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Impaired viral infection and reduced mortality of diatoms in iron-limited oceanic regions

  • 1.

    Nelson, D. M., Tréguer, P., Brzezinski, M. A., Leynaert, A. & Quéguiner, B. Production and dissolution of biogenic silica in the ocean: revised global estimates, comparison with regional data and relationship to biogenic sedimentation. Glob. Biogeochem. Cycles 9, 359–372 (1995).

    Google Scholar 

  • 2.

    Smetacek, V. et al. Deep carbon export from a Southern Ocean iron-fertilized diatom bloom. Nature 487, 313–319 (2012).

    Google Scholar 

  • 3.

    Hutchins, D. A., DiTullio, G. R., Zhang, Y. & Bruland, K. W. An iron limitation mosaic in the California upwelling regime. Limnol. Oceanogr. 43, 1037–1054 (1998).

    Google Scholar 

  • 4.

    Bruland, K. W., Rue, E. L. & Smith, G. J. Iron and macronutrients in California coastal upwelling regimes: implications for diatom blooms. Limnol. Oceanogr. 46, 1661–1674 (2001).

    Google Scholar 

  • 5.

    Boyd, P. W. et al. Mesoscale iron enrichment experiments 1993–2005: synthesis and future directions. Science 315, 612–617 (2007).

    Google Scholar 

  • 6.

    Brzezinski, M. A. et al. Enhanced silica ballasting from iron stress sustains carbon export in a frontal zone within the California Current. J. Geophys. Res. Oceans 120, 4654–4669 (2015).

    Google Scholar 

  • 7.

    Arteaga, L. A., Pahlow, M., Bushinsky, S. M. & Sarmiento, J. L. Nutrient controls on export production in the Southern Ocean. Glob. Biogeochem. Cycles 33, 942–956 (2019).

    Google Scholar 

  • 8.

    Stukel, M. R. & Barbeau, K. A. Investigating the nutrient landscape in a coastal upwelling region and its relationship to the biological carbon pump. Geophys. Res. Lett. 47, e2020GL087351 (2020).

    Google Scholar 

  • 9.

    Hutchins, D. A. & Bruland, K. W. Iron-limited diatom growth and Si:N uptake ratios in a coastal upwelling regime. Nature 393, 561–564 (1998).

    Google Scholar 

  • 10.

    Takeda, S. Influence of iron availability on nutrient consumption ratio of diatoms in oceanic waters. Nature 393, 774–777 (1998).

    Google Scholar 

  • 11.

    Pichevin, L. E., Ganeshram, R. S., Geibert, W., Thunell, R. & Hinton, R. Silica burial enhanced by iron limitation in oceanic upwelling margins. Nat. Geosci. 7, 541–546 (2014).

    Google Scholar 

  • 12.

    Brzezinski, M. A. et al. A switch from Si(OH)4 to NO3 depletion in the glacial Southern Ocean. Geophys. Res. Lett. 29, 1564 (2002).

  • 13.

    Matsumoto, K., Sarmiento, J. L. & Brzezinski, M. A. Silicic acid leakage from the Southern Ocean: a possible explanation for glacial atmospheric pCO2. Glob. Biogeochem. Cycles 16, 1031 (2002).

    Google Scholar 

  • 14.

    Sarmiento, J. L., Gruber, N., Brzezinski, M. A. & Dunne, J. P. High-latitude controls of thermocline nutrients and low latitude biological productivity. Nature 427, 56–60 (2004).

    Google Scholar 

  • 15.

    Fuhrman, J. A. Marine viruses and their biogeochemical and ecological effects. Nature 399, 541–548 (1999).

    Google Scholar 

  • 16.

    Suttle, C. A. Marine viruses—major players in the global ecosystem. Nat. Rev. Microbiol. 5, 801–812 (2007).

    Google Scholar 

  • 17.

    Wilhelm, S. W. & Suttle, C. A. Viruses and nutrient cycles in the sea: viruses play critical roles in the structure and function of aquatic food webs. Bioscience 49, 781–788 (1999).

    Google Scholar 

  • 18.

    Kranzler, C. F. et al. Silicon limitation facilitates virus infection and mortality of marine diatoms. Nat. Microbiol. 4, 1790–1797 (2019).

  • 19.

    Laber, C. P. et al. Coccolithovirus facilitation of carbon export in the North Atlantic. Nat. Microbiol. 3, 537–547 (2018).

    Google Scholar 

  • 20.

    Yamada, Y., Tomaru, Y., Fukuda, H. & Nagata, T. Aggregate formation during the viral lysis of a marine diatom. Front. Mar. Sci. 5, 167 (2018).

    Google Scholar 

  • 21.

