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

Abstract

Diatom primary productivity is tightly coupled with carbon export through the ballasted nature of the silica-based cell wall, linking the oceanic silicon and carbon cycles. However, despite low productivity, iron (Fe)-limited regimes are considered ‘hot spots’ of diatom silica burial with enhanced carbon export efficiency, raising questions about the mechanisms driving the biogeochemistry of these regions. Marine viruses are classically recognized as catalysts of remineralization through host lysis, short-circuiting the trophic transfer of carbon and facilitating the retention of dissolved organic matter and associated elements in the surface ocean. Here we used metatranscriptomic analysis of diatoms and associated viruses, along with a suite of physiological and geochemical metrics, to study the interaction between diatoms and viruses in Fe-limited regimes of the northeast Pacific. We found low cell-associated diatom virus diversity and abundance in a chronically Fe-limited region of the subarctic northeast Pacific. In a coastal upwelling region of the California Current, transient iron limitation also substantially reduced viral replication. These observations were recapitulated in Fe-limited cultures of the bloom-forming, centric diatom, Chaetoceros tenuissimus, which exhibited delayed virus-mediated mortality in addition to reduced viral replication. We suggest Fe-limited diatoms escape viral lysis and subsequent remineralization in the surface ocean, providing an additional mechanism contributing to enhanced carbon export efficiency and silica burial in Fe-limited oceanic regimes.

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Fig. 1: Biogeochemical, physiological and molecular characteristics of initial phytoplankton communities in the northeast Pacific.
Fig. 2: Metatranscriptomic analysis of cell-associated diatom viruses.
Fig. 3: Diatom molecular response and cell-associated diatom virus abundance during Fe limitation at S2.
Fig. 4: Diatom host–virus dynamics in Fe-limited C. tenuissimus.

Data availability

All cruise-related data are publicly available at the Biological & Chemical Oceanography Data Management Office (CUZ: project number 559966, https://www.bco-dmo.org/deployment/559966; Line P: http://www.waterproperties.ca/linep/2015-009/index.php). Metatranscriptome sequencing data are available in the NCBI sequence read archive (SRA) under the BioProject accession numbers PRJNA320398 and PRJNA388329. Assembled contigs, read counts and functional annotation of contigs are available at http://marchettilab.web.unc.edu/data. All data generated or analysed during this study are included in this published article and its Supplementary Information files. Source data are provided with this paper.

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Acknowledgements

We would like to thank the captain and the crew of the RV Melville (MV1405) and the Canadian Coast Guard Ship J. P. Tully (Line P 2015-09), as well as G. Smith, F. Kuzminov, K. Ellis and T. Coale for technical assistance during the cruise. Thank you to Y. Tomaru for providing the laboratory diatom host-virus systems, K. Bondoc and B. Knowles for useful discussions on statistical analyses and K. D. Bidle for thoughtful feedback on the manuscript. This work was supported by grants from the National Science Foundation (OCE-1333929 to K.T., OCE-1334387 to M.A.B., OCE-1334935 to A.M., OCE-1259776 to K.W.B. and OCE-1334632 to B.S.T.) and a postdoctoral fellowship to C.F.K. from the Simons Foundation (SF 548156). Salary support for C.F.K. was also provided by the Institute of Earth, Ocean and Atmospheric Sciences at Rutgers University, the Rappaport Fund for Advanced Studies and Israel’s Council for Higher Education.

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Authors

Contributions

C.F.K. and K.T. conceived the project, designed the laboratory experiments and wrote the manuscript. C.F.K. performed metatranscriptome and statistical analyses. C.F.K. conducted the laboratory culture-based experiments. J.M. and J.R.L. provided technical support on laboratory experiments. M.M. assisted with RdRp phylogenetic analyses. K.T., M.A.B., N.R.C., M.M., C.P.T., A.M., B.S.T. and K.W.B. participated, collected and analysed samples on the CUZ cruise; B.S.T. and N.R.C. participated, collected and analysed samples on the Line P cruise. A.M., N.R.C. and R.H.L. extracted the RNA and generated the metatranscriptome data. All authors provided comments on the manuscript.

Corresponding authors

Correspondence to Chana F. Kranzler or Kimberlee Thamatrakoln.

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The authors declare no competing interests.

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Peer review information Nature Geoscience thanks Erin Bertrand, Alex Poulton and the other, anonymous, reviewer(s) for their contribution to the peer review of this work. Primary Handling Editors: Clare Davis; Xujia Jiang.

