Composition and dynamics of the gill microbiota
of an invasive Indo-Pacific oyster in the eastern
Mediterranean Sea
Dror Zurel,
1,2
Yehuda Benayahu,
2
Amitai Or,
2
Amir Kovacs
3
and Uri Gophna
3
*
1
The Porter School of Environmental Studies, Tel Aviv
University, Ramat Aviv, Tel Aviv 69978, Israel.
Department of
2
Zoology and
3
Molecular Microbiology
and Biotechnology, George S. Wise Faculty of Life
Sciences, Tel Aviv University, Ramat Aviv, Tel Aviv
69978, Israel.
Summary
Gill bacterial communities of Chama pacifica, an Indo-
Pacific invasive oyster to the eastern Mediterranean
Sea, were compared with those of Chama savignyi, its
northern Red Sea congeneric species. Summer and
winter bacterial populations were characterized and
compared using 16S rDNA clone libraries, and sea-
sonal population dynamics were monitored by auto-
mated ribosomal intergenic spacer analysis (ARISA).
Clone libraries revealed a specific clade of bacteria,
closely related to marine endosymbionts from the
Indo-Pacific, found in both ecosystems, of which one
taxon was conserved in oysters from both sites. This
taxon was dominant in summer libraries and was
weakly present in winter ones, where other members
of this group were dominant. ARISA results revealed
significant seasonal variation in bacterial populations
of Mediterranean Sea oysters, as opposed to Red
Sea ones that were stable throughout the year. We
suggest that this conserved association between bac-
teria and oyster reflects either a symbiosis between
the oyster host and some of its bacteria, a co-invasion
of both parties, or both.
Introduction
Biological invasions in marine habitats represent a rec-
ognized worldwide threat to the integrity of native com-
munities, the economy and human health (e.g. Bax
et al., 2003; Streftaris et al., 2005; Galil, 2007; Rilov and
Crooks, 2009). Many factors have been found to affect
the success of invasion, such as the lack of predators in
the invaded ecosystem or physico–chemical conditions
that select against or in favour of the invader (reviewed
by Vermeij, 1996). One such factor is the presence of
microbial pathogens or mutualists that may affect the
invader’s success to survive and establish a community
in its target ecosystem. For example, the microsporidian
parasite Fibrillanosema crangonycis has been found to
promote the invasion of its North American amphipod
host Crangonyx pseudogracilis to the UK by altering the
host’s sex ratio towards more females (Galbreath et al.,
2004). Similarly, the shipworm Teredo navalis, hosts
cellulose-digesting symbiotic gill bacteria that allowed it
to bore into wooden substrates, such as the vessels
that have distributed this bivalve worldwide (Norman,
1977).
The eastern Mediterranean Sea (EMS) is susceptible to
biological invasions due to its location between the Atlan-
tic, Pontic and Erythrean regions, heavy maritime traffic,
and its coastal waters that are teeming with maricultured
organisms (Arvanitidis et al., 2006). The greatest influx of
invaders into the Mediterranean Sea resulted from the
opening of the Suez Canal in 1869, which allowed the
entry of Indo-Pacific and Erythrean biota (Por et al., 1972;
Galil, 2007). Several Mediterranean species have been
wholly or partially displaced by these invaders (Galil,
2007; Rilov and Crooks, 2009). Such is the case for the
Indo-Pacific oyster Chama pacifica (class Bivalvia, family
Chamidae), first recorded in the Mediterranean Sea by
Tillier and Bavay in 1905, and which has since outnum-
bered its indigenous congener C. gryphoides, which is
now hardly encountered due to the new invader that
has successfully replaced it (Mienis et al., 1993; Galil,
2007).
Chama pacifica has managed to thrive along the
Levantine basin (Mienis et al., 1993). Chamidae species
are commonly found attached to sub-littoral hard sub-
strata, in areas with low sedimentation, where they are
usually well hidden by overgrowing fouling organisms that
extend equally over the natural rocks and shells (Purchon
and Purchon, 1981). Previous studies on this species in
the Mediterranean Sea focused mainly on the structural
effects of C. pacifica on the invaded ecosystem, since it
Received 1 December, 2010; accepted 24 January, 2011. *For cor-
respondence. E-mail urigo@tauex.tau.ac.il; Tel. (+972) 3 6409988.
Environmental Microbiology (2011) 13(6), 1467–1476 doi:10.1111/j.1462-2920.2011.02448.x
© 2011 Society for Applied Microbiology and Blackwell Publishing Ltd