Research ArticleMarine Ecology

Unveiling the role and life strategies of viruses from the surface to the dark ocean

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Science Advances  06 Sep 2017:
Vol. 3, no. 9, e1602565
DOI: 10.1126/sciadv.1602565
  • Fig. 1 World map showing the location of the Malaspina sampling stations and depth-integrated viral abundance.

    (A) Map of the Malaspina 2010 cruise showing the 120 sampling stations. Colors indicate the three different oceanic regions (Atlantic, Indian, and Pacific). Average values of depth-integrated viral abundance and their SEs are shown for the three main oceanic regions in the (B) epipelagic (0 to 200 m), (C) mesopelagic (200 to 1000 m), and (D) bathypelagic (1000 to 4000 m) layers. In (E), all depth average data are summarized. ATL, Atlantic; IN, Indian; PAC, Pacific.

  • Fig. 2 Viral abundance and depth.

    (A) Power-law fit between log-transformed viral abundance and depth in the Atlantic, Indian, and Pacific oceans and in all the data. Lines denote the best power-law model regression. (B) Cumulative percentage curves of integrated viral abundance according to depth for the three oceanic regions and for all the data. Dashed lines in (B) show the depth where half of the integrated viral stock between 0 and 4000 m is contained in each oceanic region and for all the data.

  • Fig. 3 VPR and relationships between viral and prokaryotic abundances.

    Averages values of the VPR and their SEs in the three oceanic regions (Atlantic, Indian, and Pacific) sampled during the cruise in the (A) epipelagic (0 to 200 m), (B) mesopelagic (200 to 1000 m), and (C) bathypelagic (1000 to 4000 m) layers and in (D) all the data. Relationships between viral and prokaryotic abundances in the (E) epipelagic, (F) mesopelagic, and (G) bathypelagic layers from the Atlantic, Indian, and Pacific oceans and in (H) all the data. Dashed lines show the 95% prediction intervals from linear regressions of all data in the epipelagic, mesopelagic, and bathypelagic layers.

  • Fig. 4 VPL and VPLG and prokaryotic mortality due to viruses.

    (A) VPL against VPLG and (B) VMM against PMM detected at the surface (SURF; 3-m depth), DCM, and bathypelagic (BATHY; 4000-m depth) layers from 11 selected stations: 4 in the Atlantic Ocean, 3 in the Indian Ocean, and 4 in the Pacific Ocean. Three replicates were performed in each experiment. Dashed line is the 1:1 line. Lytic/lysogenic ratios at the surface, DCM, and bathypelagic layers were 4.63 ± 2.76, 10.00 ± 7.23, and 53.89 ± 39.17, respectively. Viral/grazing-mediated mortality ratios were 2.35 ± 1.47 at the surface layer, 7.15 ± 6.52 at the DCM layer, and 173.11 ± 128.91 at the bathypelagic layer.

  • Table 1 Mean, SE, median, minimum, and maximum values of viral abundance in the different layers and oceans.
    nMean
    (106 viruses ml−1)
    SE
    (105 viruses ml−1)
    Median
    (106 viruses ml−1)
    Minimum
    (105 viruses ml−1)
    Maximum
    (107 viruses ml−1)
    Epipelagic
      Atlantic2416.603.194.834.342.59
      Indian1688.314.007.702.933.31
      Pacific1938.724.716.890.854.39
      All epipelagic data6027.762.306.520.854.39
    Mesopelagic
      Atlantic880.100.640.880.850.32
      Indian601.894.221.351.222.51
      Pacific801.672.151.090.131.33
      All mesopelagic data2281.471.381.550.132.51
    Bathypelagic
      Atlantic900.510.570.470.360.47
      Indian630.520.560.470.380.25
      Pacific580.892.290.350.051.11
      All bathypelagic data2110.620.700.450.051.11
  • Table 2 Log-log slopes and fits between viral and prokaryotic abundance in the epipelagic, mesopelagic, and bathypelagic layers in the three different oceans and in all the subtropical ocean and power-law log-log slopes and fits of the relationship between depth and viral abundance in the three different oceans and in all the tropical and subtropical oceans.
    Viral abundance–prokaryotic abundance
    nEstimated interceptIntercept SESlopeSlope SEr2P
    Epipelagic
      Atlantic2401.70.540.870.090.26<0.0001
      Indian1684.720.450.360.080.12<0.0001
      Pacific1936.360.420.080.070.0070.25
      All epipelagic data5934.930.270.320.050.07<0.0001
    Mesopelagic
      Atlantic872.190.560.750.110.35<0.0001
      Indian603.761.270.450.240.050.07
      Pacific803.890.670.410.130.12<0.0001
      All mesopelagic data2273.310.380.520.070.18<0.0001
    Bathypelagic
      Atlantic892.450.850.70.190.13<0.0001
      Indian633.311.030.480.220.070.03
      Pacific582.980.920.530.190.120.007
      All bathypelagic data2103.680.440.410.090.08<0.0001
    All data10301.440.120.910.020.62<0.0001
    Viral abundance–depth (power-law function)
    Atlantic4199.260.32−1.120.050.54<0.0001
    Indian2918.770.37−1.020.060.52<0.0001
    Pacific3318.30.33−0.960.050.51<0.0001
    All data10408.750.2−1.030.030.52<0.0001
  • Table 3 Analysis of variance (ANOVA) and post hoc Tukey results testing for significant differences in viral abundance and VPR among layers [epipelagic (EPI), mesopelagic (MESO), and bathypelagic (BATHY)] and oceans [Atlantic (ATL), Indian (IN), and Pacific (PAC)].

