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Probing the evolution, ecology and physiology of marine protists using transcriptomics

Key Points

  • Single-celled eukaryotes (protists) constitute a tremendously diverse group of microorganisms. These species exhibit a wide range of nutritional modes (many species possess multiple nutritional modes simultaneously) and are essential components at several trophic levels within food webs.

  • Genetic analyses of protists have lagged behind those of other microbial taxa because protists have much larger genomes and more complicated gene expression patterns. Consequently, we have very limited knowledge about gene number, identity and function within many protistan lineages.

  • Widespread application of targeted gene sequencing (most notably, of small-subunit rRNA genes) has greatly improved our knowledge of eukaryote phylogeny and provided a framework for an emerging taxonomy incorporating morphological and molecular information.

  • A recently developed alternative approach to provide genetic information for ecologically important protistan taxa is transcriptome sequencing of cultured species. Transcriptomes are providing vital databases of genes for species that lack sequenced genomes.

  • Transcriptomic studies of cultures and natural assemblages of phototrophic protists (phytoplankton) are revealing complex metabolic responses to environmental conditions (such as nutrient limitation and light regime), pathways that are involved in toxin production by some harmful algal species and changes in gene expression that are related to shifts in nutritional mode for mixotrophic species.

  • The application of transcriptomic approaches to the study of protistan symbioses, predator–prey interactions and protist–bacterium interactions are beginning to reveal the molecular signalling that is involved in the recognition and response between microorganisms, providing insights into the origin of eukaryotic organelles and the structure of aquatic food webs.

  • We now have an improved understanding of the physiological responses of ecologically relevant protistan species and trophic groups to environmental changes. This understanding, which has been garnered through omics studies, is being harnessed to improve the predictive capabilities of global biogeochemical models.

Abstract

Protists, which are single-celled eukaryotes, critically influence the ecology and chemistry of marine ecosystems, but genome-based studies of these organisms have lagged behind those of other microorganisms. However, recent transcriptomic studies of cultured species, complemented by meta-omics analyses of natural communities, have increased the amount of genetic information available for poorly represented branches on the tree of eukaryotic life. This information is providing insights into the adaptations and interactions between protists and other microorganisms and macroorganisms, but many of the genes sequenced show no similarity to sequences currently available in public databases. A better understanding of these newly discovered genes will lead to a deeper appreciation of the functional diversity and metabolic processes in the ocean. In this Review, we summarize recent developments in our understanding of the ecology, physiology and evolution of protists, derived from transcriptomic studies of cultured strains and natural communities, and discuss how these novel large-scale genetic datasets will be used in the future.

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Figure 1: Ecological and biogeochemical roles of protists in the marine plankton.
Figure 2: The rapidly changing landscape of protistan phylogeny.
Figure 3: Symbiosis and mixotrophy among protists.
Figure 4: Improved gene identification and understanding of phytoplankton functional groups.
Figure 5: Interactions between protists and other microorganisms.

References

  1. Whittaker, R. H. New concepts of kingdoms of organisms. Science 163, 150–160 (1969).

    Article  CAS  PubMed  Google Scholar 

  2. Ohtsuka, S., Suzaki, T., Horiguchi, T., Suzuki, N. & Not, F. (eds) Marine Protists (Springer, 2015).

    Book  Google Scholar 

  3. Worden, A. Z. et al. Rethinking the marine carbon cycle: factoring in the multifarious lifestyles of microbes. Science 347, 1257594 (2015). An overview of protistan contributions to biogeochemical cycles.

    Article  CAS  PubMed  Google Scholar 

  4. de Vargas, C. et al. Eukaryotic plankton diversity in the sunlit ocean. Science 348, 1261605 (2015). Data obtained from the Tara Oceans expedition expands our knowledge of the global diversity of protists.

    Article  CAS  PubMed  Google Scholar 

  5. Keeling, P. J. 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. 12, e1001889 (2014). An article delineating the contribution of the MMETSP to expanding the global databases for gene discovery and annotation in protists.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. del Campo, J. et al. The others: our biased perspective of eukaryotic genomes. Trends Ecol. Evol. 29, 252–259 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  7. Cuvelier, M. L. et al. Targeted metagenomics and ecology of globally important uncultured eukaryotic phytoplankton. Proc. Natl Acad. Sci. USA 107, 14679–14684 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  8. Caron, D. A. Towards a molecular taxonomy for protists: benefits, risks and applications in plankton ecology. J. Eukaryot. Microbiol. 60, 407–413 (2013).

    Article  PubMed  Google Scholar 

  9. Fenchel, T. & Finlay, B. J. The ubiquity of small species: patterns of local and global diversity. Bioscience 54, 777–784 (2004).

    Article  Google Scholar 

  10. Foissner, W. Biogeography and dispersal of micro-organisms: a review emphasizing protists. Acta Protozool. 45, 111–136 (2006).

    Google Scholar 

  11. Guillou, L. et al. Widespread occurrence and genetic diversity of marine parasitoids belonging to Syndiniales (Alveolata). Environ. Microbiol. 10, 3349–3365 (2008).

    Article  CAS  PubMed  Google Scholar 

  12. Shalchian-Tabrizi, K., Kauserud, H., Massana, R., Klaveness, D. & Jakobsen, K. S. Analysis of environmental 18S ribosomal RNA sequences reveals unknown diversity of the cosmopolitan phylum Telonemia. Protist 158, 173–180 (2007).

