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.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 12 print issues and online access
$209.00 per year
only $17.42 per issue
Rent or buy this article
Prices vary by article type
from$1.95
to$39.95
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Whittaker, R. H. New concepts of kingdoms of organisms. Science 163, 150–160 (1969).
Ohtsuka, S., Suzaki, T., Horiguchi, T., Suzuki, N. & Not, F. (eds) Marine Protists (Springer, 2015).
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.
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.
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.
del Campo, J. et al. The others: our biased perspective of eukaryotic genomes. Trends Ecol. Evol. 29, 252–259 (2014).
Cuvelier, M. L. et al. Targeted metagenomics and ecology of globally important uncultured eukaryotic phytoplankton. Proc. Natl Acad. Sci. USA 107, 14679–14684 (2010).
Caron, D. A. Towards a molecular taxonomy for protists: benefits, risks and applications in plankton ecology. J. Eukaryot. Microbiol. 60, 407–413 (2013).
Fenchel, T. & Finlay, B. J. The ubiquity of small species: patterns of local and global diversity. Bioscience 54, 777–784 (2004).
Foissner, W. Biogeography and dispersal of micro-organisms: a review emphasizing protists. Acta Protozool. 45, 111–136 (2006).
Guillou, L. et al. Widespread occurrence and genetic diversity of marine parasitoids belonging to Syndiniales (Alveolata). Environ. Microbiol. 10, 3349–3365 (2008).
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).
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).
Logares, R. et al. Patterns of rare and abundant marine microbial eukaryotes. Curr. Biol. 24, 813–821 (2014).
Lynch, M. D. J. & Neufeld, J. D. Ecology and expolaration of the rare biosphere. Nat. Rev. Microbiol. 13, 217–229 (2015).
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).
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).
Pernice, M. C. et al. Global abundance of planktonic heterotrophic protists in the deep ocean. ISME J. 9, 782–792 (2015).
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).
Sogin, M. L. Early evolution and the origin of eukaryotes. Curr. Opin. Genet. Dev. 1, 457–463 (1991).
Simpson, A. G. B. & Roger, A. J. The real 'kingdoms' of eukaryotes. Curr. Biol. 14, R693–R696 (2004).
Baldauf, S. L. An overview of the phylogeny and diversity of eukaryotes. J. Systemat. Evol. 46, 263–273 (2008).
Pawlowski, J. & Burki, F. Untangling the phylogeny of amoeboid prtotist. J. Eukaryot. Microbiol. 56, 16–25 (2009).
Burki, F. et al. Phylogenomics reshuffles the eukaryotic supergroups. PLoS ONE 8, E790 (2007).
Adl, S. M. et al. The revised classification of eukaryotes. J. Eukaryot. Microbiol. 59, 429–514 (2012).
Burki, F. The eukaryotic tree of life from a global phylogenomic perspective. Cold Spring Harb. Perspect. Biol. 6, a016147 (2014).
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).
Koonin, E. V. The origin and early evolution of eukaryotes in the light of phylogenomics. Genome Biol. 11, 209 (2010).
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).
Gould, S. B., Waller, R. F. & McFadden, G. I. Plastid evolution. Annu. Rev. Plant Biol. 59, 491–517 (2008).
Keeling, P. J. The number, speed, and impact of plastid endosymbioses on eukaryotic evolution. Annu. Rev. Plant Biol. 64, 583–607 (2013).
Deschamps, P. & Moreira, D. Reevaluating the green contribution to diatom genomes. Genome Biol. Evol. 4, 683–688 (2012).
Burki, F. et al. Endosymbiotic gene transfer in tertiary plastid-containing dinoflagellates. Eukaryot. Cell 13, 246–255 (2014).
Slamovits, C. H. & Keeling, P. J. Plastid-derived genes in the non-photosynthetic alveolate Oxyrrhis marina. Mol. Biol. Evol. 25, 1297–1306 (2008).
Moore, C. E. & Archibald, J. M. Nucleomorph genomes. Annu. Rev. Genet. 43, 251–264 (2009).
Curtis, B. A. et al. Algal genomes reveal evolutionary mosaicism and the fate of nucleomorphs. Nature 492, 59–65 (2012).
Nakayama, T. & Ishida, K.-I. Another acquisition of a primary photosynthetic organelle is underway in Paulinella chromatophora. Curr. Biol. 19, R284–R285 (2009).
Nowack, E. C. et al. Endosymbiotic gene transfer and transcriptional regulation of transferred genes in Paulinella chromatophora. Mol. Biol. Evol. 28, 407–422 (2011).
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).
Nakayama, T. & Archibald, J. M. Evolving a photosynthetic organelle. BMC Biol. 10, 34 (2012).
