Seasonal time bombs: dominant temperate viruses affect Southern Ocean microbial dynamics

Abstract

Rapid warming in the highly productive western Antarctic Peninsula (WAP) region of the Southern Ocean has affected multiple trophic levels, yet viral influences on microbial processes and ecosystem function remain understudied in the Southern Ocean. Here we use cultivation-independent quantitative ecological and metagenomic assays, combined with new comparative bioinformatic techniques, to investigate double-stranded DNA viruses during the WAP spring-summer transition. This study demonstrates that (i) temperate viruses dominate this region, switching from lysogeny to lytic replication as bacterial production increases, and (ii) Southern Ocean viral assemblages are genetically distinct from lower-latitude assemblages, primarily driven by this temperate viral dominance. This new information suggests fundamentally different virus-host interactions in polar environments, where intense seasonal changes in bacterial production select for temperate viruses because of increased fitness imparted by the ability to switch replication strategies in response to resource availability. Further, temperate viral dominance may provide mechanisms (for example, bacterial mortality resulting from prophage induction) that help explain observed temporal delays between, and lower ratios of, bacterial and primary production in polar versus lower-latitude marine ecosystems. Together these results suggest that temperate virus-host interactions are critical to predicting changes in microbial dynamics brought on by warming in polar marine systems.

Figure 1

Ecological variables measured in the surface ocean at Palmer LTER Station B from November 2010 through January 2011. Bacteria refers to Bacteria plus Archaea. Lytic viral infections are measured as the frequency of infected cells (FICs) and lysogeny is measured as the percentage of bacteria with inducible prophages. Error bars for FICs are upper and lower 95% confidence intervals. Error bars for bacteria, viruses and lysogeny are s.d. of the means of triplicate samples. 0, below detection; *, statistically significant results for lysogeny; arrows indicate when samples for virome construction were collected.

Figure 2

Social network analysis comparing all sequences in the four WAP viromes from the Southern Ocean (SO) with nine lower-latitude, seasonally variable surface samples from the POV data set including five viromes from the LineP transect (LP), three from the Monterey Bay Line 67 transect (MB) and one from Scripps Pier (SP). The network analysis compares viromes based on the abundance of shared k-mers among all sequences in each virome. Small dots represent the probability of the virome position given shared sequence content, labeled white dots represent the mean virome position and dot colors encode proximity of viromes on the plot.

Figure 3

Taxonomic composition of all sequences (small pie graphs) and of sequences identified as viral (larger pie graphs) unique to temperate and lytic viruses in the WAP. Taxonomic groups comprising <2% of the sequences are included as ‘other'.

Figure 4

Generalized illustration showing how the dominance of temperate viruses in the Southern Ocean can delay bacterial response to phytoplankton blooms and reduce the ratio of bacterial production to primary production relative to lower-latitude marine environments. Lysogeny dominates pre-bloom and has been shown to suppress metabolic activity in host bacteria, whereas induction of lysogens at the onset of phytoplankton blooms results in bacterial mortality and production of free viruses, which proceed to cause bacterial mortality via lytic infections.