    Pelusi, A. et al. Virus-induced spore formation as a defense mechanism in marine diatoms. New Phytol. 229, 2251–2259 (2020).

    Google Scholar 

  • 22.

    Johnson, K. S., Chavez, F. P. & Friederich, G. E. Continental-shelf sediment as a primary source of iron for coastal phytoplankton. Nature 398, 697–700 (1999).

    Google Scholar 

  • 23.

    Harrison, P. J. Station Papa time series: insights into ecosystem dynamics. J. Oceanogr. 58, 259–264 (2002).

    Google Scholar 

  • 24.

    Marchetti, A. et al. Development of a molecular-based index for assessing iron status in bloom-forming pennate diatoms. J. Phycol. 53, 820–832 (2017).

    Google Scholar 

  • 25.

    Cohen, N. R. et al. Diatom transcriptional and physiological responses to changes in iron bioavailability across ocean provinces. Front. Mar. Sci. 4, 360 (2017).

    Google Scholar 

  • 26.

    Lampe, R. H. et al. Different iron storage strategies among bloom-forming diatoms. Proc. Natl Acad. Sci. USA 115, E12275–E12284 (2018).

    Google Scholar 

  • 27.

    King, A. L. & Barbeau, K. Evidence for phytoplankton iron limitation in the southern California Current System. Mar. Ecol. Prog. Ser. 342, 91–103 (2007).

    Google Scholar 

  • 28.

    Boyd, P. & Harrison, P. J. Phytoplankton dynamics in the NE subarctic Pacific. Deep Sea Res. II 46, 2405–2432 (1999).

    Google Scholar 

  • 29.

    Till, C. P. et al. The iron limitation mosaic in the California Current System: factors governing Fe availability in the shelf/near-shelf region. Limnol. Oceanogr. 64, 109–123 (2019).

    Google Scholar 

  • 30.

    Gozzelino, R., Jeney, V. & Soares, M. P. Mechanisms of cell protection by heme oxygenase-1. Annu. Rev. Pharmacol. Toxicol. 50, 323–354 (2010).

    Google Scholar 

  • 31.

    Richaud, C. & Zabulon, G. The heme oxygenase gene (pbsA) in the red alga Rhodella violacea is discontinuous and transcriptionally activated during iron limitation. Proc. Natl Acad. Sci. USA 94, 11736–11741 (1997).

    Google Scholar 

  • 32.

    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).

    Google Scholar 

  • 33.

    Thamatrakoln, K., Korenovska, O., Niheu, A. K. & Bidle, K. D. Whole-genome expression analysis reveals a role for death-related genes in stress acclimation of the diatom Thalassiosira pseudonana. Environ. Microbiol. 14, 67–81 (2012).

    Google Scholar 

  • 34.

    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).

    Google Scholar 

  • 35.

    De La Rocha, C. L., Hutchins, D. A., Brzezinski, M. A. & Zhang, Y. Effects of iron and zinc deficiency on elemental composition and silica production by diatoms. Mar. Ecol. Prog. Ser. 195, 71–79 (2000).

    Google Scholar 

  • 36.

    Leynaert, A. et al. Effect of iron deficiency on diatom cell size and silicic acid uptake kinetics. Limnol. Oceanogr. 49, 1134–1143 (2004).

    Google Scholar 

  • 37.

    van Creveld, S. G., Rosenwasser, S., Levin, Y. & Vardi, A. Chronic iron limitation confers transient resistance to oxidative stress in marine diatoms. Plant Physiol. 172, 968–979 (2016).

    Google Scholar 

  • 38.

    Slagter, H. A., Gerringa, L. J. A. & Brussaard, C. P. D. Phytoplankton virus production negatively affected by iron limitation. Front. Mar. Sci. 3, 156 (2016).

    Google Scholar 

  • 39.

    Drakesmith, H. & Prentice, A. Viral infection and iron metabolism. Nat. Rev. Microbiol. 6, 541–552 (2008).

    Google Scholar 

  • 40.

    Weinbauer, M. G., Arrieta, J. M., Griebler, C. & Herndlb, G. J. Enhanced viral production and infection of bacterioplankton during an iron-induced phytoplankton bloom in the Southern Ocean. Limnol. Oceanogr. 54, 774–784 (2009).

    Google Scholar 

  • 41.

    Torres, M. A., Jones, J. D. G. & Dangl, J. L. Reactive oxygen species signaling in response to pathogens. Plant Physiol. 141, 373–378 (2006).

    Google Scholar 

  • 42.

    Sheyn, U., Rosenwasser, S., Ben-Dor, S., Porat, Z. & Vardi, A. Modulation of host ROS metabolism is essential for viral infection of a bloom-forming coccolithophore in the ocean. ISME J. 10, 1742–1754 (2016).

