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14.7 Protistan Grazing of Viruses
and Ecological Implications
Despite the fact that bacteria are undoubtedly the principal
constituent in the diet of heterotrophic nanofl agellates (HNF)
in most aquatic systems, González and Suttle ( 1993 ) showed
that marine viruses can also contribute signifi cantly to the
nutrition of HNF and that being consumed is one possible
route for the decay of virioplankton, in addition to degrada-
tion by solar radiation, by heat-labile substances, or by
adsorption to particulate organic matter. The second and last
report on this topic so far was conducted in the oligotrophic
Lake Pavin and in the nearby eutrophic Lake Aydat (Bettarel
et al. 2005 ). This study provides the fi rst estimates of viral
losses from HNF predation in freshwaters, with removal
rates from HNF grazers which were relatively modest, aver-
aging 4.1 and 0.8 % of viral production in Lake Pavin and
Lake Aydat, respectively (Table 14.1 ). Although phagotro-
phy by nanofl agellates appears of minor importance as a loss
process for natural virioplankton communities, our study
suggests that viruses are probably of higher nutritional sig-
nifi cance for HNF in oligotrophic systems than in productive
ones. Based on the amount of carbon (C), nitrogen (N) and
phosphorus (P) contained per single virus and bacterium
(Gonzàlez and Suttle 1993 ), we estimated that ingested
viruses would constitute only 0.6, 0.7 and 1.4 % of C, N and
P, respectively, in the total diet of HNF in Lake Pavin, and
only 0.1, 0.2, and 0.4 % in Lake Aydat. This suggests that
viruses are not as energetically valuable as bacteria in the
HNF diet. Clearly, we conclude that (i) there is a trophic link
between HNF and viruses in the functioning of aquatic
microbial food webs , (ii) where viruses would represent a
weak food source for HNF (i.e. compared to bacteria), (iii)
but they still may not be inconsequential for the HNF diet,
primarily in systems with low productivity (Bettarel et al.
2005 ). A question that now emerges is to what extent does
ingestion of viruses by HNF represent a source of infection
for these protists? More details on HNF bacterivory are pro-
vided in Chap. 18.
14.8 Conclusions and Perspectives
Aquatic viral ecology is a relatively recent discipline. Pioneer
ecological and molecular researches in Lake Pavin have con-
tributed to demonstrate that viruses are omnipresent in
aquatic environments, including one of the most extreme
biotopes such as the dark permanently anoxic monimolimnic
waters and sediments of Lake Pavin. These environments are
highly selective for heterotrophic prokaryotes whose sea-
sonal activity offers an optimal and unique resource for
thriving viral communities, some of which may be endemic.
Because all types of cells in the nature have their specifi c
viruses and offer ecological niches to different viral life-
styles, viruses are considered the greatest reservoir of the
uncharacterized biological diversity on the earth, which is
being probed and described at an increasingly rapid rate,
almost exclusively with molecular sequence data. Studies in
Lake Pavin suffer from the lack of such attempts for the
exploration of viruses other than viruses of Bacteria and the
related functions, some of which may be crucial to get better
insights into global change processes (e.g. consumption and
production of greenhouse gas such as methane etc.), in the
seasonal successions of phytoplankton or zooplankton com-
munities, and the sudden mortality events affecting fi sh,
crustacean, mollusks, etc. For example, Hewson et al. ( 2013 )
recently used a metagenomic approach to identify circular,
single-stranded DNA viruses that may be involved in the sea-
sonal dynamics of Daphnia spp. in Oneida and Cayuga lakes
(upstate New York). Because Daphnia plays a critical role in
many lake ecosystems , such viruses may have important
effects on herbivory and thus carbon fl ow through the lake
ecosystem.
Our conceptual understanding of the function and regula-
tion of aquatic ecosystems, from microbial to global biogeo-
chemical processes, has changed with the study of viruses.
Viral-mediated prokaryotic mortality seems lower in Lake
Pavin but roughly equals bacterivory from protists in the
world aquatic ecosystems , which is a signifi cant departure
from the traditional view that predation and resource avail-
ability are the main factors controlling prokaryotic abun-
dance and production in pelagic systems. Viruses infl uence
both the retention and the export of organic matter in pelagic
environments, and thus affect the biogeochemical cycling of
the major conserved elements (C, N, P). Besides, given the
prevalence of phage-encoded biological functions within
host cells as attested by the substantial levels of lysogens in
Lake Pavin, and the occurrence of recombination between
phage and host genes, phage populations serve as gene reser-
voirs that contribute to niche partitioning of microbial spe-
cies in aquatic ecosystems. Viral-mediated gene transfers
include diverse mechanisms ( transduction , transforma-
tion , conjugation and recombination ) that are known to
affect gene evolution in the marine environment. It is thus
clear that most of the viruses are not pathogens but mutualis-
tic cell partners that provide helper functions, and this must
be included in the future agenda of viral studies in freshwater
ecosystems.Acknowledgements This study includes results from PhD and postdoc
researches supported by various instances: Région Auvergne, CNRS,
Université Blaise Pascal, French Ministère de la Recherche et de la
Technologie, and the Ministry of Culture, High School and Research of
Grand-Duché de Luxembourg. Part of the results presented, most of
which are detailed in different Chapters of this book, were obtained
with the collaboration of colleagues: G. Borrel, D. Debroas, F. Enault,
L. Jardillier, A. C. Lehours, V. Ravet, S. Roux. The study was also
granted from different sources: French National Programme EC2COT. Sime-Ngando et al.