species. Hydrobiologia. 2007. pp. 47–57.
McCauley E, Downing JA, Rigler FH. A manual on methods for the assessment of secondary productivity in fresh waters. Oxford: Blackwell Scientific UK; 1984. pp. 228–65.
Li D, Luo R, Liu C-M, Leung C-M, Ting H-F, Sadakane K, et al. MEGAHIT v1.0: a fast and scalable metagenome assembler driven by advanced methodologies and community practices. Methods. 2016;102:3–11. doi: 10.1016/j.ymeth.2016.02.020. PubMed DOI
Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 2013;41:D590–6. doi: 10.1093/nar/gks1219. PubMed DOI PMC
Steinegger M, Söding J. MMseqs2 enables sensitive protein sequence searching for the analysis of massive data sets. Nat Biotechnol. 2017;35:1026–1028. doi: 10.1038/nbt.3988. PubMed DOI
Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, et al. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997;25:3389–402. doi: 10.1093/nar/25.17.3389. PubMed DOI PMC
Kang DD, Froula J, Egan R, Wang Z. MetaBAT, an efficient tool for accurately reconstructing single genomes from complex microbial communities. PeerJ. 2015;3:e1165. doi: 10.7717/peerj.1165. PubMed DOI PMC
Kieft K, Zhou Z, Anantharaman K. VIBRANT: automated recovery, annotation and curation of microbial viruses, and evaluation of viral community function from genomic sequences. Microbiome. 2020;8:90. doi: 10.1186/s40168-020-00867-0. PubMed DOI PMC
Aylward FO, Moniruzzaman M. ViralRecall-A flexible command-line tool for the detection of giant virus signatures in ’omic data. Viruses. 2021;13. Available from: 10.3390/v13020150 PubMed PMC
Hyatt D, Chen G-L, Locascio PF, Land ML, Larimer FW, Hauser LJ. Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics. 2010;11:119. doi: 10.1186/1471-2105-11-119. PubMed DOI PMC
Parks DH, Chuvochina M, Waite DW, Rinke C, Skarshewski A, Chaumeil P-A, et al. A standardized bacterial taxonomy based on genome phylogeny substantially revises the tree of life. Nat Biotechnol. 2018;36:996–1004. doi: 10.1038/nbt.4229. PubMed DOI
Chaumeil PA, Mussig AJ, Hugenholtz P, Parks DH. GTDB-Tk: a toolkit to classify genomes with the Genome Taxonomy Database. Bioinformatics. 2019. academic.oup.com; 10.1093/bioinformatics/btz848. PubMed PMC
Parks DH, Imelfort M, Skennerton CT, Hugenholtz P, Tyson GW. CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res. 2015;25:1043–1055. doi: 10.1101/gr.186072.114. PubMed DOI PMC
Olm MR, Brown CT, Brooks B, Banfield JF. dRep: a tool for fast and accurate genomic comparisons that enables improved genome recovery from metagenomes through de-replication. ISME J. 2017;11:2864–8. doi: 10.1038/ismej.2017.126. PubMed DOI PMC
Lu S, Wang J, Chitsaz F, Derbyshire MK, Geer RC, Gonzales NR, et al. CDD/SPARCLE: the conserved domain database in 2020. Nucleic Acids Res. 2020;48:D265–D268. doi: 10.1093/nar/gkz991. PubMed DOI PMC
Mann NH, Cook A, Millard A, Bailey S, Clokie M. Marine ecosystems: bacterial photosynthesis genes in a virus. Nature. 2003;424:741. doi: 10.1038/424741a. PubMed DOI
Mizuno CM, Rodriguez-Valera F, Kimes NE, Ghai R. Expanding the marine virosphere using metagenomics. PLoS Genet. 2013;9:e1003987. doi: 10.1371/journal.pgen.1003987. PubMed DOI PMC
