Lysogeny and virus-induced mortality of bacterioplankton in surface, deep, and anoxic marine waters

Lysogeny (bacteria containing inducible prophages) and lytic viral infection (bacteria in a lytic stage of infection) were investigated at the community level in contrasting marine environments such as estuarine versus offshore waters, surface versus deep waters, and oxic versus anoxic waters in the Mediterranean and Baltic Seas. The frequency of lysogenic cells (FLC) in bacterioplankton communities ranged from not detectable to 84% as estimated by prophage induction due to mitomycin C, and highest values were typically found in deep waters (800–2,000 m). Transmission electron microscopy based estimates of virus-induced mortality of bacterioplankton (VMB) ranged from a few percent to 71%, and highest values were found in anoxic waters of the Baltic Sea. FLC and the frequency of infected cells (FIC) were related in form of a negative power function indicating that environments exist where one of the two viral life strategies prevails. Across all investigated environments, FLC was negatively related to bacterial abundance and production, whereas FIC showed a positive relationship with viral and bacterial parameters. FIC was higher and FLC was lower in moderately productive estuarine and offshore surface waters than in less productive mesopelagic and deep waters. Thus, lysogeny seems to be a survival strategy at low host abundance and activity, whereas high host abundance and activity seems to favor the lytic life cycle. The key process for the prevalence of lytic infection compared to prophage replication at high host abundance could be competition due to outnumbering. Between 11% and 88% (average, 35%) of the bacteria contained a functional (lytic or lysogenic) viral genome. Viruses play a significant role in ecological and biogeochemical processes of the ocean, and their impact depends on the reproductive pathway (Fuhrman 1999; Wilhelm and Suttle 1999; Wommack and Colwell 2000). The two major viral reproductive strategies are lysogeny and lytic viral infection. In the lytic cycle, the (bacterio)phage forces the host metabolism to produce new phages, which are released during the lysis of the cell. In the lysogenic cycle, the lysogenic phage either enters the lytic cycle directly or the phage genome remains within the host in a dormant stage (prophage) and replicates along with the host until the lytic cycle is induced. In the pseudolysogenic life cycle, a fraction of the infected population is lysed (Ackermann and DuBow 1987); however, this has not been studied at the community level. Based on studies with isolated phage–host systems and using models, it was proposed that lysogeny is a survival strategy of phages at low host densities (Steward and Levin 1984). Consequently, reproduction of lytic phages should be 1 To whom correspondence should be addressed. Present address: Laboratoire d’Océanographie de Villefranche-sur-Mer (LOV), UMR 7093 CNRS-UPMC, BP 28, 06234 Villefranche-sur-Mer (wein@