    Lower panel: ANOVA and post hoc Tukey results testing for significant differences in viral abundances among water masses in the mesopelagic and bathypelagic layers. Only significant values are shown (P < 0.05).

    ANOVATukey’s test
    Viral abundance
    Layers
    nFPLayersP
    10401040.16<0.0001EPI-BATHY<0.0001
    EPI-MESO<0.0001
    MESO-BATHY<0.0001
    Oceans
    LayersnFPOceansP
    Epipelagic60110.59<0.0001PAC-ATL0.0002
    IN-ATL0.0004
    Mesopelagic2275.120.007ATL-IN0.01
    ATL-PAC0.05
    Bathypelagic2100.0050.1
    VPR
    Layers
    nFPLayersP
    10302.930.05EPI-MESO0.05
    Oceans
    LayersnFPOceansP
    Epipelagic60117.71<0.0001PAC-ATL<0.0001
    PAC-IN0.004
    Mesopelagic2271.140.321
    Bathypelagic2103.10.05ATL-IN0.04
    Water masses
    nFPWater massesP
    Mesopelagic2283.080.001AAIW-13EqPac0.04
    AAIW-ICW_130.02
    ENACW-ICW_130.03
    Bathypelagic2111.530.16

Supplementary Materials

  • Supplementary material for this article is available at http://advances.sciencemag.org/cgi/content/full/3/9/e1602565/DC1

    table S1. Mean, SE, median, minimum, and maximum values of viral abundance in each of the water masses identified in the mesopelagic layer (200 to 1000 m).

    table S2. Mean, SE, median, minimum, and maximum values of viral abundance according to the water masses in the bathypelagic layer (1000 to 4000 m).

    table S3. Results of the multivariate multiple regression analyses to explain variability of viral abundance in the epipelagic layer (0 to 200 m).

    table S4. Results of the multivariate multiple regression analyses to explain variability of viral abundance in the mesopelagic layer (200 to 1000 m).

    table S5. Results of the multivariate multiple regression analyses to explain variability of viral abundance in the bathypelagic layer (1000 to 4000 m).

    table S6. Values of VPL and VPLG.

    table S7. Mean and SE of the estimated C, N, and P released by viruses and that incorporated by grazers in the three layers (surface, DCM, and bathypelagic).

    fig. S1. Viral abundance with depth along the entire cruise visualized with Ocean Data View.

    fig. S2. VPL and VPLG and prokaryotic mortality due to viruses.

    data file S1. List of all the environmental and biological variables used in this study.

  • Supplementary Materials

    This PDF file includes:

    • table S1. Mean, SE, median, minimum, and maximum values of viral abundance in each of the water masses identified in the mesopelagic layer (200 to 1000 m).
    • table S2. Mean, SE, median, minimum, and maximum values of viral abundance according to the water masses in the bathypelagic layer (1000 to 4000 m).
    • table S3. Results of the multivariate multiple regression analyses to explain variability of viral abundance in the epipelagic layer (0 to 200 m).
    • table S4. Results of the multivariate multiple regression analyses to explain variability of viral abundance in the mesopelagic layer (200 to 1000 m).
    • table S5. Results of the multivariate multiple regression analyses to explain variability of viral abundance in the bathypelagic layer (1000 to 4000 m).
    • table S6. Values of VPL and VPLG.
    • table S7. Mean and SE of the estimated C, N, and P released by viruses and that incorporated by grazers in the three layers (surface, DCM, and bathypelagic).
    • fig. S1. Viral abundance with depth along the entire cruise visualized with Ocean Data View.
    • fig. S2. VPL and VPLG and prokaryotic mortality due to viruses.

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    Other Supplementary Material for this manuscript includes the following:

    • data file S1 (Microsoft Excel format). List of all the environmental and biological variables used in this study.

    Files in this Data Supplement:

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