Ocean time-series reveals recurring seasonal patterns of virioplankton dynamics in the northwestern Sargasso Sea

Abstract

There are an estimated 10(30) virioplankton in the world oceans, the majority of which are phages (viruses that infect bacteria). Marine phages encompass enormous genetic diversity, affect biogeochemical cycling of elements, and partially control aspects of prokaryotic production and diversity. Despite their importance, there is a paucity of data describing virioplankton distributions over time and depth in oceanic systems. A decade of high-resolution time-series data collected from the upper 300 m in the northwestern Sargasso Sea revealed recurring temporal and vertical patterns of virioplankton abundance in unprecedented detail. An annual virioplankton maximum developed between 60 and 100 m during periods of summer stratification and eroded during winter convective mixing. The timing and vertical positioning of this seasonal pattern was related to variability in water column stability and the dynamics of specific picophytoplankton and heterotrophic bacterioplankton lineages. Between 60 and 100 m, virioplankton abundance was negatively correlated to the dominant heterotrophic bacterioplankton lineage SAR11, as well as the less abundant picophytoplankton, Synechococcus. In contrast, virioplankton abundance was positively correlated to the dominant picophytoplankton lineage Prochlorococcus, and the less abundant alpha-proteobacteria, Rhodobacteraceae. Seasonally, virioplankton abundances were highly synchronous with Prochlorococcus distributions and the virioplankton to Prochlorococcus ratio remained remarkably constant during periods of water column stratification. The data suggest that a significant fraction of viruses in the mid-euphotic zone of the subtropical gyres may be cyanophages and patterns in their abundance are largely determined by Prochlorococcus dynamics in response to water column stability. This high-resolution, decadal survey of virioplankton abundance provides insight into the possible controls of virioplankton dynamics in the open ocean.

Figure 1

Contour plot of virioplankton abundance ( × 10⁹ l⁻¹) over 300 m from 2000 to 2010 with MLD (m) superimposed as a white line. Each dot represents an individual sampling point.

Figure 2

Contour plot of (a) Bacterioplankton ( × 10⁸ l⁻¹); (b) Synechococcus ( × 10⁷ l⁻¹) and (c) Prochlorococcus ( × 10⁸ l⁻¹) cell abundance over 300 m from 2002 through 2009 with virioplankton abundance ( × 10⁹ l⁻¹) overlaid as contour lines. MLD (m) is superimposed as a white line in panel (a).

Figure 3

Annual composite plots of (a) MLD (m) in black with the total range in grey. (b) Virioplankton abundance ( × 10⁹ l⁻¹) (filled circle) and bacterioplankton abundance ( × 10⁸ l⁻¹) (open circle; and for all bacterial lineages in the following panels). (c) Virioplankton abundance ( × 10⁹ l⁻¹) and SAR11 abundance ( × 10⁸ l⁻¹). (d) Virioplankton abundance ( × 10⁹ l⁻¹and Synechococcus abundance ( × 10⁷ l⁻¹). (e) Virioplankton abundance ( × 10⁹ l⁻¹) and Prochlorococcus abundance ( × 10⁸ l⁻¹). (f) Virioplankton abundance ( × 10⁹ l⁻¹) and Rhodobacteraceae abundance ( × 10⁷ l⁻¹). (g) VBR. (h) Virioplankton-to-SAR11 ratio. (i) Virioplankton-to-Synechococcus ratio. (j) Virioplankton-to-Prochlorococcus ratio and (k) virioplankton-to-Rhodobacteraceae ratio. The annual composite plots focused on the virioplankton maximum by integrating and depth-normalizing cell abundances between 60 m and 100 m. The decadal time-series was then collapsed to a single annual composite where a mean value and standard error for each month was derived.

Figure 4

Contour plot of (a) SAR11 cell abundance ( × 10⁸ l⁻¹) and (b) Rhodobacteraceae ( × 10⁷ l⁻¹) cell abundance over 300 m from 2003 through 2005 with virioplankton abundance ( × 10⁹ l⁻¹) overlaid as contour lines. MLD (m) is superimposed as a white line in panel (a).