Phytoplankton form the base of marine food webs and are a primary means for carbon export in the Southern Ocean, a key area for global pCO₂ drawdown. Viral lysis and grazing have very different effects on microbial community dynamics and carbon export, yet, very little is known about the relative magnitude and ecological impact of viral lysis on natural phytoplankton communities, especially in Antarctic waters. Here, we report on the temporal dynamics and relative importance of viral lysis rates, in comparison to grazing, for Antarctic nano- and pico-sized phytoplankton of varied taxonomy and size over a full productive season. Our results show that viral lysis was a major loss factor throughout the season, responsible for roughly half (58%) of seasonal phytoplankton carbon losses. Viral lysis appeared critically important for explaining temporal dynamics and for obtaining a complete seasonal mass balance of Antarctic phytoplankton. Group-specific responses indicated a negative correlation between grazing and viral losses in Phaeocystis and picoeukaryotes, while for other phytoplankton groups losses were more evenly spread throughout the season. Cryptophyte mortality was dominated by viral lysis, whereas small diatoms were mostly grazed. Larger diatoms dominated algal carbon flow and a single ‘lysis event’ directed >100% of daily carbon production away from higher trophic levels. This study highlights the need to consider viral lysis of key Antarctic phytoplankton for a better understanding of microbial community interactions and more accurate predictions of organic matter flux in this climate-sensitive region.

Climate change at the Western Antarctic Peninsula (WAP) is predicted to cause major changes in phytoplankton community composition, however, detailed seasonal field data remain limited and it is largely unknown how (changes in) environmental factors influence cell size and ecosystem function. Physicochemical drivers of phytoplankton community abundance, taxonomic composition and size class were studied over two productive austral seasons in the coastal waters of the climatically sensitive WAP. Ice type (fast, grease, pack or brash ice) was important in structuring the pre-bloom phytoplankton community as well as cell size of the summer phytoplankton bloom. Maximum biomass accumulation was regulated by light and nutrient availability, which in turn were regulated by wind-driven mixing events. The proportion of larger-sized (> 20 µm) diatoms increased under prolonged summer stratification in combination with frequent and moderate-strength wind-induced mixing. Canonical correspondence analysis showed that relatively high temperature was correlated with nano-sized cryptophytes, whereas prymnesiophytes (Phaeocystis antarctica) increased in association with high irradiance and low salinities. During autumn of Season 1, a large bloom of 4.5-µm-sized diatoms occurred under conditions of seawater temperature > 0 °C and relatively high light and phosphate concentrations. This bloom was followed by a succession of larger nano-sized diatoms (11.4 µm) related to reductions in phosphate and light availability. Our results demonstrate that flow cytometry in combination with chemotaxonomy and size fractionation provides a powerful approach to monitor phytoplankton community dynamics in the rapidly warming Antarctic coastal waters.

Global climate change-induced warming of the Artic seas is predicted to shift the phytoplankton community towards dominance of smaller-sized species due to global warming. Yet, little is known about their viral mortality agents despite the ecological importance of viruses regulating phytoplankton host dynamics and diversity. Here we report the isolation and basic characterization of four prasinoviruses infectious to the common Arctic picophytoplankter Micromonas. We furthermore assessed how temperature influenced viral infectivity and production. Phylogenetic analysis indicated that the putative double-stranded DNA (dsDNA) Micromonas polaris viruses (MpoVs) are prasinoviruses (Phycodnaviridae) of approximately 120 nm in particle size. One MpoV showed intrinsic differences to the other three viruses, i.e., larger genome size (205 ± 2 vs. 191 ± 3 Kb), broader host range, and longer latent period (39 vs. 18 h). Temperature increase shortened the latent periods (up to 50%), increased the burst size (up to 40%), and affected viral infectivity. However, the variability in response to temperature was high for the different viruses and host strains assessed, likely affecting the Arctic picoeukaryote community structure both in the short term (seasonal cycles) and long term (global warming).

The Southern Ocean microbial ecosystem, with its pronounced seasonal shifts, is vulnerable to the impacts of climate change. Since viruses are key modulators of microbial abundance, diversity, and evolution, we need a better understanding of the effects of seasonality on the viruses in this region. Our comprehensive exploration of DNA viral diversity in the Southern Ocean reveals a unique and largely uncharted viral landscape, of which 75% was previously unidentified in other oceanic areas. We uncover novel viral taxa at high taxonomic ranks, expanding our understanding of crassphage, polinton-like virus, and virophage diversity. Nucleocytoviricota viruses represent an abundant and diverse group of Antarctic viruses, highlighting their potential as important regulators of phytoplankton population dynamics. Our temporal analysis reveals complex seasonal patterns in marine viral communities (bacteriophages, eukaryotic viruses) which underscores the apparent interactions with their microbial hosts, whilst deepening our understanding of their roles in the world’s most sensitive and rapidly changing ecosystem.

Whether phytoplankton mortality is caused by grazing or viral lysis has important implications for phytoplankton dynamics and biogeochemical cycling. The ecological relevance of viral lysis for Antarctic phytoplankton is still under-studied. The Amundsen Sea is highly productive in spring and summer, especially in the Amundsen Sea Polynya (ASP), and very sensitive to global warming-induced ice-melt. This study reports on the importance of the viral lysis, compared to grazing, of pico- and nanophytoplankton, using the modified dilution method (based on apparent growth rates) in combination with flow cytometry and size fractionation. Considerable viral lysis was shown for all phytoplankton populations, independent of sampling location and cell size. In contrast, the average grazing rate was 116% higher for the larger nanophytoplankton, and grazing was also higher in the ASP (0.45 d⁻¹ vs. 0.30 d⁻¹ outside). Despite average specific viral lysis rates being lower than grazing rates (0.17 d⁻¹ vs. 0.29 d⁻¹), the average amount of phytoplankton carbon lost was similar (0.6 µg C L⁻¹ d⁻¹ each). The viral lysis of the larger-sized phytoplankton populations (including diatoms) and the high lysis rates of the abundant P. antarctica contributed substantially to the carbon lost. Our results demonstrate that viral lysis is a principal loss factor to consider for Southern Ocean phytoplankton communities and ecosystem production.

Southern Ocean phytoplankton are especially subjected to pronounced seasonal and interannual changes in light availability. Although previous studies have examined the role of light in these environments, very few combined pigment-based taxonomy with flow cytometry to better discriminate the light response of various phytoplankton groups. In particular the different populations within the diverse and important taxonomic group of diatoms require further investigation. Six incubation experiments (9–10 days) were performed during the main productive period with natural seawater collected at the Western Antarctic Peninsula. Standing stock of Phaeocystis spp. cells displayed relatively fast accumulation under all levels of light (low, medium, high; 4–7, 30–50 and 150–200 µmol quanta m⁻² s⁻¹), whilst the small- and larger-sized diatom populations (4.5 and 20 µm diameter) exhibited faster accumulation in medium and high light. In contrast, intermediate-sized diatoms (11.5 µm diameter) displayed fastest net growth under low light, subsequently dominating the phytoplankton community. Low light was a key factor limiting accumulation and peak phytoplankton biomass, except one incubation displaying relatively high accumulation rates under low light. The 3-week low-light period prior to experimentation likely allowed adaptation to maximize achievable growth and seems a strong determinant of whether the different natural Antarctic phytoplankton populations sustain, thrive or decline. Our study provides improved insight into how light intensity modulates the net response of key Antarctic phytoplankton, both between and within taxonomic groups.