High occurrence of viruses in the mucus layer of
scleractinian corals
Hanh Nguyen-Kim,
1,2
Thierry Bouvier,
1
Corinne Bouvier,
1
Hai Doan-Nhu,
2
Lam Nguyen-Ngoc,
2
Emma Rochelle-Newall,
3
Anne-Claire Baudoux,
4
Christelle Desnues,
5
Stéphanie Reynaud,
6
Christine Ferrier-Pages
6
and
Yvan Bettarel
1
*
1
Institute of Research for Development (IRD), CNRS,
ECOSYM, Montpellier, France.
2
Institute of Oceanography of Nha Trang, VAST,
Viet Nam.
3
IRD, BIOEMCO, Paris, France.
4
CNRS, AD2M, Roscoff, France.
5
CNRS, URMITE, Marseille, France.
6
Scientific Center of Monaco (CSM), Monaco.
Summary
Viruses attract increasing interest from environmen-
tal microbiologists seeking to understand their func-
tion and role in coral health. However, little is known
about their main ecological traits within the coral
holobiont. In this study, a quantitative and qualitative
characterization of viral and bacterial communities
was conducted on the mucus of seven different coral
species of the Van Phong Bay (Vietnam). On average,
the concentrations of viruses and bacteria were,
respectively, 17- and twofold higher in the mucus
than in the surrounding water. The examination of
bacterial community composition also showed
remarkable differences between mucus and water
samples. The percentage of active respiring cells was
nearly threefold higher in mucus (m = 24.8%) than in
water (m = 8.6%). Interestingly, a positive and highly
significant correlation was observed between the
proportion of active cells and viral abundance in the
mucus, suggesting that the metabolism of the bacte-
rial associates is probably a strong determinant
of the distribution of viruses within the coral
holobiont. Overall, coral mucus, given its unique
physicochemical characteristics and sticking proper-
ties, can be regarded as a highly selective biotope for
abundant, diversified and specialized symbiotic
microbial and viral organisms.
Introduction
Prokaryotes play a pivotal role in the health of reef eco-
systems because they provide scleractinian corals with
crucial ecological services (Ceh et al., 2013), including
protection from pathogen colonization (Krediet et al.,
2013) and nutrition (Rosenberg et al., 2009). However,
these prokaryote associates have been shown to
be highly susceptible to environmental perturbations
(increased temperature, chemical pollutants, changes in
nutrients, salinity, pH, etc.), and changes in their compo-
sition and/or physiology may directly or indirectly affect
scleractinian metabolism, as postulated in the probiotic
theory of coral diseases (Reshef et al., 2006). Recently,
other (biological) sources of prokaryotic mortality have
been identified within the coral holobiont. For example,
the discovery of virus occurrence in coral tissues (Bettarel
et al., 2012), mucus (Davy and Patten, 2007) and skel-
eton (Vega Thurber et al., 2008) has raised a number of
questions regarding their effective roles in coral health,
which could be ambivalent. Indeed, viruses could either
cause profound changes in the commensal prokaryotic
and eukaryotic communities, which may lead to coral
disfunctioning or diseases (van Oppen et al., 2009), or
conversely act as a natural phage therapy for diseased
scleractinians by removing bacterial pathogens (Atad
et al., 2012; Cohen et al., 2013).
Despite their potentially decisive role in coral health,
viruses remain surprisingly understudied (Garren and
Azam, 2012). Viral functions and ecological traits in wild
corals are still poorly understood, and so are their specific
interactions with the various members of the coral
holobiont. Prior to evaluating their potential role, there is
an urgent need for basic ecological information, such as
their in situ abundance in corals, their variability among the
large diversity of scleractinian species, their colonization
processes and the ecological links with their hosts.
In this study, the specific objectives were to (i) deter-
mine the concentrations of coral-associated viruses in the
superficial mucus layer of seven different scleractinian
species (Favia truncatus, Acropora aculeus, Platygyra
pini, Montastrea colemani, Acropora muricata, Favites
Received 13 February, 2014; accepted 26 March, 2014. *For corre-
spondence. E-mail yvan.bettarel@ird.fr; Tel. +84 1 695 437 450; Fax
+84 4 373 467 14.
Environmental Microbiology Reports (2014) doi:10.1111/1758-2229.12185
© 2014 Society for Applied Microbiology and John Wiley & Sons Ltd