Dual Symbiosis in a Bathymodiolus sp. Mussel from a Methane Seep on the Gabon Continental Margin (Southeast Atlantic): 16S rRNA Phylogeny and Distribution of the Symbionts in Gills

IFREMER Départment Environnement Profond, Centre de Brest, Plouzané, Germany.
Applied and Environmental Microbiology (Impact Factor: 3.67). 05/2005; 71(4):1694-700. DOI: 10.1128/AEM.71.4.1694-1700.2005
Source: PubMed

ABSTRACT Deep-sea mussels of the genus Bathymodiolus (Bivalvia: Mytilidae) harbor symbiotic bacteria in their gills and are among the dominant invertebrate species at cold seeps
and hydrothermal vents. An undescribed Bathymodiolus species was collected at a depth of 3,150 m in a newly discovered cold seep area on the southeast Atlantic margin, close
to the Zaire channel. Transmission electron microscopy, comparative 16S rRNA analysis, and fluorescence in situ hybridization
indicated that this Bathymodiolus sp. lives in a dual symbiosis with sulfide- and methane-oxidizing bacteria. A distinct distribution pattern of the symbiotic
bacteria in the gill epithelium was observed, with the thiotrophic symbiont dominating the apical region and the methanotrophic
symbiont more abundant in the basal region of the bacteriocytes. No variations in this distribution pattern or in the relative
abundances of the two symbionts were observed in mussels collected from three different mussel beds with methane concentrations
ranging from 0.7 to 33.7 μM. The 16S rRNA sequence of the methanotrophic symbiont is most closely related to those of known
methanotrophic symbionts from other bathymodiolid mussels. Surprisingly, the thiotrophic Bathymodiolus sp. 16S rRNA sequence does not fall into the monophyletic group of sequences from thiotrophic symbionts of all other Bathymodiolus hosts. While these mussel species all come from vents, this study describes the first thiotrophic sequence from a seep mussel
and shows that it is most closely related (99% sequence identity) to an environmental clone sequence obtained from a hydrothermal
plume near Japan.