    Article  CAS  PubMed  Google Scholar 

  13. Caron, D. A. & Countway, P. D. Hypotheses on the role of the protistan rare biosphere in a changing world. Aquat. Microb. Ecol. 57, 227–238 (2009).

    Article  Google Scholar 

  14. Logares, R. et al. Patterns of rare and abundant marine microbial eukaryotes. Curr. Biol. 24, 813–821 (2014).

    Article  CAS  PubMed  Google Scholar 

  15. Lynch, M. D. J. & Neufeld, J. D. Ecology and expolaration of the rare biosphere. Nat. Rev. Microbiol. 13, 217–229 (2015).

    Article  CAS  PubMed  Google Scholar 

  16. Caron, D. A., Worden, A. Z., Countway, P. D., Demir, E. & Heidelberg, K. B. Protists are microbes too: a perspective. ISME J. 3, 4–12 (2009).

    Article  CAS  PubMed  Google Scholar 

  17. Cohen, L., Alexander, H. & Brown, C. T. Marine Microbial Eukaryotic Transcriptome Sequencing Project, re-assemblies. Figshare https://dx.doi.org/10.6084/m9.figshare.3840153.v1 (2016).

  18. Pernice, M. C. et al. Global abundance of planktonic heterotrophic protists in the deep ocean. ISME J. 9, 782–792 (2015).

    Article  CAS  PubMed  Google Scholar 

  19. Woese, C. R., Kandler, O. & Wheelis, M. L. Towards a natural system of organisms: Proposal for the domains Archaea, Bacteria and Eucarya. Proc. Natl Acad. Sci. USA 87, 4576–4579 (1990).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Sogin, M. L. Early evolution and the origin of eukaryotes. Curr. Opin. Genet. Dev. 1, 457–463 (1991).

    Article  CAS  PubMed  Google Scholar 

  21. Simpson, A. G. B. & Roger, A. J. The real 'kingdoms' of eukaryotes. Curr. Biol. 14, R693–R696 (2004).

    Article  CAS  PubMed  Google Scholar 

  22. Baldauf, S. L. An overview of the phylogeny and diversity of eukaryotes. J. Systemat. Evol. 46, 263–273 (2008).

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  24. Burki, F. et al. Phylogenomics reshuffles the eukaryotic supergroups. PLoS ONE 8, E790 (2007).

    Article  CAS  Google Scholar 

  25. Adl, S. M. et al. The revised classification of eukaryotes. J. Eukaryot. Microbiol. 59, 429–514 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  26. Burki, F. The eukaryotic tree of life from a global phylogenomic perspective. Cold Spring Harb. Perspect. Biol. 6, a016147 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Grant, J. R. & Katz, L. A. Building a phylogenomic pipeline for the eukaryotic tree of life — addressing deep phylogenies with genome-scale data. PLOS Curr. http://dx.doi.org/10.1371/currents.tol.c24b6054aebf3602748ac042ccc8f2e9 (2014).

  28. Koonin, E. V. The origin and early evolution of eukaryotes in the light of phylogenomics. Genome Biol. 11, 209 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Barberà, M. J., Ruiz-Trillo, I., Leigh, J., Hug, L. A. & Roger, A. J. in Origin of Mitochondria and Hydrogenosomes (eds Martin, W. F. & Müller, M.) 239–275 (Springer, 2007).

    Book  Google Scholar 

  30. Gould, S. B., Waller, R. F. & McFadden, G. I. Plastid evolution. Annu. Rev. Plant Biol. 59, 491–517 (2008).

    Article  CAS  PubMed  Google Scholar 

  31. Keeling, P. J. The number, speed, and impact of plastid endosymbioses on eukaryotic evolution. Annu. Rev. Plant Biol. 64, 583–607 (2013).

    Article  CAS  PubMed  Google Scholar 

  32. Deschamps, P. & Moreira, D. Reevaluating the green contribution to diatom genomes. Genome Biol. Evol. 4, 683–688 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Burki, F. et al. Endosymbiotic gene transfer in tertiary plastid-containing dinoflagellates. Eukaryot. Cell 13, 246–255 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Slamovits, C. H. & Keeling, P. J. Plastid-derived genes in the non-photosynthetic alveolate Oxyrrhis marina. Mol. Biol. Evol. 25, 1297–1306 (2008).

    Article  CAS  PubMed  Google Scholar 

  35. Moore, C. E. & Archibald, J. M. Nucleomorph genomes. Annu. Rev. Genet. 43, 251–264 (2009).

    Article  CAS  PubMed  Google Scholar 

  36. Curtis, B. A. et al. Algal genomes reveal evolutionary mosaicism and the fate of nucleomorphs. Nature 492, 59–65 (2012).

    Article  CAS  PubMed  Google Scholar 

  37. Nakayama, T. & Ishida, K.-I. Another acquisition of a primary photosynthetic organelle is underway in Paulinella chromatophora. Curr. Biol. 19, R284–R285 (2009).

    Article  CAS  PubMed  Google Scholar 

  38. Nowack, E. C. et al. Endosymbiotic gene transfer and transcriptional regulation of transferred genes in Paulinella chromatophora. Mol. Biol. Evol. 28, 407–422 (2011).

    Article  CAS  PubMed  Google Scholar 

  39. Nowack, E. C. & Grossman, A. R. Trafficking of protein into the recently established photosynthetic organelles of Paulinella chromatophora. Proc. Natl Acad. Sci. USA 109, 5340–5345 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  40. Nakayama, T. & Archibald, J. M. Evolving a photosynthetic organelle. BMC Biol. 10, 34 (2012).

