227rial fraction (0.2–1.2 μm fraction). Finally, we found that the
concentrations of 2–5 and 5–50 μm TEP were related to the
V max of glycolytic activities in the 1.2–5 μm and > 5 μm
fractions. This indicates that TEP-associated bacteria were
specialized bacteria of high hydrolytic capacity. It is note-
worthy however that the enhanced rates of enzymatic
activities associated with particles may be the result of
enzymes released by the grazing of bacterivorous protists.
V max values as well cell-specifi c activities were on average
highest in the 1.2–5 μm fraction, in which bacterivores are
often dominant (Carrias et al. 1996 ).
13.7 Flagellates-TEP Relationships
Freshwater heterotrophic nanofl agellates (HNF) consume
bacteria and, due to their high densities, they are considered
the main bacterivores in the pelagic food web (Carrias et al.
1996 ; Simek et al. 2000 ; Sherr and Sherr 2002 ). Assuming
that the activity of TEP-associated bacteria may stimulate
the growth rates of the free-living bacteria in the vicinity of
the particle, we hypothesized that HNF abundances could be
related to TEP densities and to attached bacteria density. In
Lake Pavin, HNF densities (total or taxon-specifi c) were
however uncorrelated to bacterial density within TEP as
expressed by coeffi cient a. However, during 2 years of the
study, HNF densities were highly correlated to TEP abun-
dances (r^2 = 0.63 in 2005 and 0.61 in 2006, P < 0.001 for both
years). In assessing factors that can control the dynamics of
HNF, the structure of the food web is frequently expected to
have a major impact. In particular, the top-down impact of
predators (ciliates and metazooplankton) is deemed an
important control mechanism of the seasonal dynamics of
free-living HNF in lakes (Weisse 1990 ; Carrias et al. 1998 ,
2001 ). To our knowledge, the role of particles has never been
evaluated, and there are still too few studies on the interac-
tions between protozoans and TEP. Our results suggest
freshwater HNF are at least partially dependent on TEP den-
sities. Particle distribution explained 63 % and 61 % of the
variability in HNF abundance in 2005 and 2006, respec-
tively. We thus conclude that TEP is a relevant factor of HNF
distribution during the spring diatom bloom in Lake Pavin.
Based on studies of organic aggregates in pelagic environ-
ments, it has been hypothesized that particles may be
involved in the growth of certain HNF species in pelagic
environments by grazing on particle-associated bacteria
(Caron et al. 1982 , 1986 ). In Lake Pavin, bodonids, Monas -
like cells and the small-sized dominant taxa are potentially
able to feed on attached bacteria. Given that they exhibit the
properties of gels (Passow 2002 ), TEP may constitute a
pelagic microhabitat protecting HNF against the ciliate and
metazoan predation, resulting in higher HNF densities dur-
ing spring plankton development. In addition, the smallest
TEP may be an alternative food resource for HNF during low
bacterial densities and/or periods of strong competition
between bacterivorous taxa.13.8 Conclusions
The inclusion of TEP in food webs will provide us a much
better understanding of ecosystem functioning. TEP contain
attached bacteria that exhibit pronounced differences com-
pared to free-living bacteria in the surrounding water.
Attached bacteria are more active and release inorganic
nutrients that can enhance the growth of phytoplankton. Both
attached and free bacteria (in the vicinity of the particle) con-
stitute prey for protozoa that in turn are grazed by zooplank-
ton. Finally, phytodretitus (mainly frustules of diatoms)
interact with TEP to form large organic aggregates or lake
snow that contribute to the sinking fl ux of matter in deep
aphotic layers and the related carbon pump. Thus, based on
the case study of Lake Pavin, we conclude that TEP are
microbial microhabitats of major importance for biogeo-
chemical cycles in the pelagic zone of aquatic ecosystems.Acknowledgement We are indebted to Dr Xavier MARI for a critical
review of the ms.References
Arnous M-B, Courcol N, Carrias J-F (2010) The signifi cance of
Transparent Exopolymer Particles in the vertical distribution of bac-
teria and Heterotrophic Nanofl agellates in Lake Pavin. Aquat Sci
72:245–253
Bockelmann U, Manz W, Neu TR, Szewzyk U (2000) Characterization
of the microbial community of lotic organic aggregates (river snow)
in the Elbe river of German by cultivation and molecular methods.
FEMS Microbiol Ecol 33:157–170
Brachvogel T, Schweitzer B, Simon M (2001) Dynamics and bacterial
colonization of microaggregates in a large mesotrophic lake. Aquat
Microb Ecol 26:23–35
Brümmer IHM, Fehr W, Wagner-Döbler I (2000) Biofi lm community
structure in polluted rivers: abundance of dominant phylogenetic
groups over a complete annual cycle. Appl Environ Microbiol
66:3789–3796
Caron DA, Davis PG, Madin LP, Sieburth JMN (1982) Heterotrophic
bacteria and bacterivorous protozoans in oceanic macroaggregates.
Science 218:795–797
Caron DA, Davis PG, Madin LP, Sieburth JMN (1986) Enrichment of
microbial populations in macroaggregates (marine snow) from sur-
face waters of the North Atlantic. J Mar Res 44:643–565
Carrias J-F, Amblard C, Bourdier G (1996) Protistan bacterivory in an
oligomesotrophic lake: importance of attached ciliates and fl agel-
lates. Microb Ecol 31:249–268
Carrias J-F, Amblard C, Bourdier G (1998) Seasonal dynamics of free
and attached heterotrophic nanofl agellates in an oligomesotrophic
lake. Freshw Biol 39:101–111
Carrias J-F, Thouvenot A, Amblard C, Sime-Ngando T (2001) Dynamics
and growth estimates of planktonic protists during early spring in
Lake Pavin (France). Aquat Microb Ecol 24:163–17413 The Signifi cance of Transparent Exopolymeric Particles (TEP) for Microorganisms in Lake Pavin