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Extended data

Extended Data Fig. 1 Bulk parameters measured during incubations at each site.

a, Size-fractionated chlorophyll a (>5 µm; μg L−1), b, biogenic silica (μM), and c, maximum photochemical quantum yield of photosystem II (photosynthetic efficiency; Fv/Fm) throughout each incubation. Treatments included an initial sample (t0; open), and unamended Control (Ctrl; yellow), DFB (blue) and +Fe (orange). d, Fold-change in chlorophyll a (open bars) and biogenic silica (filled bars) between +Fe and Ctrl treatments at each timepoint. Note that at sites S2 and P4, 15 μM of Si(OH)4 and 10 µM of NO3 were added, respectively, to all treatments due to low initial concentrations (Si(OH)4 at S2 < 4.7 μM; NO3 at P4 < 1.5 μM). Mean and standard error of triplicate incubations are shown along with individual replicates (diamonds). Statistical significance of the community response to iron addition is depicted (panels a-c) for each time point with ***P < 0.001, **P < 0.01, *P < 0.05 by analysis of variance (ANOVA) followed by Tukey’s HSD post hoc test. Additional statistical analysis is available in Supplementary Data 2. Source data

Extended Data Fig. 2 Silicon stress during incubation experiments at each site.

Kinetic limitation of Si uptake, or Si stress (Vamb:Venh), at each site for initial samples (t0; open diamonds) and unamended Control (Ctrl; yellow), DFB (blue) and +Fe (orange) treatments throughout each incubation experiment. Each point represents a distinct treatment (color) and time point (symbol) within each incubation (diamonds, t0; circles, t1, 24–48 h; triangles, t2, 48–96 h). See methods and Supplementary Fig. 1 for individual time points. Values approaching zero are indicative of severe Si stress and values ~1 are indicative of silicon replete populations. The boxes depict the median (horizontal line) and upper and lower quartiles of the data with whiskers encompassing data points within 1.5× of the interquartile range. ***P < 0.001 by Kruskal-Wallis with Dunn’s multiple comparison test. No Si stress data was collected during the P4 and P26 incubations, or at t2 in the S1 and S2 incubations for Ctrl and +Fe treatments. Source data

Extended Data Fig. 3 Phylogenetic analysis and size distribution of diatom virus-like contigs.

a, Maximum likelihood phylogenetic tree of RNA-dependent RNA polymerase (RdRp) amino acid sequences within the order Picornavirales and placement of homologous contigs identified in metatranscriptomes. Bootstrap values >50 are shown (100 replicates). Triangles denote sequences that fall within the family Marnaviridae with blue triangles denoting the genus Marnavirus, which is distinctly comprised of dinoflagellate viruses and red triangles identifying putative diatom viruses that were selected for downstream analysis. b, Size distribution (bp) of diatom virus-like contigs. The abbreviations, names and NCBI database accession numbers of the amino acid sequences used to construct the reference alignment are: AglaRNAV, Asterionellopsis glacialis RNA virus, BAP16719; CsfrRNAV, Chaetoceros socialis radians RNA virus 1, YP_002647032; RsRNAV, Rhizosolenia setigera RNA virus 01, YP_006732323; CtenRNAV01, C. tenuissimus RNA virus 01, YP_009505620; CtenRNAVII, C. tenuissimus RNA virus type-II, BAP99818; CspRNAV2, Chaetoceros species RNA virus 02, BAK40203; HaRNAV, Heterosigma akashiwo RNA virus, AAP97137; CPSMV, cowpea severe mosaic virus, NP_619518; BPMV, Bean pod mottle virus, NP_612349; PYFV, Parsnip yellow fleck virus, BAA03151; RTSV, Rice tungro spherical virus, NP_042507;SBV, Sacbrood virus, AIZ75645; PV, Human poliovirus 1, CAA24461; AIV, Aichi virus 1, ADN52312; BQCV, Black queen cell virus, NP_620564; TrV, Triatoma virus, NP_620562; CPV, Cricket paralysis virus, NP_647481; DCV, Drosophila C virus, NP_044945; TSV, Taura syndrome virus, NP_149057.

Extended Data Fig. 4 Temporal changes in cell-associated diatom viruses throughout each incubation.

Log2 fold change in diatom virus contig abundance (nCv) at t1 (circles, 24–48 h) or t2 (triangles, when present, 48–72 h) compared to t0 for Ctrl (yellow), DFB (blue) and +Fe (orange) treatments (n = 3), *P < 0.05 by a one-way analysis of variance (ANOVA) followed by a Tukey HSD post hoc test. The boxes depict the median (horizontal line) and upper and lower quartiles of the data with whiskers encompassing data points within 1.5× of the interquartile range. See methods and Supplementary Fig. 1 for individual time points (symbols) in each incubation.