    Article  CAS  Google Scholar 

  41. Estrela, S., Kerr, B. & Morris, J. J. Transitions in individuality through symbiosis. Curr. Opin. Microbiol. 31, 191–198 (2016).

    Article  PubMed  Google Scholar 

  42. Lin, S. et al. The Symbiodinium kawagutii genome illuminates dinoflagellate gene expression and coral symbiosis. Science 350, 691–694 (2015).

    Article  CAS  PubMed  Google Scholar 

  43. Bayer, T. et al. Symbiodinium transcriptomes: genome insights into the dinoflagellate symbionts of reef-building corals. PLoS ONE 7, e35269 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Biard, T. et al. In situ imaging reveals the biomass of large protists in the global ocean. Nature 532, 504–507 (2016).

    Article  CAS  PubMed  Google Scholar 

  45. Decelle, J. et al. An original mode of symbiosis in open ocean plankton. Proc. Natl Acad. Sci. USA 109, 18000–18005 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  46. Balzano, S. et al. Transcriptome analyses to investigate symbiotic relationships between marine protists. Front. Microbiol. 6, 98 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  47. Pillet, L. & Pawlowski, J. Transcriptome analysis of foraminiferan Elphidium margaritaceum questions the role of gene transfer in kleptoplastidy. Mol. Biol. Evol. 30, 66–69 (2013).

    Article  CAS  PubMed  Google Scholar 

  48. Chen, M. M., Chory, J. & Fankhauser, C. Light signal transduction in higher plants. Annu. Rev. Genet. 38, 87–117 (2004).

    Article  CAS  PubMed  Google Scholar 

  49. Falciatore, A. & Bowler, C. The evolution and function of blue and red light photoreceptors. Curr. Top. Dev. Biol. 68, 317–350 (2005).

    Article  CAS  PubMed  Google Scholar 

  50. Rodriguez-Romero, J., Hedtke, M., Kastner, C., Muller, S. & Fischer, R. Fungi, hidden in soil or up in the air: light makes a difference. Annu. Rev. Microbiol. 64, 585–610 (2010).

    Article  CAS  PubMed  Google Scholar 

  51. Fortunato, A. E. et al. Diatom phytochromes reveal the existence of far-red light-based sensing in the ocean. Plant Cell 28, 616–628 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Worden, A. Z. et al. Green evolution and dynamic adaptations revealed by genomes of the marine picoeukaryotes Micromonas. Science 324, 268–272 (2009).

    Article  CAS  PubMed  Google Scholar 

  53. Duanmu, D. et al. Marine algae and land plants share conserved phytochrome signaling systems. Proc. Natl Acad. Sci. USA 111, 15827–15832 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Moreau, H. et al. Gene functionalities and genome structure in Bathycoccus prasinos reflect cellular specializations at the base of the green lineage. Genome Biol. 13, 1–16 (2012).

    Article  Google Scholar 

  55. Allen, A. E. et al. Evolution and functional diversification of fructose bisphosphate aldolase genes in photosynthetic marine diatoms. Mol. Biol. Evol. 29, 367–379 (2012).

    Article  CAS  PubMed  Google Scholar 

  56. Armbrust, E. The life of diatoms in the world's oceans. Nature 459, 185–192 (2009).

    Article  CAS  PubMed  Google Scholar 

  57. Farikou, O. et al. Inferring the seasonal evolution of phytoplankton groups in the Senegalo-Mauritanian upwelling region from satellite ocean-color spectral measurements. J. Geophys. Res.: Oceans 120, 6581–6601 (2015).

    Article  Google Scholar 

  58. Dyhrman, S. T. et al. The transcriptome and proteome of the diatom Thalassiosira pseudonana reveal a diverse phosphorus stress response. PLoS ONE 7, e33768 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Gobler, C. J. et al. Niche of harmful alga Aureococcus anophagefferens revealed through ecogenomics. Proc. Natl Acad. Sci USA. 108, 4352–4357 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Shrestha, R. P. et al. Whole transcriptome analysis of the silicon response of the diatom Thalassiosira pseudonana. BMC Genomics 13, 499 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Schmollinger, S. et al. Nitrogen-sparing mechanisms in Chlamydomonas affect the transcriptome, the proteome, and photosynthetic metabolism. Plant Cell 26, 1410–1435 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Zones, J. M., Blaby, I. K., Merchant, S. S. & Umen, J. G. High-resolution profiling of a synchronized diurnal transcriptome from Chlamydomonas reinhardtii reveals continuous cell and metabolic differentiation. Plant Cell 27, 2743–2769 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  63. Whitney, L. P. & Lomas, M. W. Growth on ATP elicits a P-stress response in the picoeukaryote Micromonas pusilla. PLoS ONE 11, e0155158 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Monnier, A. et al. Orchestrated transcription of biological processes in the marine picoeukaryote Ostreococcus exposed to light/dark cycles. BMC Genomics 11, 192 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Poliner, E. et al. Transcriptional coordination of physiological responses in Nannochloropsis oceanica CCMP1779 under light/dark cycles. Plant J. 83, 1097–1113 (2015).

    Article  CAS  PubMed  Google Scholar 

  66. Allen, A. E., Vardi, A. & Bowler, C. An ecological and evolutionary context for integrated nitrogen metabolism and related signaling pathways in marine diatoms. Curr. Opin. Plant Biol. 9, 264–273 (2006).