Estrela, S., Kerr, B. & Morris, J. J. Transitions in individuality through symbiosis. Curr. Opin. Microbiol. 31, 191–198 (2016).
Lin, S. et al. The Symbiodinium kawagutii genome illuminates dinoflagellate gene expression and coral symbiosis. Science 350, 691–694 (2015).
Bayer, T. et al. Symbiodinium transcriptomes: genome insights into the dinoflagellate symbionts of reef-building corals. PLoS ONE 7, e35269 (2012).
Biard, T. et al. In situ imaging reveals the biomass of large protists in the global ocean. Nature 532, 504–507 (2016).
Decelle, J. et al. An original mode of symbiosis in open ocean plankton. Proc. Natl Acad. Sci. USA 109, 18000–18005 (2012).
Balzano, S. et al. Transcriptome analyses to investigate symbiotic relationships between marine protists. Front. Microbiol. 6, 98 (2015).
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).
Chen, M. M., Chory, J. & Fankhauser, C. Light signal transduction in higher plants. Annu. Rev. Genet. 38, 87–117 (2004).
Falciatore, A. & Bowler, C. The evolution and function of blue and red light photoreceptors. Curr. Top. Dev. Biol. 68, 317–350 (2005).
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).
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).
Worden, A. Z. et al. Green evolution and dynamic adaptations revealed by genomes of the marine picoeukaryotes Micromonas. Science 324, 268–272 (2009).
Duanmu, D. et al. Marine algae and land plants share conserved phytochrome signaling systems. Proc. Natl Acad. Sci. USA 111, 15827–15832 (2014).
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).
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).
Armbrust, E. The life of diatoms in the world's oceans. Nature 459, 185–192 (2009).
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).
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).
Gobler, C. J. et al. Niche of harmful alga Aureococcus anophagefferens revealed through ecogenomics. Proc. Natl Acad. Sci USA. 108, 4352–4357 (2011).
Shrestha, R. P. et al. Whole transcriptome analysis of the silicon response of the diatom Thalassiosira pseudonana. BMC Genomics 13, 499 (2012).
Schmollinger, S. et al. Nitrogen-sparing mechanisms in Chlamydomonas affect the transcriptome, the proteome, and photosynthetic metabolism. Plant Cell 26, 1410–1435 (2014).
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).
Whitney, L. P. & Lomas, M. W. Growth on ATP elicits a P-stress response in the picoeukaryote Micromonas pusilla. PLoS ONE 11, e0155158 (2016).
Monnier, A. et al. Orchestrated transcription of biological processes in the marine picoeukaryote Ostreococcus exposed to light/dark cycles. BMC Genomics 11, 192 (2010).
Poliner, E. et al. Transcriptional coordination of physiological responses in Nannochloropsis oceanica CCMP1779 under light/dark cycles. Plant J. 83, 1097–1113 (2015).
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).
Allen, A. E. et al. Evolution and metabolic significance of the urea cycle in photosynthetic diatoms. Nature 473, 203–207 (2011).
Armbrust, E. V. et al. The genome of the diatom Thalassiosira pseudonana: ecology, evolution, and metabolism. Science 306, 79–86 (2004).
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).
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).
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).
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).
Hackett, J. D., Anderson, D. M., Erdner, D. L. & Bhattacharya, D. Dinoflagellates: a remarkable evolutionary experiment. Am. J. Bot. 91, 1523–1534 (2004).
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).
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).
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).
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).
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).
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).
Smetacek, V. A watery arms race. Nature 411, 745 (2001).
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).
Manning, S. R. & La Claire, J. W. Prymnesins: toxic metabolites of the golden alga, Prymnesium parvum Carter (Haptophyta). Mar. Drugs 8, 678–704 (2010).
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).
Stüken, A. et al. Discovery of nuclear-encoded genes for the neurotoxin saxitoxin in dinoflagellates. PLoS ONE 6, e20096 (2011).
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).
Liu, Z. et al. Changes in gene expression of Prymnesium parvum due to nitrogen and phosphorus limitation. Front. Microbiol. 6, 631 (2015).
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).
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).
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).
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).
Boyd, P. W. et al. A mesoscale phytoplankton bloom in the polar Southern Ocean stimulated by iron fertilization. Nature 407, 695–702 (2000).
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.
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).
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).
Ashworth, J. et al. Genome-wide diel growth state transitions in the diatom Thalassiosira pseudonana. Proc. Natl Acad. Sci. USA 110, 7518–7523 (2013).
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.
Alexander, H. et al. Functional group-specific traits drive phytoplankton dynamics in the oligotrophic ocean. Proc. Natl Acad. Sci. USA 112, E5972–E5979 (2015).