Extended Data Fig. 5 Temporal changes in cell-associated diatom viruses throughout the S2 incubation.

a, Log2 fold change in diatom virus contig abundance (nCv) between t48 and t0 for Ctrl (yellow), DFB (blue) and +Fe (orange) treatments (n = 3), *P < 0.05 by a one-way analysis of variance (ANOVA) followed by a Tukey HSD post hoc test. The boxes depict the median (horizontal line) and upper and lower quartiles of the data with whiskers encompassing data points within 1.5× of the interquartile range. b, Heatmap of mean abundance for each diatom virus contig (nCv) identified in the initial (t0) sample and at t48 across the treatments for both high (top panel) and low abundance (bottom panel) contigs. Contigs that were below detection are depicted in white. c, Abundance (nCv) of each cell-associated diatom virus contig in Ctrl (left panel), DFB (middle panel) and +Fe (right panel) treatments at t48 vs t0. Mean ± standard error is shown (n = 3). Dotted lines denote unity-slope lines, indicating no difference between timepoints. Insets depict ‘high’ abundance contigs. In panels a and c, open and closed symbols denote ‘high’ and ‘low’ abundance diatom virus contigs, respectively.

Extended Data Fig. 6 Diagnosing iron limitation in Chaetoceros tenuissimus.

a, Specific growth rates (day−1), b, mean chlorophyll autofluorescence (RFU cell−1) and c, electron transport rates (e s−1 PSII−1) of C. tenuissimus cultures in replete (orange symbols) and Fe-limited (blue symbols) growth media. d, Cell abundance and e, maximum photochemical quantum yield of photosystem II (photosynthetic efficiency; Fv/Fm) during Fe-limitation (blue) and after Fe addition (orange) in an Fe ‘rescue’ experiment. Each independent biological replicate (n = 3) is shown by individual symbols with lines of best fit depicting a LOESS regression. f, cellular biogenic silica (µmol bSiO2 cell−1) and g, cellular antioxidant capacity (mM Trolox eq cell−1) of replete and iron-limited C. tenuissimus. Statistical significance was determined using an unpaired, two-sided t-test. Different symbols denote biologically independent replicates across six independent experiments. Source data

Extended Data Fig. 7 The impact of Fe limitation on diatom host-virus dynamics in laboratory cultures of Chaetoceros tenuissimus infected with CtenRNAV.

Host abundance in replete (orange circles) and Fe-limited (blue triangles), uninfected (open symbols) and infected (closed symbols) cultures with the single stranded (ss) RNA-containing virus, CtenRNAV. Individual symbols represent independent biological replicates (n = 3) with lines of best fit depicting a LOESS regression. Source data

Extended Data Fig. 8 A role for oxidative stress and reactive oxygen species during infection of Chaetoceros tenuissimus.

a, Host abundance and b, intracellular levels of reactive oxygen species (ROS; assessed by the diagnostic, fluorescent stain H2DCFDA in replete, uninfected (open, orange symbols/bars) and infected (closed, orange symbols/bars) C. tenuissimus cultures with CtenDNAV. Mean ± standard error is shown (n = 3). c, Host abundance and d, maximum photochemical quantum yield of photosystem II (photosynthetic efficiency; Fv/Fm) following addition of different doses of hydrogen peroxide (H2O2; 0-150 µM). Mean ± standard error is shown for biological duplicates. Due to the observed decrease in cell abundance and photosynthetic efficiency, followed by physiological recovery, 100 µM H2O2 was chosen for downstream infection experiments. Time course of e, host abundance and f, photosynthetic efficiency during viral infection with CtenDNAV of untreated control cultures (orange circles) and cultures pre-exposed to a sub- lethal dose of H2O2 (100 µM; blue squares) for uninfected (open symbols) and infected (closed symbols) cultures (n = 3). Data are representative of three independent experiments. Source data

Extended Data Table 1 Initial bulk parameters and underlying nutrient regime at each site

Supplementary information

Supplementary Data 1

Data 1a Taxonomic assignment of mapped reads: taxa. Data 1b Taxonomic assignment of mapped reads: diatom genera. Data 2 Summary of statistical analyses. Data 3a Diatom virus TBLASTN hits. Data 3b Putative diatom virus contig abundance. Data 4a Differentially expressed contigs_S2_DFB/Fe. Data 4b Differentially expressed contigs_S2_Fe/Ctrl. Data 4c Differentially expressed contigs_S2_DFB/Ctrl.

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Kranzler, C.F., Brzezinski, M.A., Cohen, N.R. et al. Impaired viral infection and reduced mortality of diatoms in iron-limited oceanic regions. Nat. Geosci. 14, 231–237 (2021). https://doi.org/10.1038/s41561-021-00711-6

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