    Google Scholar 

  • 43.

    Hyodo, K., Hashimoto, K., Kuchitsu, K., Suzuki, N. & Okuno, T. Harnessing host ROS-generating machinery for the robust genome replication of a plant RNA virus. Proc. Natl Acad. Sci. USA 114, E1282–E1290 (2017).

    Google Scholar 

  • 44.

    Espinoza, J. A., Gonzalez, P. A. & Kalergis, A. M. Modulation of antiviral immunity by heme oxygenase-1. Am. J. Pathol. 187, 487–493 (2017).

    Google Scholar 

  • 45.

    Durkin, C. A. et al. Frustule-related gene transcription and the influence of diatom community composition on silica precipitation in an iron-limited environment. Limnol. Oceanogr. 57, 1619–1633 (2012).

    Google Scholar 

  • 46.

    Assmy, P. et al. Thick-shelled, grazer-protected diatoms decouple ocean carbon and silicon cycles in the iron-limited Antarctic Circumpolar Current. Proc. Natl Acad. Sci. USA 110, 20633–20638 (2013).

    Google Scholar 

  • 47.

    Kimura, K. & Tomaru, Y. Effects of temperature and salinity on diatom cell lysis by DNA and RNA viruses. Aquat. Microb. Ecol. 79, 79–83 (2017).

    Google Scholar 

  • 48.

    Thamatrakoln, K. et al. Light regulation of coccolithophore host–virus interactions. New Phytol. 221, 1289–1302 (2019).

    Google Scholar 

  • 49.

    Zimmerman, A. E. et al. Metabolic and biogeochemical consequences of viral infection in aquatic ecosystems. Nat. Rev. Microbiol. 18, 21–34 (2020).

    Google Scholar 

  • 50.

    Brzezinski, M. A. et al. Co-limitation of diatoms by iron and silicic acid in the equatorial Pacific. Deep Sea Res. II 58, 493–511 (2011).

    Google Scholar 

  • 51.

    Boyer, T. P. et al. World Ocean Database 2013 (NOAA Atlas, 2013).

  • 52.

    Krause, J. W. et al. The interaction of physical and biological factors drives phytoplankton spatial distribution in the northern California Current. Limnol. Oceanogr. 65, 1974–1989 (2020).

    Google Scholar 

  • 53.

    Krause, J. W., Nelson, D. M. & Brzezinski, M. A. Biogenic silica production and the diatom contribution to primary production and nitrate uptake in the eastern equatorial Pacific Ocean. Deep Sea Res. II 58, 434–448 (2011).

    Google Scholar 

  • 54.

    Brzezinski, M. A. & Phillips, D. R. Evaluation of 32Si as a tracer for measuring silica production rates in marine waters. Limnol. Oceanogr. 42, 856–865 (1997).

    Google Scholar 

  • 55.

    Nelson, D. M., Brzezinski, M. A., Sigmon, D. E. & Franck, V. M. A seasonal progression of Si limitation in the Pacific sector of the Southern Ocean. Deep Sea Res. II 48, 3973–3995 (2001).

    Google Scholar 

  • 56.

    Krause, J. W., Brzezinski, M. A., Villareal, T. A. & Wilson, C. Increased kinetic efficiency for silicic acid uptake as a driver of summer diatom blooms in the North Pacific subtropical gyre. Limnol. Oceanogr. 57, 1084–1098 (2012).

    Google Scholar 

  • 57.

    Birol, I. et al. De novo transcriptome assembly with ABySS. Bioinformatics 25, 2872–2877 (2009).

    Google Scholar 

  • 58.

    Robertson, G. et al. De novo assembly and analysis of RNA-seq data. Nat. Methods 7, 909–912 (2010).

    Google Scholar 

  • 59.

    Gremme, G., Steinbiss, S. & Kurtz, S. GenomeTools: a comprehensive software library for efficient processing of structured genome annotations. IEEE/ACM Trans. Comput. Biol. Bioinform. 10, 645–656 (2013).

    Google Scholar 

  • 60.

    Kanehisa, M., Furumichi, M., Tanabe, M., Sato, Y. & Morishima, K. KEGG: new perspectives on genomes, pathways, diseases and drugs. Nucleic Acids Res. 45, D353–D361 (2017).

    Google Scholar 

  • 61.

    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).

    Google Scholar 

  • 62.

    Patro, R., Duggal, G., Love, M. I., Irizarry, R. A. & Kingsford, C. Salmon provides fast and bias-aware quantification of transcript expression. Nat. Methods 14, 417–419 (2017).

    Google Scholar 

  • 63.

