Viral lysis of Phaeocystis pouchetii: Implications for algal population dynamics and heterotrophic C, N and P cycling

Abstract

A model ecosystem with two autotrophic flagellates, Phaeocystis pouchetii and Rhodomonas salina, a virus specific to P. pouchetii (PpV) and bacteria and heterotrophic nanoflagellates was used to investigate effects of viral lysis on algal population dynamics and heterotrophic nitrogen and phosphorus mineralization. Lysis of P. pouchetii by PpV had strong positive effects on bacterial and HNF abundance, and the mass balance of C, N and P suggested an efficient transfer of organic material from P. pouchetii to bacterial and HNF biomass through viral lysis. At the same time, the degradation of P. pouchetii lysates was associated with significant regeneration of inorganic N and P resulting in 148 lg N l À1 and 7 lg P l À1 , corresponding to 78% and 26% of lysate N and P being mineralized to NH 4 þ and PO 4 3À, respectively. These results showed that the turnover of viral lysates in the microbial food web was associated with significant N and P mineralization, supporting the current view that viral lysates can be an important source of inorganic nutrients in marine systems. In the presence of R. salina, the generated NH 4 þ supported 11% of the observed R. salina growth. Regrowth of virus-resistant P. pouchetii following cell lysis was observed in long-term incubations (150 days), and possibly influenced by nutrient availability and competition from R. salina. The observed impact of viral activity on autotrophic and heterotrophic processes provides direct experimental evidence for virus-driven nutrient generation and emphasizes the potential importance of the viral activity in supporting marine primary production.

Responses of the coastal bacterial community to viral infection of the algae Phaeocystis globosa

“…Studies conducted in the last years have made it increasingly evident that viruses are significant driving forces in algal (Haaber and Middelboe, 2009) and bacterioplankton populations dynamics (Middelboe et al, 2003). Moreover, through the 'viral shunt' (Wilhelm and Suttle, 1999), the release of dissolved organic carbon and nutrients from the particulate organic pool is enhanced, leading to increased substrate availability for microbially mediated processes.…”

“…Moreover, through the 'viral shunt' (Wilhelm and Suttle, 1999), the release of dissolved organic carbon and nutrients from the particulate organic pool is enhanced, leading to increased substrate availability for microbially mediated processes. Thereby, viruses can influence biogeochemical cycling in the world's oceans (Brussaard et al, 2005b;Haaber and Middelboe, 2009).…”

Virus-mediated transfer of nitrogen from heterotrophic bacteria to phytoplankton

“…When the C : N of DOM is low relative to bacterial nutritional requirements, bacteria deaminate DOM and release ammonium (Hollibaugh, 1978;Goldman et al, 1987) to acquire carbon for energy and growth (e.g. Brussaard et al, 1996;Fouilland et al, 2014); the release of ammonium can support phytoplankton growth (Haaber and Middelboe, 2009;Weinbauer et al, 2011;Shelford et al, 2012).…”

Importance of the Viral Shunt in Nitrogen Cycling in Synechococcus Spp. Growth in Subtropical Western Pacific Coastal Waters

“…Lysed bacterial cells, however, release dissolved organic matter (DOM), which recycles bacterial carbon as bacterial production (Middelboe et al 1996;Middelboe and Lyck 2002;Wilhelm et al 2002). Thus, viral lysis may also serve as a significant pathway for the regeneration of nutrients, directly enhancing nutrient supply rates to phytoplankton (Haaber and Middelboe 2009;Weinbauer et al 2011;Shelford et al 2012).…”