    Article  CAS  PubMed  Google Scholar 

  67. Allen, A. E. et al. Evolution and metabolic significance of the urea cycle in photosynthetic diatoms. Nature 473, 203–207 (2011).

    Article  CAS  PubMed  Google Scholar 

  68. Armbrust, E. V. et al. The genome of the diatom Thalassiosira pseudonana: ecology, evolution, and metabolism. Science 306, 79–86 (2004).

    Article  CAS  PubMed  Google Scholar 

  69. Mock, T. et al. Whole-genome expression profiling of the marine diatom Thalassiosira pseudonana identifies genes involved in silicon bioprocesses. Proc. Natl Acad. Sci. USA 105, 1579–1584 (2008).

    Article  PubMed  PubMed Central  Google Scholar 

  70. Hockin, N. L., Mock, T., Mulholland, F., Kopriva, S. & Malin, G. The response of diatom central carbon metabolism to nitrogen starvation is different from that of green algae and higher plants. Plant Physiol. 158, 299–312 (2012).

    Article  CAS  PubMed  Google Scholar 

  71. Allen, A. E. et al. Whole-cell response of the pennate diatom Phaeodactylum tricornutum to iron starvation. Proc. Natl Acad. Sci. USA 105, 10438–10443 (2008).

    Article  PubMed  PubMed Central  Google Scholar 

  72. Bender, S. J., Durkin, C. A., Berthiaume, C. T., Morales, R. L. & Armbrust, E. V. Transcriptional responses of three model diatoms to nitrate limitation of growth. Front. Mar. Sci. 1, 3 (2014).

    Article  Google Scholar 

  73. Hackett, J. D., Anderson, D. M., Erdner, D. L. & Bhattacharya, D. Dinoflagellates: a remarkable evolutionary experiment. Am. J. Bot. 91, 1523–1534 (2004).

    Article  CAS  PubMed  Google Scholar 

  74. Cooper, J. T., Sinclair, G. & Wawrik, B. Transcriptome analysis of Scrippsiella trochoidea CCMP 3099 reveals physiological changes related to nitrate depletion. Front. Microbiol. 7, 639 (2016).

    PubMed  PubMed Central  Google Scholar 

  75. Guo, R., Wang, H., Suh, Y. S. & Ki, J.-S. Transcriptomic profiles reveal the genome-wide responses of the harmful dinoflagellate Cochlodinium polykrikoides when exposed to the algicide copper sulfate. BMC Genomics 17, 29 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Frischkorn, K. R., Harke, M. J., Gobler, C. J. & Dyhrman, S. T. De novo assembly of Aureococcus anophagefferens transcriptomes reveals diverse responses to the low nutrient and low light conditions present during blooms. Front. Microbiol. 5, 375 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  77. Gobler, C. J., Boneillo, G. E., Debenham, C. J. & Caron, D. A. Nutrient limitation, organic matter cycling, and plankton dynamics during an Aureococcus anophagefferens bloom. Aquat. Microb. Ecol. 35, 31–43 (2004).

    Article  Google Scholar 

  78. Wurch, L. L., Gobler, C. J. & Dyhrman, S. T. Expression of a xanthine permease and phosphate transporter in cultures and field populations of the harmful alga Aureococcus anophagefferens: tracking nutritional deficiency during brown tides. Environ. Microbiol. 8, 2444–2457 (2014).

    Article  CAS  Google Scholar 

  79. Qiu, X. et al. Allelopathy of the raphidophyte Heterosigma akashiwo against the dinoflagellate Akashiwo sanguinea is mediated via allelochemicals and cell contact. Mar. Ecol. Prog. Ser. 446, 107–118 (2012).

    Article  Google Scholar 

  80. Smetacek, V. A watery arms race. Nature 411, 745 (2001).

    Article  CAS  PubMed  Google Scholar 

  81. Remmel, E. J. & Hambright, K. D. Toxin-assisted micropredation: experimental evidence shows that contact micropredation rather than exotoxicity is the role of Prymnesium toxins. Ecol. Lett. 15, 126–132 (2012).

    Article  PubMed  Google Scholar 

  82. Manning, S. R. & La Claire, J. W. Prymnesins: toxic metabolites of the golden alga, Prymnesium parvum Carter (Haptophyta). Mar. Drugs 8, 678–704 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Strom, S., Wolfe, G. V., Slajer, A., Lambert, S. & Clough, J. Chemical defenses in the microplankton II: inhibition of protist feeding by β-dimethylsulfoniopropionate (DMSP). Limnol. Oceanogr. 48, 230–237 (2003).

    Article  CAS  Google Scholar 

  84. Stüken, A. et al. Discovery of nuclear-encoded genes for the neurotoxin saxitoxin in dinoflagellates. PLoS ONE 6, e20096 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Beszteri, S. et al. Transcriptomic response of the toxic prymnesiophyte Prymnesium parvum (N. Carter) to phosphorus and nitrogen starvation. Harmful Algae 18, 1–15 (2012).

    Article  CAS  Google Scholar 

  86. Liu, Z. et al. Changes in gene expression of Prymnesium parvum due to nitrogen and phosphorus limitation. Front. Microbiol. 6, 631 (2015).

    PubMed  PubMed Central  Google Scholar 

  87. McLean, T. I. “Eco-omics”: a review of the application of genomics, transcriptomics, and proteomics for the study of the ecology of harmful algae. Microb. Ecol. 65, 901–915 (2013).

