Aggregate Formation During the Viral Lysis of a Marine Diatom

Abstract

Recent studies have suggested that the viral lysis of microbes not only facilitates the conversion of particulate organic matter into dissolved organic matter, but also promotes the formation of organic aggregates, which enhance the export of organic carbon from the surface ocean to the deep sea. However, experimental data supporting this proposition are limited. Here, we tested the hypothesis that the viral infection of marine diatoms enhances aggregate formation. We used a model system consisting of Chaetoceros tenuissimus, a bloom-forming diatom with an approximate cell size of 3-10 µm, and a DNA virus, CtenDNAV type II, which replicates in the nucleus of C. tenuissimus. The volume of large particles (50-400 µm in equivalent spherical diameters, determined from photographic images) was measured over time (up to 15 days) in the diatom-alone control and a virus-added diatom culture. We also determined the concentrations of Coomassie-stainable particles (CSP, proteinaceous particles) and transparent exopolymeric particles (TEP, acid-polysaccharide-rich particles) with colorimetric methods. The total volume of large particles was significantly higher (5-59 fold) in the virus-added diatoms than in the diatom-alone control during the period in which the viral lysis of the diatoms proceeded. One class of large particles produced in the virus-added diatoms was flake-shaped. The flakes were tightly packed and dense, and sank rapidly, possibly playing an important role in the vertical delivery of materials from the surface to the deep sea. The bulk CSP concentrations tended to be higher in the virus-added diatoms than in the diatom-alone control, whereas the reverse was true for the TEP. These results suggest that proteinaceous polymers are involved in aggregate formation. Our data support the emerging notion that the viral lysis of microbes facilitates aggregate formation and the export of organic carbon in the ocean.

Eukaryotic virus composition can predict the efficiency of carbon export in the global ocean

“…A previous study revealed an increase in abundance of viruses infecting diatoms of Chaetoceros in both the water columns and the sediments during the bloom of their hosts in a coastal area ( Tomaru et al., 2011 ), suggesting sinking of cells caused by viruses. Furthermore, the diatom Chaetoceros tenuissimus infected with a DNA virus (CtenDNAV type II) has been shown to produce higher levels of large-sized particles (50–400 μm) compared with non-infected cultures ( Tomaru et al., 2011 ; Yamada et al., 2018 ).…”

“…For instance, a theoretical study proposed that the CEE increases if viral lysis augments the ratio of exported carbon relative to the primary production-limiting nutrients (nitrogen and phosphorous) ( Suttle, 2007 ). Laboratory experimental studies reported that cells infected with viruses form larger particles ( Peduzzi and Weinbauer, 1993 ; Yamada et al., 2018 ), can sink faster ( Lawrence and Suttle, 2004 ), and can lead to preferential grazing by heterotrophic protists ( Evans and Wilson, 2008 ) and/or to higher growth of grazers ( Goode et al., 2019 ). This process termed “viral shuttle” ( Sullivan et al., 2017 ) is supported by several field studies that reported association of viruses with sinking material.…”

Seasonal Dynamics of Algae-Infecting Viruses and Their Inferred Interactions with Protists

“…The release of organic matter through the viral shunt has been estimated to be 150 billion tons of organic carbon per year [3]. A strong correlation between viral activity and carbon export by sinking particulate matter has recently been observed [9,10,11,12], indicating that viruses significantly contribute not only to the structuring of host communities, nutrient release, and ecosystem productivity, but also to the downward vertical transport of particulate carbon that comprises the biological carbon pump [2].…”

Aquatic virus culture collection: an absent (but necessary) safety net for environmental microbiologists

“…For instance, it is work with virus isolates in the laboratory that elucidated the role of virus-derived glycosphingolipids in terminating coccolithophore blooms and the rate-limiting biochemical steps in this process (Han et al, 2006;Vardi et al, 2012Vardi et al, , 2009, the competitive interactions between different coccolithoviruses (i. e., viruses infecting the E. huxleyi microalga) over the host for infection and the use of glycosphingolipid as virulence factors affecting viral success (Nissimov, Napier, Allen, & Kimmance, 2016;Nissimov et al, 2019), autophagy pathways in E. huxleyi during infection (Schatz et al, 2014), the virus strain-specific variations with regards to the induction of polysaccharide production in infected E. huxleyi cells (Nissimov et al, 2018), and the role of diatom-infecting viruses in aggregating material into sinking particles, important to the carbon biogeochemistry of the ocean (Yamada et al, 2018). Other notable examples where aquatic virus isolates were used to shed light on putative functions include the discovery of auxiliary metabolic genes (AMGs) in marine cyanophages (Breitbart, 2012), chlorovirus genes involved in carbohydrate metabolism (Van Etten et al, 2017), and genes involved in the production of fibers in Mimiviruses (Sobhy, La Scola, Pagnier, Raoult, & Colson, 2015).…”

“…Through this release (a process named "the viral shunt"), different metabolites and dissolved substances are remineralized and become readily available via the "microbial loop" to heterotrophic bacteria which utilise these as a food and energy source for growth (Azam, Fandino, Grossart, & Long, 1998;Pomeroy, Williams, le, Azam, & Hobbie, 2007;Wilhelm & Suttle, 1999). The second process is the "virus shuttle" which has a contrasting effect (Sullivan, Weitz, & Wilhelm, 2017;Yamada, Tomaru, Fukuda, & Nagata, 2018), in that the excreted metabolites and substances from the dying cells, which often include sticky polysaccharides and proteinaceous substances (Nissimov & Bidle, 2017;Thornton & Chen, 2017), clump cellular debris and other exuded compounds into larger particles of organic and inorganic material (Laber et al, 2018;Nissimov et al, 2018), which if heavy enough and negatively buoyant, sink through the water column, resulting in a net export of carbon from the surface ocean into the deep.…”