Viral lysis modifies seasonal phytoplankton dynamics and carbon flow in the Southern Ocean

Abstract

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.

Diversity and ecological footprint of Global Ocean RNA viruses

“…For decades, extensive studies have focused on plankton dynamics and activity to infer the pairwise links among plankton and carbon export, including recent experimental work with viruses ( 42 , 43 ). Because these seminal studies were focused on narrow geographic ranges or oceanic provinces, we sought here to instead explore Global Ocean signals by taking advantage of the uniform Tara Oceans strategy for sampling plankton and sinking particles to broadly investigate oceanic conditions and ecosystem biota ( 10 ).…”

“…Recent experimental work has emerged to assess how DNA viruses affect ocean carbon export over small scales ( 42 , 43 ). We sought to complement these efforts through Global Ocean assessment of RNA viruses by using previously developed machine learning and ecosystem modeling approaches (materials and methods) ( 10 ) to evaluate in silico whether RNA viruses might affect ocean carbon export.…”

Identifying potential sources of iron-binding ligands in coastal Antarctic environments and the wider Southern Ocean

“…However, co-occurring surface ligand sources and various sinks often mean the relationship between Lt and fluorescence is only weakly positive (albeit often significant due to large sample sizes typically collected). Ligands may be released during phytoplankton death through viral lysis (Poorvin et al, 2011;Slagter et al, 2016;Biggs et al, 2021) or 'sloppy feeding' by zooplankton (Rue and Bruland, 1997;Boye et al, 2001). In parallel, microbial endocytosis removes entire Fe-ligand complexes from the water column (Hutchins et al, 1999;Sutak et al, 2020).…”

Distributions and relationships of virio- and picoplankton in the epi-, meso- and bathypelagic zones of the Amundsen Sea, West Antarctica during the austral summer

“…Viruses can also influence the cycling and sequestration of organic matter through the ‘viral shunt’ and ‘viral shuttle’ ( Wilhelm and Suttle, 1999 ; Zimmerman et al, 2020 ). Recently, a study reported that viral lysis was a major loss factor, responsible for roughly half (58%) of seasonal phytoplankton carbon losses in the Southern Ocean ( Biggs et al, 2021 ). Heterotrophic prokaryotes (including bacteria and archaea) are key components of the microbial food web and play critical roles in the utilization, transformation, remineralization and sequestration of dissolved and particulate organic matter ( Azam and Malfatti, 2007 ; Jiao et al, 2010 ).…”