Cold Surface Waters of the Sub-Antarctic Pacific Ocean Support High Cyanophage Abundances and Infection Levels

Abstract

Cyanobacterial distributions are shaped by abiotic factors including temperature, light and nutrient availability as well as biotic factors such as grazing and viral infection. In this study, we investigated the abundances of T4-like and T7-like cyanophages and the extent of picocyanobacterial infection in the cold, high-nutrient-low-chlorophyll, sub-Antarctic waters of the southwest Pacific Ocean during austral spring. Synechococcus was the dominant picocyanobacterium, ranging from 4.7 × 10³ to 1.2 × 10⁵ cells∙mL^-1, while Prochlorococcus abundances were relatively low overall, ranging from 1.0 × 10³ to 3.9 × 10⁴ cells∙mL^-1. Using taxon-specific, single-virus and single-cell polony methods, we found that cyanophages were on average 15-fold, and up to 50-fold, more abundant than cyanobacteria in these waters. T4-like cyanophages (ranging from 1.7 × 10⁵ to 6.5 × 10⁵ phage·mL^-1) were 2.7-fold more abundant than T7-like cyanophages (ranging from 3.1 × 10⁴ to 2.8 × 10⁵ phage·mL^-1). Picocyanobacteria were primarily infected by T4-like cyanophages with more Synechococcus (4.8%-12.1%) infected than Prochlorococcus (2.5%-6.2%), whereas T7-like cyanophages infected less than 1% of both genera. These infection levels translated to daily mortality in the range of 5.7%-26.2% and 2.9%-14.3% of the standing stock of Synechococcus and Prochlorococcus, respectively. Our findings suggest that T4-like cyanophages are significant agents of cyanobacterial mortality in the cold, low-iron, sub-Antarctic waters of the South Pacific Ocean.

Keywords: cyanobacteria; microbe:virus interactions; microbial ecology; southern ocean.

FIGURE 1

Sampling locations and environmental conditions in the Chatham Rise, east of New Zealand, during the TAN1810 cruise. (a) Map of the region with the sampling location of cycle 1 and cycle 2. Features of the currents are based on Orsi, Whitworth, and Nowlin (1995), STF—subtropical Front; SPF—Subpolar Front; the colour corresponds to the bathymetry of the region; (b) temperature versus salinity plot of the water parcels sampled. Values are the averages for surface waters between depths of 0 and 15 m. Cycle 1 was sampled between 24 and 29 October 2018, and cycle 2 was sampled between 2 and 4 November 2018.

FIGURE 2

Cyanobacterial abundances measured during the two sampling cycles. Abundances of cyanobacteria during sampling cycle 1 (a) and sampling cycle 2 (b). The grey vertical lines depict the beginning of the day (00:00). A total of 19 and 9 samples are shown for cycle 1 and cycle 2, respectively. Samples were collected in October–November of 2018.

FIGURE 3

Free cyanophage abundances measured during the two sampling cycles. Abundances of cyanophages during sampling cycle 1 (a) and sampling cycle 2 (b). The grey vertical lines depict the beginning of the day (00:00). A total of 17 and 9 samples are shown for cycle 1 and cycle 2, respectively. Samples were collected in October–November of 2018.

FIGURE 4

Cyanobacterial infection during sampling cycle 2. Percentage of Synechococcus (a) and Prochlorococcus (b) infected by the two different cyanophage families. The grey vertical lines depict the beginning of the day (00:00). Samples were collected in November of 2018.

FIGURE 5

Total abundances of cyanobacteria, cyanophages and cyanobacterial infection. (a) Sampling cycle 1, (b) sampling cycle 2. The grey vertical lines depict the beginning of the day (00:00). The left y‐axis shows total abundances of cyanobacteria and cyanophages, and the right y‐axis shows infection (%) by both T4‐like and T7‐like cyanophages. Samples were collected in October and November of 2018.

FIGURE 6

Viral‐induced mortality estimates. (a) Daily loss of cyanobacterial cells. (b) Cyanobacterial cell loss per cyanobacterial generation.