    Article  CAS  PubMed  Google Scholar 

  88. Delmont, T. O., Eren, A. M., Vineis, J. H. & Post, A. F. Genome reconstructions indicate the partitioning of ecological functions inside a phytoplankton bloom in the Amundsen Sea, Antarctica. Front. Microbiol. 6, 1090 (2015).

    PubMed  PubMed Central  Google Scholar 

  89. Ottesen, E. A. et al. Pattern and synchrony of gene expression among sympatric marine microbial populations. Proc. Natl Acad. Sci. USA 110, E488–E497 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  90. Marchetti, A. et al. Comparative metatranscriptomics identifies molecular bases for the physiological responses of phytoplankton to varying iron availability. Proc. Natl Acad. Sci. USA 109, E317–E325 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  91. Boyd, P. W. et al. A mesoscale phytoplankton bloom in the polar Southern Ocean stimulated by iron fertilization. Nature 407, 695–702 (2000).

    Article  CAS  PubMed  Google Scholar 

  92. Pearson, G. A. et al. Metatranscriptomes reveal functional variation in diatom communities from the Antarctic Peninsula. ISME J. 9, 2275–2289 (2015). A metatranscriptomic study of phytoplankton communities off the Antarctic peninsula.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Bertrand, E. M. et al. Phytoplankton–bacterial interactions mediate micronutrient colimitation at the coastal Antarctic sea ice edge. Proc. Natl Acad. Sci. USA 112, 9938–9943 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Aylward, F. O. et al. Microbial community transcriptional networks are conserved in three domains at ocean basin scales. Proc. Natl Acad. Sci. USA 112, 5443–5448 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Ashworth, J. et al. Genome-wide diel growth state transitions in the diatom Thalassiosira pseudonana. Proc. Natl Acad. Sci. USA 110, 7518–7523 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  96. Alexander, H., Jenkins, B. D., Rynearson, T. A. & Dyhrman, S. T. Metatranscriptome analyses indicate resource partitioning between diatoms in the field. Proc. Natl Acad. Sci. USA 112, E2182–E2190 (2015). The application of transcriptomic approaches help to identify examples of resource competition and to understand its effects within natural phytoplankton assemblages.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Alexander, H. et al. Functional group-specific traits drive phytoplankton dynamics in the oligotrophic ocean. Proc. Natl Acad. Sci. USA 112, E5972–E5979 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. von Dassow, P. et al. Life-cycle modification in open oceans accounts for genome variability in a cosmopolitan phytoplankton. ISME J. 9, 1365–1377 (2015).

    Article  PubMed  Google Scholar 

  99. Read, B. A. et al. Pan genome of the phytoplankton Emiliania underpins its global distribution. Nature 499, 209–213 (2013).

    Article  CAS  PubMed  Google Scholar 

  100. Karl, D. M., Church, M. J., Dore, J. E., Letelier, R. M. & Mahaffey, C. Predictable and efficient carbon sequestration in the North Pacific Ocean supported by symbiotic nitrogen fixation. Proc. Natl Acad. Sci. USA 109, 1842–1849 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  101. Benitez-Nelson, C. R. et al. Mesoscale eddies drive increased silica export in the subtropical Pacific Ocean. Science 316, 1017–1021 (2007).

    Article  CAS  PubMed  Google Scholar 

  102. Lewin, J. C. Heterotrophy in diatoms. J. Gen. Microbiol. 9, 305–313 (1953).

    Article  CAS  PubMed  Google Scholar 

  103. Croft, M. T., Warren, M. J. & Smith, A. G. Algae need their vitamins. Eukaryot. Cell 5, 1175–1183 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  104. Mitra, A. et al. Defining planktonic protist functional groups on mechanisms for energy and nutrient acquisition: incorporation of diverse mixotrophic strategies. Protist 167, 106–120 (2016).

    Article  CAS  PubMed  Google Scholar 

  105. Ward, B. A. & Follows, M. J. Marine mixotrophy increases trophic transfer efficiency, mean organism size, and vertical carbon flux. Proc. Natl Acad. Sci. USA 113, 2958–2963 (2016). A recent attempt to introduce mixotrophic behaviour into global marine biogeochemical models.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  106. Liu, Z., Campbell, V., Heidelberg, K. B. & Caron, D. A. Gene expression characterizes different nutritional strategies among three mixotrophic protists. FEMS Microbiol. Ecol. 92, fiw106 (2016).

    Article  CAS  PubMed  Google Scholar 

  107. Sanders, R. W., Caron, D. A., Davidson, J. M., Dennett, M. R. & Moran, D. M. Nutrient acquisition and population growth of a mixotrophic alga in axenic and bacterized cultures. Microb. Ecol. 42, 513–523 (2001).

    Article  CAS  PubMed  Google Scholar 

  108. Stoecker, D. K. Mixotrophy among dinoflagellates. J. Eukaryot. Microbiol. 46, 397–401 (1999).

    Article  Google Scholar 

  109. Johnson, M. D. Acquired phototrophy in ciliates: a review of cellular interactions and structural adaptations. J. Eukaryot. Microbiol. 58, 185–195 (2011).

    Article  PubMed  Google Scholar 

  110. Johnson, M. D., Oldach, D., Delwiche, D. F. & Stoecker, D. K. Retention of transcriptionally active cryptophyte nuclei by the ciliate Myrionecta rubra. Nature 445, 426–428 (2007).