    R Core Team R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2013).

  • 64.

    Robinson, M. D., McCarthy, D. J. & Smyth, G. K. EdgeR: a bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26, 139–140 (2010).

    Google Scholar 

  • 65.

    Benjamini, Y. & Hochberg, Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. B 57, 289–300 (1995).

    Google Scholar 

  • 66.

    Wickham, H. ggplot2: Elegant Graphics for Data Analysis (Springer, 2016).

  • 67.

    Wagner, G. P., Kin, K. & Lynch, V. J. Measurement of mRNA abundance using RNA-seq data: RPKM measure is inconsistent among samples. Theory Biosci. 131, 281–285 (2012).

    Google Scholar 

  • 68.

    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).

    Google Scholar 

  • 69.

    Lampe, R. H. et al. Divergent gene expression among phytoplankton taxa in response to upwelling. Environ. Microbiol. 20, 3069–3082 (2018).

    Google Scholar 

  • 70.

    Warnes, G. R. et al. gplots: Various R Programming Tools for Plotting Data https://cran.r-project.org/web/packages/gplots/index.html (2019).

  • 71.

    Oksanen, J. et al. vegan: Community Ecology Package https://cran.r-project.org/web/packages/vegan/index.html (2019).

  • 72.

    Thompson, J. D., Higgins, D. G. & Gibson, T. J. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22, 4673–4680 (1994).

    Google Scholar 

  • 73.

    Kumar, S., Stecher, G. & Tamura, K. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol. Biol. Evol. 33, 1870–1874 (2016).

    Google Scholar 

  • 74.

    Stamatakis, A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312–1313 (2014).

    Google Scholar 

  • 75.

    Matsen, F. A., Kodner, R. B. & Armbrust, E. V. pplacer: linear time maximum-likelihood and Bayesian phylogenetic placement of sequences onto a fixed reference tree. BMC Bioinform. 11, 538 (2010).

    Google Scholar 

  • 76.

    Shirai, Y. et al. Isolation and characterization of a single-stranded RNA virus infecting the marine planktonic diatom Chaetoceros tenuissimus Meunier. Appl. Environ. Microbiol. 74, 4022–4027 (2008).

    Google Scholar 

  • 77.

    Chen, L.-M., Edelstein, T. & McLachlan, J. Bonnemaisonia hamifera Hariot in nature and in culture. J. Phycol. 5, 211–220 (1969).

    Google Scholar 

  • 78.

    Harrison, P. J., Waters, R. E. & Taylor, F. J. R. A broad spectrum artificial sea water medium for coastal and open ocean phytoplankton. J. Phycol. 16, 28–35 (1980).

    Google Scholar 

  • 79.

    Berges, J. A., Franklin, D. J. & Harrison, P. J. Evolution of an artificial seawater medium: improvements in enriched seawater, artificial water over the last two decades. J. Phycol. 37, 1138–1145 (2001).

    Google Scholar 

  • 80.

    Sunda, W. G., Price, N. M. & Morel, F. M. M. Trace metal ion buffers and their use in culture studies. Algal Cult. Tech. 4, 35–63 (2005).

    Google Scholar 

  • 81.

    Tomaru, Y., Shirai, Y., Toyoda, K. & Nagasaki, K. Isolation and characterization of a single-stranded DNA virus infecting the marine planktonic diatom Chaetoceros tenuissimus. Aquat. Microb. Ecol. 64, 175–184 (2011).

    Google Scholar 

  • 82.

    Parsons, T. R. A Manual of Chemical & Biological Methods for Seawater Analysis (Elsevier, 2013).

  • 83.

    Krause, J. W., Lomas, M. W. & Nelson, D. M. Biogenic silica at the Bermuda Atlantic time-series study site in the Sargasso Sea: temporal changes and their inferred controls based on a 15-year record. Glob. Biogeochem. Cycles 23, GB3004 (2009).

  • 84.

    Gorbunov, M. Y. & Falkowski, P. G. Fluorescence induction and relaxation (FIRe) technique and instrumentation for monitoring photosynthetic processes and primary production in aquatic ecosystems. In Photosynthesis: Fundamental Aspects to Global Perspectives—Proc. 13th International Congress of Photosynthesis (eds Van der Est, A. & Bruce, D.) 1029–1031 (Allen and Unwin, 2004).

  • 85.

    Suttle, C. A. in Handbook of Methods in Aquatic Microbial Ecology (eds Kemp, P. F. et al.) 121–134 (CRC Press, 1993).

  • 86.

    Klee, A. J. A computer program for the determination of most probable number and its confidence limits. J. Microbiol. Methods 18, 91–98 (1993).

    Google Scholar 


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