Release and bioavailability of C, N, P Se, and Fe following viral lysis of a marine chrysophyte

Abstract

The potential importance of the viral lysis of phytoplankton for nutrient and carbon cycling has been acknowledged, but no quantitative assessments of this phenomenon exist. Radiotracer experiments examined the release and bioavailability of C, N, P Fe, and Se following viral lysis of the "brown tide" chrysophyte Aureococcus anophagefSeerens. Photochemical effects on the dissolved-particulate partitioning and biological uptake of virally released elements were also investigated. Viral lysis of A. anophagefSerens released 50% more C and Se than uninfected control cells to the dissolved phase, while N, P, and Fe remained in the particulate phase. There was a significant inverse correlation between A. unophugefirens and bacterial densities, as well as an increase in particulate organic nitrogen levels in cultures during viral lysis. These observations indicate thitt released dissolved organic matter supported bacterial growth and may be a pathway by which various elements are diverted in microbial food webs. Dissolved nutrients released by viral lysis were accumulated to varying degrees by natural assemblages of marine bacteria and cultured diatoms, and virally regenerated N and P relieved diatom nutrient limitation. During a 4-wk incubation, 80% of C and P within cell lysis debris was released to the diss,olved phase, likely due to bacterial activity. Photochemical degradation of cell lysis debris enhanced dissolved levels of Se (100%) and Fe (50%) and reduced total dissolved C by 15%. Photochemistry doubled the bioavailability of virally released Se to diatoms, while decreasing the bioavailability of C to bacteria threefold. The viral lysis of an A. unophugefirens bloom in the field could release 40 PM dissolved organic carbon and rapidly transfer other released elements to bacteria. Such occurrences may significantly affect water column chemistry, species composition, and succession within marine plankton communities.

Bridging the Gap between Knowing and Modeling Viruses in Marine Systems—An Upcoming Frontier

“…This semi-closed trophic loop (Figure 2), fed externally by the release of DOM from phytoplankton and grazers, has the net effect of oxidizing organic matter and regenerating inorganic nutrients (Proctor and Fuhrman, 1991).Viral lysis of bacterial and phytoplankton cells removes a portion of autotrophic and microbial heterotrophic production from protozoan grazers providing, at the same time, a short circuit to the "traditional" concept of carbon cycling. It was even suggested that the recycling of organic material in a bacteriaphage-dissolved organic material loop could lead bacterial production to exceed primary production (Strayer, 1988;Gobler et al, 1997). From these results, the canonical view of the "microbial loop" as a way of loss of organic material from the particulate flux toward larger organisms, and the reincorporation of this organic material via heterotrophic bacteria (Azam et al, 1983), was upgraded with the "viral loop" as a subset.…”

“…Besides the already mentioned high levels of viral abundance and infection on bacteria, infection of phytoplankton is also common during intense episodes of coastal algal bloom (Proctor and Fuhrman, 1991;Yau et al, 2011;Shelford et al, 2012;Hasumi and Nagata, 2014;Stock et al, 2014). Consequently, viral lysis of phytoplankton can significantly affect the partitioning and biological cycling of elements such as C, N, P, Si, and Fe (Gobler et al, 1997), and the potential consequences of viral infection on nutrient cycling has been extensively discussed ever since (Bergh et al, 1989;Heldal and Bratbak, 1991;Proctor and Fuhrman, 1991;Suttle et al, 1991).…”

“…One major consequence of this process is the release of DOM, plus some particulate organic matter (POM), which has an important role in the regeneration of nutrients. Thus, viral infection is an extremely efficient way to convert biomass into dissolved and particulate detritus readily available to bacteria (Fuhrman, 1992;Middelboe et al, 1996;Gobler et al, 1997). This, in turn, has repercussions through the entire food web considering the close coupling between heterotrophic bacteria and phytoplankton (Lancelot and Billen, 1984;Vanduyl and Kop, 1988;Brussaard et al, 1995).…”

Remineralization and recycling of iron, thorium and organic carbon by heterotrophic marine protists in culture

“…Our data suggest that protistan grazing may be an additional source of iron binding ligands in seawater, through the regeneration of iron from bacterial biomass. Similar theories have been suggested for metazoan grazing (Hutchins & Bruland 1994) and viral lysis of cells (Gobler et al 1997). The binding strength and bioavailability of the putative iron ligands produced in our model systems is unknown.…”

Isolation and Characterization of a Novel Single-Stranded RNA Virus Infectious to a Marine Fungoid Protist, Schizochytrium sp. (Thraustochytriaceae, Labyrinthulea)

“…Viruses and virus-like particles (VLPs) have been discovered in a variety of phytoplankton and bacteria (48,54,64) and have been recognized as important agents in controlling bacterial and algal biomass (4,41,48) and nutrient cycling (17,66) and in maintaining the biodiversity of bacteria and microalgae (5,10,12). So far, more than 13 viruses infecting marine microalgae have been isolated and characterized (5).…”