Download full-text


Available from: Nicole Dubilier, Sep 26, 2015
46 Reads
  • Source
    • "To establish whether previously identified bacterial Idas-symbiont phylotypes occur in these mussels, fluorescence in situ hybridisations (FISH) were performed on a subsample of unstained 1e2- mm whole-specimen LR white sections, employing dualehybridisation combinations (Cy3 and Cy5-labelled probes) of the general eubacterial probe EUB338 (Amann et al., 1990), the nonsense probe NON338 (Wallner et al., 1993), and specific oligonucleotide probes initially designed to target various symbiont 16S rRNA phylotypes identified in I. modiolaeformis and B. heckerae. These probes target M1 methanotrophs (probe ImedM-138), M2 methylotrophs (probe BhecM2-822), and the two phylotypes of sulphur oxidizers T1 and T2 (probes Bthio-193 and ImedT2-193, respectively, details in Duperron et al., 2008) following the postpermeabilisation steps only of the FISH protocol in Duperron et al. (2005). Slides were photographed as in the H & E analysis, but with a monochrome filter. "
    [Show abstract] [Hide abstract]
    ABSTRACT: Symbioses between microbiota and marine metazoa occur globally at chemosynthetic habitats facing imminent threat from anthropogenic disturbance, yet little is known concerning the role of symbiosis during early development in chemosymbiotic metazoans: a critical period in any benthic species' lifecycle. The emerging symbiosis of Idas (sensu lato) simpsoni mussels undergoing development is assessed over a post-larval-to-adult size spectrum using histology and fluorescence in situ hybridisation (FISH). Post-larval development shows similarities to that of both heterotrophic and chemosymbiotic mussels. Data from newly settled specimens confirm aposymbiotic, planktotrophic larval development. Sulphur-oxidising (SOX) symbionts subsequently colonise multiple exposed, non-ciliated epithelia shortly after metamorphosis, but only become abundant on gills as these expand with greater host size. This wide-spread bathymodiolin recorded from sulphidic wood, bone and cold-seep habitats, displays a suite of adaptive traits that could buffer against anthropogenic disturbance. Copyright © 2015 Elsevier Ltd. All rights reserved.
    Marine Environmental Research 07/2015; DOI:10.1016/j.marenvres.2015.07.014 · 2.76 Impact Factor
  • Source
    • "The presence of methanotrophic and thiotrophic bacterial endosymbiont in B. azoricus gill tissue was determined according to Duperron et al. (2005) with slight modifications [15] [23]. Gill tissues were fixed in 5% buffered formalin and processed for paraffin embedding according to standard protocol. "
    [Show abstract] [Hide abstract]
    ABSTRACT: Deep-sea hydrothermal vents are extreme habitats that are distributed worldwide in association with volcanic and tectonic events, resulting thus in the establishment of particular environmental conditions, in which high pressure, steep temperature gradients, and potentially toxic concentrations of sulfur, methane and heavy metals constitute driving factors for the foundation of chemosynthetic-based ecosystems. Of all the different macroorganisms found at deep-sea hydrothermal vents, the mussel Bathymodiolus azoricus is the most abundant species inhabiting the vent ecosystems from the Mid-Atlantic Ridge (MAR). In the present study, the effect of long term acclimatization at atmospheric pressure on host-symbiotic associations were studied in light of the ensuing physiological adaptations from which the immune and endosymbiont gene expressions were concomitantly quantified by means of real-time PCR.
    Fish &amp Shellfish Immunology 11/2014; 42(1):159-170. DOI:10.1016/j.fsi.2014.10.018 · 2.67 Impact Factor
  • Source
    • "m À 2 ), and cover large areas paved with authigenic carbonate crusts (up to 1400 m 2 ) within the pockmark (Olu-LeRoy et al., 2007; Marcon et al., 2014). Specimens were part of a large bush sampled using a BushMaster device (Penn State University, C.R. Fisher) manipulated by the arm of the ROV Victor6000 (dive 426; 5.7981S, 9.7111E, 3152 m depth) in the central zone of the pockmark (Duperron et al., 2005; Olu-LeRoy et al., 2007; Cowart et al., 2013). Hydrogen sulfide is undetectable in bottom waters at Regab, but present in anoxic methane-rich sediment below the seawater/sediment interface (Olu-LeRoy et al., 2007; Cambon- Bonavita et al., 2009; Ristova et al., 2012). "
    [Show abstract] [Hide abstract]
    ABSTRACT: Tubeworms within the annelid family Siboglinidae rely on sulfur-oxidizing autotrophic bacterial symbionts for their nutrition, and are among the dominant metazoans occurring at deep-sea hydrocarbon seeps. Contrary to their relatives from hydrothermal vents, sulfide uptake for symbionts occurs within the anoxic subsurface sediment, in the posterior 'root' region of the animal. This study reports on an integrated microbiological and geochemical investigation of the cold seep tubeworm Escarpia southwardae collected at the Regab pockmark (Gulf of Guinea). Our aim was to further constrain the links between the animal and its symbiotic bacteria, and their environment. We show that E. southwardae harbors abundant sulfur-oxidizing bacterial symbionts in its trophosome. Symbionts are able to fix inorganic carbon using the Calvin-Benson cycle, as reported in most other Siboglinidae, but can also use the reverse Tricarboxilic Acid Cycle. Surprisingly, the observed bacteria appear to be more closely related to symbionts of Escarpia and Lamellibrachia species from very distant sites located in the Gulf of Mexico and eastern Pacific, than to symbionts of a siboglinid occurring at a nearby methane seep site, only a few hundred km away from Regab. Then, by combining scanning electron microscopy and trace element (Mn, Fe, Sr, Zr) analyses of E. southwardae tube, we also show that two distinct oxidation fronts occur along the tube. The first one, near the posterior end of the tube, corresponds to the interface between oxic bottom waters and the underlying anoxic sediment. In contrast, the second redox front is located in the most anterior part of the tube, and could result from active oxygen uptake by the plume of the tubeworm. We speculate that intense oxygen consumption in this region could create favorable conditions for sulfate reduction by specialized bacteria associated with the plume, possibly leading to an additional source of dissolved sulfide that would further enhance the productivity of bacterial symbionts.
Show more