241This pattern has the strong feedback effect of preventing spe-
cies dominance and enhanced species cohabitation within
microbial communities, i.e. the so-called ‘phage kills the
winner’ hypothesis (Thingstad and Lignell 1997 ). In early
June 2001, we conducted a short-term experiment to exam-
ine the impact of viral lysis on bacterial community compo-
sition in Lake Pavin using fl uorescence in situ hybridization
(FISH) and terminal restriction fragment length polymor-
physm (T-RFLP) (Jardillier et al. 2005 ). The main fi ndings
suggested a control of the PCC (i) by viral lysis of some
dominant phylotypes, and (ii) by interspecifi c competition
between resistant strains for the uptake of substrates released
by viral lysis. The increase of Archaea suggested that these
cells benefi t such resources.
The dependence of lytic virulent viruses on the availabil-
ity of specifi c hosts implies that viruses respond to the growth
rate of the most active hosts (Palesse et al. 2014 ). In our
recent study conducted in 11 freshwater lakes (Pradeep Ram
et al. 2013 ), we found that high nucleic acid content cells are
the best determinant of viral abundance, and served as the
main host target for viral proliferation. Such preferential
lysis can have a strong impact on the overall prokaryote
community metabolism. We tested the hypothesis of top-
down control on prokaryotic growth effi ciency (PGE), which
we used as an index of physiological and energetic status at
the community level. Viruses through lytic infection had a
strong antagonistic impact on PGE at the aphotic zone,
whereas fl agellate grazing was found to enhance PGE in the
euphotic zone. These differences may have signifi cant impli-
cations on the food web dynamics because the nature of
nutrients released through the processes of grazing and viral
lysis is different. Grazing activity results in more effective
release of inorganic nutrients, whereas viral lysis has been
shown to produce elements in organic complexes (Fuhrman
1999 ; Wilhelm and Suttle 1999 ).
14.6.2 Lysogeny : A Survival Strategy
for Viruses
One of the key explanations for the omnipresence of viruses
in natural ecosystems is undoubtedly through the existence
of several lifestyles, of which two major pathways, namely
viral lytic and lysogenic pathways , are prevalent in aquatic
systems. Examination of natural prokaryotic communities
inducible with a mutagenic agent (e.g. mitomycin C ) has
suggested that the fraction of lysogenic bacteria (known as
FLC, frequency of lysogenically infected cells) is typi-
cally < 50 % (range 0–100 %) of the total abundance in
marine environments. In freshwaters, these values fl uctuate
from 0 to 16 % in temperate and tropical lakes, and from 0 to
73 % in Antarctic lakes (Sime-Ngando and Colombet 2009 ).
In Lake Pavin, analysis of samples collected through the
whole water column on 20 April 2004 yielded FLC values
between 0.1 and 16 % (Colombet et al. 2006 ). This suggests
that a substantial proportion of bacteria in Lake Pavin con-
tain functional viral genomes. The relative abundance of
lysogens appeared negatively correlated with bacterial abun-
dance and production, with the frequency of infected cells,
and with viral lytic production, supporting the hypothesis
that lysogeny is a strategy for survival of phages in environ-
ments with low host availability (Colombet et al. 2006 ).
From these fi ndings, we hypothesized that (i) there are envi-
ronmental characteristics, in relation with potential host den-
sities and availability, favoring one of the two “viral life
cycles”, and (ii) host availability is prevalent over the physi-
cal and chemical environments and favors lytic over lyso-
genic “viral life cycles.”
To test these hypotheses, we designed an experimental
study to investigate the effects of added organic and inor-
ganic nutrients on the two viral lifestyles in freshwater
microbial (i.e. < 0.8 μm fraction) microcosms collected in
Lake Pavin during a nutrient-depleted period, using mito-
mycin C a s prophage inductor agent (Pradeep Ram and
Sime-Ngando 2010 ). In the absence of mitomycin C , viral
lytic production increased as a functional response to the
strong stimulation of bacterial growth rates (0.7–0.8 day −1 )
by the added nutrients, primarily the organic nutrients
which appeared scarcer than inorganic nutrients. In the
presence of mitomycin C , temperate phage production
(frequency of lysogenically infected bacterial cells,
FLC = 17–19 % of total cells) signifi cantly exceeded lytic
production (frequency of lytically infected bacterial cells,
FIC = 9–11 %) in natural samples (i.e. without nutrient
additions) as a result of higher prophage induction, which
relatively increased with the decreasing contact probability
between viruses and their potential hosts. In contrast, addi-
tion of nutrients drastically reduced FLC (<4 %) and
increased FIC (>22 %). Both variables were antagonisti-
cally correlated as was the correlation between FLC and
bacterial growth rates. This strongly supports the idea that
lysogeny may represent a maintenance strategy for viruses
in harsh nutrient/host conditions which appeared as major
instigators of the trade-off between the two viral lifestyles.
Overall, at the community level, we reject the hypothesis
that nutrients but mitomycin C stimulate temperate phage
induction, and retained the hypotheses that nutrients rather
(i) stimulate lytic viruses via enhanced host growth and (ii)
when limiting, promote lysogenic conversion in natural
waters (Pradeep Ram and Sime-Ngando 2010 ).14 Ecology of Viruses in Lake Pavin