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).
Read, B. A. et al. Pan genome of the phytoplankton Emiliania underpins its global distribution. Nature 499, 209–213 (2013).
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).
Benitez-Nelson, C. R. et al. Mesoscale eddies drive increased silica export in the subtropical Pacific Ocean. Science 316, 1017–1021 (2007).
Lewin, J. C. Heterotrophy in diatoms. J. Gen. Microbiol. 9, 305–313 (1953).
Croft, M. T., Warren, M. J. & Smith, A. G. Algae need their vitamins. Eukaryot. Cell 5, 1175–1183 (2006).
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).
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.
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).
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).
Stoecker, D. K. Mixotrophy among dinoflagellates. J. Eukaryot. Microbiol. 46, 397–401 (1999).
Johnson, M. D. Acquired phototrophy in ciliates: a review of cellular interactions and structural adaptations. J. Eukaryot. Microbiol. 58, 185–195 (2011).
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).
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).
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.
Sillo, A. et al. Genome-wide transcriptional changes induced by phagocytosis or growth on bacteria in Dictyostelium. BMC Genomics 9, 291 (2008).
Liu, Z. et al. Gene expression in the mixotrophic prymnesiophyte, Prymnesium parvum, responds to prey availability. Front. Microbiol. 6, 319 (2015).
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).
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).
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).
Guo, Z., Zhang, H. & Lin, S. Light-promoted rhodopsin expression and starvation survival in the marine dinoflagellate Oxyrrhis marina. PLoS ONE 9, e114941 (2014).
Amin, S. A. et al. Interaction and signalling between a cosmopolitan phytoplankton and associated bacteria. Nature 522, 98–101 (2015).
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.
Sapp, M. et al. Species-apecific bacterial communities in the phycosphere of microalgae? Microb. Ecol. 53, 683–699 (2007).
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).
Durham, B. P. et al. Cryptic carbon and sulfur cycling between surface ocean plankton. Proc. Natl Acad. Sci. USA 112, 453–457 (2015).
Thompson, A. W. et al. Unicellular cyanobacterium symbiotic with a single-celled eukaryotic alga. Science 337, 1546–1550 (2012).
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).
Amin, S. A., Parker, M. S. & Armbrust, E. V. Interactions between diatoms and bacteria. Microbiol. Mol. Biol. Rev. 76, 667–684 (2012).
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).
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).
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).
Woznica, A. et al. Bacterial lipids activate, synergize, and inhibit a developmental switch in choanoflagellates. Proc. Natl Acad. Sci. USA 113, 7894–7899 (2016).
Van Etten, J. L., Lane, L. C. & Meints, R. H. Viruses and viruslike particles of eukaryotic algae. Microbiol. Rev. 55, 586–620 (1991).
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).
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).
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).
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).
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).
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.
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).
Lovén, J. et al. Revisiting global gene expression analysis. Cell 151, 476–482 (2012).
Nunn, B. L. et al. Diatom proteomics reveals unique acclimation strategies to mitigate Fe limitation. PLoS ONE 8, e75653 (2013).
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).
Aksoy, S. & Initiative, I. G. G. Genome sequence of the tsetse fly (Glossina morsitans): vector of african trypanosomiasis. Science 344, 380–386 (2014).
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).
Strong, A., Chisholm, S., Miller, C. & Cullen, J. Ocean fertilization: time to move on. Nature 461, 347–348 (2009).
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).
Woese, C. R. Interpreting the universal phylogenetic tree. Proc. Natl Acad. Sci. USA 97, 8392–8396 (2000).
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).
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.).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing financial interests.
Related links
Supplementary information
Supplementary information S1 (box)
A list of participants and informal collaborators in the MMETSP (alphabetical order of first affiliate) (PDF 129 kb)
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.
Rights and permissions
About this article
Cite this article
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
Published:
Issue Date:
DOI: https://doi.org/10.1038/nrmicro.2016.160
This article is cited by
-
Reverse engineering environmental metatranscriptomes clarifies best practices for eukaryotic assembly
BMC Bioinformatics (2023)
-
Gene expression dynamics of natural assemblages of heterotrophic flagellates during bacterivory
Microbiome (2023)
-
Plastoquinone synthesis inhibition by tetrabromo biphenyldiol as a widespread algicidal mechanism of marine bacteria
The ISME Journal (2023)
-
MarFERReT, an open-source, version-controlled reference library of marine microbial eukaryote functional genes
Scientific Data (2023)
-
Linking extreme seasonality and gene expression in Arctic marine protists
Scientific Reports (2023)