    Article  CAS  PubMed  Google Scholar 

  111. Lasek-Nesselquist, E., Wisecaver, J. H., Hackett, J. D. & Johnson, M. D. Insights into transcriptional changes that accompany organelle sequestration from the stolen nucleus of Mesodinium rubrum. BMC Genomics 16, 805 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  112. Lima-Mendez, G. et al. Determinants of community structure in the global plankton interactome. Science 348, 1262073 (2015). The introduction of the 'interactome', a concept for the organization of marine microbes into groups or 'gilds' of closely interacting taxa.

    Article  CAS  PubMed  Google Scholar 

  113. Sillo, A. et al. Genome-wide transcriptional changes induced by phagocytosis or growth on bacteria in Dictyostelium. BMC Genomics 9, 291 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  114. Liu, Z. et al. Gene expression in the mixotrophic prymnesiophyte, Prymnesium parvum, responds to prey availability. Front. Microbiol. 6, 319 (2015).

    PubMed  PubMed Central  Google Scholar 

  115. Barratt, J. L. N., Cao, M., Stark, D. J. & Ellis, J. T. The transcriptome sequence of Dientamoeba fragilis offers new biological insights on its metabolism, kinome, degradome and potential mechanisms of pathogenicity. Protist 166, 389–408 (2015).

    Article  CAS  PubMed  Google Scholar 

  116. Lu, Y., Wohlrab, S., Glöckner, G., Guillou, L. & John, U. Genomic insights into processes driving the infection of Alexandrium tamarense by the parasitoid Amoebophrya sp. Eukaryot. Cell 13, 1439–1449 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  117. Lee, R. et al. Analysis of EST data of the marine protist Oxyrrhis marina, an emerging model for alveolate biology and evolution. BMC Genomics 15, 122 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  118. Guo, Z., Zhang, H. & Lin, S. Light-promoted rhodopsin expression and starvation survival in the marine dinoflagellate Oxyrrhis marina. PLoS ONE 9, e114941 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  119. Amin, S. A. et al. Interaction and signalling between a cosmopolitan phytoplankton and associated bacteria. Nature 522, 98–101 (2015).

    Article  CAS  PubMed  Google Scholar 

  120. Stocker, R. Marine microbes see a sea of gradients. Science 338, 628–633 (2012). A report about the microscales of physics and chemistry, and their role in shaping aquatic microbial activities.

    Article  CAS  PubMed  Google Scholar 

  121. Sapp, M. et al. Species-apecific bacterial communities in the phycosphere of microalgae? Microb. Ecol. 53, 683–699 (2007).

    Article  PubMed  Google Scholar 

  122. Schäfer, H., Abbas, B., Witte, H. & Muyzer, G. Genetic diversity of 'satellite' bacteria present in cultures of marine diatoms. FEMS Microbiol. Ecol. 42, 25–35 (2002).

    PubMed  Google Scholar 

  123. Durham, B. P. et al. Cryptic carbon and sulfur cycling between surface ocean plankton. Proc. Natl Acad. Sci. USA 112, 453–457 (2015).

    Article  CAS  PubMed  Google Scholar 

  124. Thompson, A. W. et al. Unicellular cyanobacterium symbiotic with a single-celled eukaryotic alga. Science 337, 1546–1550 (2012).

    Article  CAS  PubMed  Google Scholar 

  125. Cruz-López, R. & Maske, H. The vitamin B1 and B12 required by the marine dinoflagellate Lingulodinium polyedrum can be provided by its associated bacterial community in culture. Front. Microbiol. 7, 560 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  126. Amin, S. A., Parker, M. S. & Armbrust, E. V. Interactions between diatoms and bacteria. Microbiol. Mol. Biol. Rev. 76, 667–684 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  127. Moustafa, A. et al. Transcriptome profiling of a toxic dinoflagellate reveals a gene-rich protist and a potential impact on gene expression due to bacterial presence. PLoS ONE 5, e9688 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  128. Choi, J. Y., Lee, T. W., Jeon, K. W. & Ahn, T. I. Evidence for symbiont-induced alteration of a host's gene expression: irreversible loss of SAM synthetase from Amoeba proteus. J. Eukaryot. Microbiol. 44, 412–419 (1997).

    Article  CAS  PubMed  Google Scholar 

  129. Seyedsayamdost, M. R., Carr, G., Kolter, R. & Clardy, J. Roseobacticides: small molecule modulators of an algal–bacterial symbiosis. J. Am. Chem. Soc. 133, 18343–18349 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  130. Woznica, A. et al. Bacterial lipids activate, synergize, and inhibit a developmental switch in choanoflagellates. Proc. Natl Acad. Sci. USA 113, 7894–7899 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  131. Van Etten, J. L., Lane, L. C. & Meints, R. H. Viruses and viruslike particles of eukaryotic algae. Microbiol. Rev. 55, 586–620 (1991).

    CAS  PubMed  PubMed Central  Google Scholar 

  132. Massana, R., Del Campo, J., Dinter, C. & Sommaruga, R. Crash of a population of the marine heterotrophic flagellate Cafeteria roenbergensis by viral infection. Environ. Microbiol. 9, 2660–2669 (2007).

