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Bacterial symbionts and mineral deposits in the branchial chamber of the hydrothermal vent shrimp AQUATIC BIOLOGY
Aquat Biol
Vol. 1: 225238, 2008
doi: 10.3354/ab00024
Published online January 15, 2008
INTRODUCTION
The discovery of deep-sea hydrothermal vents in
1977 revealed many new animals that derive their
nutrition from chemoautotrophic bacteria, housed in a
variety of tissues and structures (Cavanaugh et al.
2006). The caridean hydrothermal vent shrimp
Rimi-
caris exoculata (Williams & Rona 1986) is one species
that dominates the fauna at several Mid-Atlantic Ridge
(MAR) vent sites. It forms large swarms on the chimney
walls, reaching densities of up to 2500 ind. m
2
(Des-
bruyères et al. 2001).
R. exoculata possesses an en-
larged gill chamber, housing an abundant community
of bacteria, mostly distributed on bacteriophore setae
of the shrimp mouthparts (i.e. scaphognathites, exo-
podites of the first maxilliped) and on the inner side of
the gill chamber (Casanova et al. 1993). Although
several morphotypes have been observed in electron
microscopy, the bacteria are described as a mono-
culture of a single phylotype of epsilon-Proteobacteria
(Polz & Cavanaugh 1995). Their appearance, abun-
dance, and attachment to the cuticle suggest an ecto-
symbiosis (Van Dover et al. 1988, Casanova et al. 1993,
Segonzac et al. 1993). Several studies (Wirsen et al.
1993, Polz & Cavanaugh 1995) suggesting that the bac-
terial symbionts acquire energy from sulphide oxidation
© Inter-Research 2008 · www.int-res.com
*Email: lcorbari@ulg.ac.be
Bacterial symbionts and mineral deposits in the
branchial chamber of the hydrothermal vent shrimp
Rimicaris exoculata: relationship to moult cycle
Laure Corbari
1,
*, Magali Zbinden
2
, Marie-Anne Cambon-Bonavita
3
,
Françoise Gaill
2
, Philippe Compère
1
1
Université de Liège, Laboratoire de Morphologie Fonctionnelle et Évolutive, Unité de Morphologie Ultrastructurale,
Allée de la Chimie, 3, 4000 Liège, Belgium
2
UMR CNRS 7138 Systématique, Adaptation et Evolution, Université Pierre et Marie Curie, 7 Quai St Bernard, Bâtiment A,
75252 Paris Cedex 05, France
3
Laboratoire de Microbiologie et Biotechnologie des Extrêmophiles, IFREMER, Centre de Brest, BP 70, 29280 Plouzané, France
ABSTRACT: The shrimp
Rimicaris exoculata is considered a primary consumer that dominates the
fauna of most Mid-Atlantic Ridge hydrothermal ecosystems. The shrimps harbour in their gill
chamber an important ectosymbiotic community of chemoautotrophic bacteria associated with iron
oxide deposits. The settlement and development of this ectosymbiosis was investigated using micro-
scopy techniques (light microscopy, LM; and scanning, transmission and environmental scanning
electron microscopy: SEM and ESEM, respectively) for shrimps from 2 different vent fields (Rainbow,
36° 14.0 N and TAG, 26° 08.0 N). The results revealed a bacterial re-colonisation after each exuvia-
tion and a development of the bacterial community in 5 steps in relation to the moult stages, which
were used as a reference time scale. In 287 shrimps from both vent fields, pre-ecdysial stages pre-
vailed in the population, suggesting a short anecdysis and high moulting rate, probably to renew the
ectosymbiosis. Comparisons with moult cycles of littoral shrimps suggest that the interval between
successive exuviations in
R. exoculata may be as short as 10 d. The colours of R. exoculata result from
accumulation of iron oxide, which forms a bacteria-associated mineral crust in the gill chambers. The
close correspondence between moult stages, the development of the ectosymbiont community and
shrimp colours indicate that colour could be used to rapidly determine shrimp moult stages.
KEY WORDS: Hydrothermal vents · Shrimp · Moult cycle · Ectosymbiosis · Iron oxides
Resale or republication not permitted without written consent of the publisher
O
PEN
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A
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CCESS Aquat Biol 1: 225238, 2008
have not been experimentally confirmed. The defini-
tive role of these bacteria has still not been clarified, al-
though ectosymbionts have often been considered part
of the shrimp diet. Shrimp could feed directly on the
bacterial ectosymbionts by grazing on them inside the
gill chamber, as indicated by stable isotope measure-
ments (Gebruk et al. 1993, Rieley et al. 1999), but the
bacteria in the shrimp mid-gut have also been proposed
as an alternative nutritional source (Pond et al. 1997,
Polz et al. 1998, Zbinden & Cambon-Bonavita 2003).