Edwards RA, McNair K, Faust K, Raes J, Dutilh BE. Computational approaches to predict bacteriophage-host relationships. FEMS Microbiol Rev. 2016;40:258–272. doi: 10.1093/femsre/fuv048. PubMed DOI PMC
Moniruzzaman M, Martinez-Gutierrez CA, Weinheimer AR, Aylward FO. Dynamic genome evolution and complex virocell metabolism of globally-distributed giant viruses. Nat Commun. 2020;11:1710. doi: 10.1038/s41467-020-15507-2. PubMed DOI PMC
Sievers F, Higgins DG. Clustal Omega for making accurate alignments of many protein sequences. Protein Sci. 2018;27:135–145. doi: 10.1002/pro.3290. PubMed DOI PMC
Criscuolo A, Gribaldo S. BMGE (Block Mapping and Gathering with Entropy): a new software for selection of phylogenetic informative regions from multiple sequence alignments. BMC Evol Biol. 2010;10:210. doi: 10.1186/1471-2148-10-210. PubMed DOI PMC
Minh BQ, Schmidt HA, Chernomor O, Schrempf D, Woodhams MD, von Haeseler A, et al. IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. Mol Biol Evol. 2020;37:1530–1534. doi: 10.1093/molbev/msaa015. PubMed DOI PMC
Hoang DT, Chernomor O, von Haeseler A, Minh BQ, Vinh LS. UFBoot2: improving the ultrafast bootstrap approximation. Mol Biol Evol. 2018;35:518–522. doi: 10.1093/molbev/msx281. PubMed DOI PMC
Kalyaanamoorthy S, Minh BQ, Wong TKF, von Haeseler A, Jermiin LS. ModelFinder: fast model selection for accurate phylogenetic estimates. Nat Methods. 2017;14:587–589. doi: 10.1038/nmeth.4285. PubMed DOI PMC
Levy Karin E, Mirdita M, Söding J. MetaEuk—sensitive, high-throughput gene discovery, and annotation for large-scale eukaryotic metagenomics. Microbiome. 2020;8:48. doi: 10.1186/s40168-020-00808-x. PubMed DOI PMC
Seppey M, Manni M, Zdobnov EM. BUSCO: assessing genome assembly and annotation completeness. Methods Mol Biol Springer. 2019;1962:227–245. doi: 10.1007/978-1-4939-9173-0_14. PubMed DOI
UniProt Consortium UniProt: the universal protein knowledgebase in 2021. Nucleic Acids Res. 2021;49:D480–D489. doi: 10.1093/nar/gkaa1100. PubMed DOI PMC
Keeling PJ, Burki F, Wilcox HM, Allam B, Allen EE, Amaral-Zettler LA, et al. The Marine Microbial Eukaryote Transcriptome Sequencing Project (MMETSP): illuminating the functional diversity of eukaryotic life in the oceans through transcriptome sequencing. PLoS Biol. 2014;12:e1001889. doi: 10.1371/journal.pbio.1001889. PubMed DOI PMC
Mirarab S, Nguyen N, Guo S, Wang L-S, Kim J, Warnow T. PASTA: ultra-large multiple sequence alignment for nucleotide and amino-acid sequences. J Comput Biol. 2015;22:377–386. doi: 10.1089/cmb.2014.0156. PubMed DOI PMC
Weese D, Holtgrewe M, Reinert K. RazerS 3: faster, fully sensitive read mapping. Bioinformatics. 2012;28:2592–2599. doi: 10.1093/bioinformatics/bts505. PubMed DOI
Emiola A, Oh J. High throughput in situ metagenomic measurement of bacterial replication at ultra-low sequencing coverage. Nat Commun. 2018;9:4956. doi: 10.1038/s41467-018-07240-8. PubMed DOI PMC
Phenology and ecological role of aerobic anoxygenic phototrophs in freshwaters
Global freshwater distribution of Telonemia protists
Isolation of a widespread giant virus implicated in cryptophyte bloom collapse
Flexible genomic island conservation across freshwater and marine Methylophilaceae