    Article  CAS  PubMed  Google Scholar 

  133. Hovde, B. T. et al. Genome sequence and transcriptome analyses of Chrysochromulina tobin: metabolic tools for enhanced algal fitness in the prominent Order Prymnesiales (Haptophyceae). PLoS Genet. 11, e1005469 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  134. Rokitta, S. D., von Dassow, P., Rost, B. & John, U. P- and N-depletion trigger similar cellular responses to promote senescence in eukaryotic phytoplankton. Front. Mar. Sci. 3, 109 (2016).

    Article  Google Scholar 

  135. Morgan-Smith, D., Clouse, M. A., Herndl, G. J. & Bochdansky, A. B. Diversity and distribution of microbial eukaryotes in the deep tropical and subtropical North Atlantic Ocean. Deep Sea Res. Part I : Oceanogr. Res. Pap. 78, 58–69 (2013).

    Article  CAS  Google Scholar 

  136. Farnelid, H. M., Turk-Kubo, K. A. & Zehr, J. P. Identification of associations between bacterioplankton and photosynthetic picoeukaryotes in coastal waters. Front. Microbiol. 7, 339 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  137. Yoon, H. S. et al. Single-cell genomics reveals organismal interactions in uncultivated marine protists. Science 332, 714–717 (2011). The application of single-cell genomes is beginning to reveal the relationships among microbes.

    Article  CAS  PubMed  Google Scholar 

  138. Veluchamy, A. et al. Insights into the role of DNA methylation in diatoms by genome-wide profiling in Phaeodactylum tricornutum. Nat. Commun. 4, 2091 (2013).

    Article  CAS  PubMed  Google Scholar 

  139. Lovén, J. et al. Revisiting global gene expression analysis. Cell 151, 476–482 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  140. Nunn, B. L. et al. Diatom proteomics reveals unique acclimation strategies to mitigate Fe limitation. PLoS ONE 8, e75653 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  141. Poulson-Ellestad, K. L. et al. Metabolomics and proteomics reveal impacts of chemically mediated competition on marine plankton. Proc. Natl Acad. Sci. USA 111, 9009–9014 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  142. Aksoy, S. & Initiative, I. G. G. Genome sequence of the tsetse fly (Glossina morsitans): vector of african trypanosomiasis. Science 344, 380–386 (2014).

    Article  CAS  Google Scholar 

  143. Fonnes Flaten, G. A. et al. Studies of the microbial P-cycle during a Lagrangian phosphate-addition experiment in the Eastern Mediterranean. Deep Sea Res. Part 2 : Top. Stud. Oceanogr. 52, 2928–2943 (2005).

    Article  CAS  Google Scholar 

  144. Strong, A., Chisholm, S., Miller, C. & Cullen, J. Ocean fertilization: time to move on. Nature 461, 347–348 (2009).

    Article  CAS  PubMed  Google Scholar 

  145. Tekle, Y. I., Wegener Parfrey, L. & Katz, L. A. Molecular data are transforming hypotheses on the origin and diversification of eukaryotes. Bioscience 59, 471–481 (2009).

    Article  PubMed  Google Scholar 

  146. Woese, C. R. Interpreting the universal phylogenetic tree. Proc. Natl Acad. Sci. USA 97, 8392–8396 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  147. Decelle, J., Colin, S. & Forster, R. A. in Marine Protists: Diversity and Dynamics (eds Ohtsuka, S., Suzaki, T., Horiguchi, T., Suzuki, N. & Not, F.) 465–500 (Springer, 2015).

    Book  Google Scholar 

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Acknowledgements

The authors are grateful to the staff of the National Center for Genome Resources (NCGR; Santa Fe, New Mexico, USA) who assisted with sequencing (R. Bharti, J. Jacobi, J. Martinez, S. Nelson, P. Ngam and P. Umale), bioinformatics (C. Cameron, J. Crow, R. Kramer and K. Schilling) and software (N. Miller and K. Seal). They thank V. Chandler for input and guidance on the MMETSP and A. Lie for assistance with the figures. This research was funded in part by the Gordon and Betty Moore Foundation, through grants GBMF2637 to the NCGR and GBMF3111 to the National Center for Marine Algae and Microbiota (NCMA; East Boothbay, Maine, USA). Preparation of the manuscript was supported in part by a grant from the Simons Foundation (grant P49802 to D.A.C.).

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Glossary

Phototrophy

A nutritional mode that involves the use of light for the production of organic carbon and the acquisition of energy.

Phytoplankton

Planktonic protists that use phototrophy as their nutritional mode. The term has ecological importance but little phylogenetic importance because the behaviour occurs across many lineages of protists.

Heterotrophy

A nutritional mode that involves the use of preformed organic matter for the acquisition of carbon and energy.

Protozoa

Protists that are not photosynthetic, but are instead dependent on the ingestion of preformed organic matter (usually prey) for their nutrition. This older term is still in use; 'heterotrophic protists' is used synonymously.

Parasitoids

Protists that exhibit a parasitic lifestyle, infecting other protists or multicellular organisms. Parasitoids are typically differentiated from parasites by the fact that parasitoids, unlike parasites, always kill their hosts.

Metazoa

Multicellular, eukaryotic organisms (animals) that have differentiated cells and tissues.

Mixotrophy

A nutritional mode in which an individual cell can use both inorganic and preformed organic sources of carbon and nutrients for growth. In protists, mixotrophy is generally accomplished by combining heterotrophy with a photosynthetic ability acquired through chloroplasts, kleptoplastidy or harbouring endosymbiotic algae.

Primary production

The photosynthetic production of organic carbon, carried out by a wide variety of protists, macroalgae and plants.