In previous studies the presence has been observed
of red-brown mineral deposits in the gill chamber of
Rimicaris exoculata, including mouthparts and bran-
chiostegites (Gloter et al. 2004, Zbinden et al. 2004).
These deposits have been identified as hydrous iron
oxide in the form of ferrihydrite (Gloter et al. 2004).
Because of their close association with the bacterial
cell walls, these minerals have been hypothesised to
result from bacterial metabolism, suggesting, there-
fore, the presence of chemoautotrophic iron-oxidisers
among the bacterial community (Zbinden et al. 2004).
Macroscopically, these iron oxides deposited in the gill
chamber generate different shrimp colours (Zbinden et
al. 2004). For instance, shrimps from the Rainbow vent
site exhibit rusty or red hues, while those from the TAG
vent site appear mostly dark or black and rusty brown
(Gebruk et al. 1993, Zbinden et al. 2004). Changes in
iron oxide organization, structure, and abundance are
probably responsible for these colour changes.
Zbinden et al. (2004) described 3 bacterial morpho-
types (rods, thin and thick filaments) and mapped
these bacteria and associated minerals within the
whole gill chamber, including the mouthparts, by sub-
dividing the chamber into 3 functional compartments
(Fig. 1), considered as distinct microenvironments:
(1) the lower pre-branchial chamber, which houses
bacteria but few minerals, (2) the true branchial
chamber, which contains the gills but is free of bacteria
and minerals, and (3) the upper prebranchial chamber,
housing most of the bacteria and associated minerals.
Zbinden et al. (2004) were the first authors to suggest
that the abundance of bacteria and associated minerals
could be related to the shrimp moult cycle, because the
bacteria are directly attached to the cuticle which is
shed at ecdysis and subsequently renewed, as is the
case in all arthropods (Drach 1939; see review in
Charmantier-Daures & Vernet 2004, Compère et al.
2004). Thus, bacterial re-colonisation must occur after
each exuviation.
The aim of the present study was to follow the
bacterial re-colonisation of the gill chamber and the
progress of the mineralbacteria association between 2
successive moults, in
Rimicaris exoculata shrimps from
2 MAR hydrothermal vent sites, Rainbow and TAG.
These observations have been related to the moult
stages and the external colour of the shrimps, in an
attempt to provide a relative and/or an absolute time
scale for bacterial colonisation and mineral deposition.
MATERIALS AND METHODS
Shrimp collection.
Specimens of
Rimicaris exoculata
(Williams & Rona 1986) were collected during the
French EXOMAR cruise (August 2005) to the Rain-
bow (36° 14.0 N, 2300 m depth) and TAG (26° 08.0 N,
3600 m depth) hydrothermal vent sites on the MAR.
A suction sampler on the ROV (remotely operated
226
Fig. 1.
Rimicaris exoculata. Colour patterns: (A) speci-
men with white branchiostegites; and (B) specimen
with red branchiostegites. (C) Schematic view of the
gill chamber showing the disposition of the scaphog-
nathite (sc) and the exopodite of the 1st maxilliped
(ex) as well as the location of its 3 functional compart-
ments (1) lower pre-branchial chamber; (2) true gill
chamber facing the gills; (3) upper pre-branchial
chamber. The dotted lines delimit the observed area
(median zone) with predominant bacterial colonisation
(redrawn from Zbinden et al. 2004) Corbari et al.: Ectosymbiosis and moult cycle in vent shrimp
vehicle) Victor 6000 was used, operating from the
RV Atalante. Immediately after retrieval, entire living
specimens were dissected into body parts (e.g.
branchiostegites, tail) and fixed onboard in a solution
of 2.5% glutaraldehyde in a mixture of seawater (salin-
ity 33 ) and freshwater (dilution 7/10 at pH 7.2).
Moult stages and colour categories.
The moult
stages of 143 ind. of
Rimicaris exoculata from Rainbow
and 144 ind. from TAG were determined according
to the Drach & Tchernigovtzeff (1967) moult-staging
method, based on the development of setae matrices
along the uropod borders and on the hardness of the
new cuticle. According to the common nomenclature
in use in decapod crustaceans (Charmantier-Daure