Trade-Offs between Competition and Defense Specialists among Unicellular Planktonic Organisms: the “Killing the Winner” Hypothesis Revisited

Abstract

SUMMARY A trade-off between strategies maximizing growth and minimizing losses appears to be a fundamental property of evolving biological entities existing in environments with limited resources. In the special case of unicellular planktonic organisms, the theoretical framework describing the trade-offs between competition and defense specialists is known as the “killing the winner” hypothesis (KtW). KtW describes how the availability of resources and the actions of predators (e.g., heterotrophic flagellates) and parasites (e.g., viruses) determine the composition and biogeochemical impact of such organisms. We extend KtW conceptually by introducing size- or shape-selective grazing of protozoans on prokaryotes into an idealized food web composed of prokaryotes, lytic viruses infecting prokaryotes, and protozoans. This results in a hierarchy analogous to a Russian doll, where KtW principles are at work on a lower level due to selective viral infection and on an upper level due to size- or shape-selective grazing by protozoans. Additionally, we critically discuss predictions and limitations of KtW in light of the recent literature, with particular focus on typically neglected aspects of KtW. Many aspects of KtW have been corroborated by in situ and experimental studies of isolates and natural communities. However, a thorough test of KtW is still hampered by current methodological limitations. In particular, the quantification of nutrient uptake rates of the competing prokaryotic populations and virus population-specific adsorption and decay rates appears to be the most daunting challenge for the years to come.

Mixing alters the lytic activity of viruses in the dark ocean

“…2006, Winter et al. 2009a , b, 2010). The deep ocean itself is vertically‐structured due to fine‐grained differences in temperature and salinity resulting in subtle density differences that give rise to defined water masses (Emery 2001) and harbor distinct prokaryotic and virus communities (Galand et al.…”

“…2009, Winter et al. 2010), considered to be a key mechanism in maintaining prokaryotic richness. Most viruses infecting prokaryotes are either lytic or lysogenic.…”

Quantification of virus genes provides evidence for seed-bank populations of phycodnaviruses in Lake Ontario, Canada

“…As these Chlorella-like OTUs never represented a substantial proportion of any library it is difficult to speculate that they are hosts for any Lake Ontario chloroviruses. Nonetheless, if these OTUs represent Chlorovirus hosts and their frequency in the psbA clone libraries reflects their low abundance in nature, their low concentration could be the major factor driving the relatively low abundances of the Chlorovirus fragments monitored, as shown for certain scenarios of virus-host dynamics in the 'killing the winner model' (Winter et al, 2010). It is interesting that although we only found two psbA sequences closely related to members of the Prasinophyceae, most sequences in the Lake Ontario AVS libraries are closely related to algal viruses known to infect prasinophytes.…”

Modulation of host ROS metabolism is essential for viral infection of a bloom-forming coccolithophore in the ocean

“…Thus, viruses have a huge impact on ocean biogeochemical cycles by short-circuiting the flux of carbon and nutrients from phytoplankton and bacteria to higher trophic levels, shunting it to the pool of dissolved and particulate organic matter, and making it more available for recycling by microbial respiration (Fuhrman, 1999;Wilhelm and Suttle, 1999;Suttle, 2007). Marine viruses are known to regulate phytoplankton population size, distribution and composition by eliminating more dominant phytoplankton species and are considered major vehicles for horizontal gene transfer between distantly related species (Lindell et al, 2005;Suttle, 2005;Rohwer and Thurber, 2009;Sharon et al, 2009;Winter et al, 2010;Breitbart, 2012).…”