Metatranscriptomes

Collections of all the transcriptomes (all RNA transcripts) present in communities of microorganisms; a metatranscriptome of a community is derived from RNA extraction and purification, reverse transcription of RNA to cDNA and sequencing of the resulting cDNA.

Metagenomes

Collections of all the DNA present in communities of microorganisms, representing all the genetic potential of the communities. The metagenome of a community can be used to reconstruct the genomes of the individual species comprising that community, thus assigning specific metabolic roles to those taxa.

Dinoflagellates

Members of a major, flagellated protistan lineage (the class Dinophyta, in the supergroup Alveolata) containing phototrophic, heterotrophic and mixotrophic (kleptoplastidic) species. Numerous photosynthetic and mixotrophic dinoflagellates are harmful and produce toxic algal blooms that have traditionally been called red tides.

Amoebozoa

A protist supergroup that includes many small amoeboid forms and the slime moulds.

Rhizaria

A large protist supergroup that includes ecologically important, large amoeboid forms (radiolaria and foraminifera) and the Cercozoa.

Stramenopiles

A diverse protist supergroup of phototrophic, heterotrophic and mixotrophic (phagotrophic phytoflagellates) species characterized by the presence of two flagella of unequal length and structure in their motile life stages. The supergroup includes the brown algae, the chrysophytes, the diatoms and other important groups. The term is generally used synonymously with heterokonts.

Alveolata

A supergroup that includes three important groups of protists: the dinoflagellates, the ciliates and the parasitic apicomplexans. The defining characteristic of the Alveolata is the presence of alveoli (flattened vesicles beneath the cell wall).

Glaucophytes

(Also known as glaucocystophytes). Members of the class Glaucocystophyceae, a small algal clade that is grouped together with the green algae and land plants in the supergroup Archaeplastida.

Euglenids

Members of the phylum Euglenida (in the supergroup Excavata). Free-living euglenids include phototrophic, heterotrophic and mixotrophic species, and a few notable parasites of animals.

Diatoms

Members of the phylum Bacillariophyta (in the supergroup Stramenopiles), a clade that is characterized by siliceous cell walls.

Haptophytes

Members of an algal group that encompasses prymnesiophytes (supergroup unresolved), including the bloom-forming species of the genus Phaeocystis as well as globally and biogeochemically important forms such as the coccolithophorids, which often bear calcium carbonate plates (coccoliths).

Cryptophyte

A member of the class Cryptophyta (supergroup unresolved); this is a group of small, flagellated protists that contains mostly photosynthetic forms but also mixotrophic and heterotrophic species. The photosynthetic species have plastids that contain phycobiliprotein pigments and are derived from red algae.

Chlorarachniophyte

A member of a group of algae (Chlorarachniophyceae) that are often mixotrophic. These species are also often amoeboid in form and are placed in the supergroup Rhizaria within the Cercozoa, together with large amoeboid forms, such as radiolaria and foraminifera.

Nucleomorph

A vestigial nucleus that is associated with plastids in some protists. They are derived from the engulfment and reduction of a eukaryotic endosymbiont.

Chromatophore

(In this Review:) An endosymbiotic cyanobacterium with a reduced genome. In the protist Paulinella chromatophora, this structure is considered an early stage of chloroplast acquisition.

Plastid

One of several types of cyanobacterium-derived, double-membrane-bound organelles that are present in many protists; an example is the chloroplast.

Prasinophyte

A type of green alga (phylum Chlorophyta, supergroup Archaeplastida). Prasinophytes are important primary producers in freshwater and marine ecosystems.

Autecologies

The ecologies of individual species and their interactions with the surrounding environment and co-occurring species.

Allelopathy

The production of growth-inhibiting chemicals by one species to target competing species. The term is commonly used in reference to chemical warfare among co-occurring phytoplankton.

High-nitrate low-chorophyll regions

(HNLC regions). Regions of the global ocean in which inorganic nitrogen does not limit phytoplankton growth, and other elements (most notably iron) limit the rate and amount of primary production.

Quantitative metabolic fingerprints

(QMFs). Comparisons of the relative expression levels of genes or gene families for a species under different environmental conditions or for different species under the same conditions. The fingerprints can indicate specific pathways that are upregulated or downregulated, and can thus provide insight into the metabolic responses of the organism.

Kleptoplastic

Able to ingest and partially digest photosynthetic prey, but retain the chloroplasts from the prey in a functional state, usually for periods of days to a few weeks.

Ciliates

Members of the phylum Ciliophora (supergroup Alveolata), a monophyletic group of heterotrophic and mixotrophic (kleptoplastidic) protists characterized by the presence of cilia that are used for motility and feeding. The ciliates are major consumers of phytoplankton, bacteria and other microorganisms.

Phagotrophy

A mode of nutrition that is characterized by the engulfment and digestion of particulate material, usually microbial prey.

Osmotrophy

A mode of nutrition that is characterized by the absorption and utilization of dissolved organic compounds.

Chrysophytes

Small, flagellated algal protists of the class Chrysophyceae (supergroup Stramenopiles), which contains photosynthetic, heterotrophic and mixotrophic species. Chloroplast-bearing species were previously referred to as golden-brown algae, an imprecise term no longer used by specialists.

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Caron, D., Alexander, H., Allen, A. et al. Probing the evolution, ecology and physiology of marine protists using transcriptomics. Nat Rev Microbiol 15, 6–20 (2017). https://doi.org/10.1038/nrmicro.2016.160

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