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Off-axis symbiosis found: characterization and biogeography of bacterial symbionts of Bathymodiolus mussels from Lost City hydrothermal vents
Citation
DeChaine, EG and Bates, AE and Shank, TM and Cavanaugh, CM, Off-axis symbiosis found: characterization and biogeography of bacterial symbionts of Bathymodiolus mussels from Lost City hydrothermal vents, Environmental Microbiology, 8, (Annual) pp. 1902-1912. ISSN 1462-2912 (2006) [Refereed Article]
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The definitive published version is available online at: http://www3.interscience.wiley.com/
DOI: doi:10.1111/j.1462-2920.2005.01113.x
Abstract
Organisms at hydrothermal vents inhabit discontinuous
chemical ‘islands’ along mid-ocean ridges, a scenario
that may promote genetic divergence among
populations. The 2003 discovery of mussels at the
Lost City Hydrothermal Field provided a means of
evaluating factors that govern the biogeography of
symbiotic bacteria in the deep sea. The unusual
chemical composition of vent fluids, the remote location,
and paucity of characteristic vent macrofauna at
the site, raised the question of whether microbial
symbioses existed at the extraordinary Lost City. If
so, how did symbiotic bacteria therein relate to those
hosted by invertebrates at the closest known hydrothermal
vents along the Mid-Atlantic Ridge (MAR)? To
answer these questions, we performed microscopic
and molecular analyses on the bacteria found within
the gill tissue of Bathymodiolus mussels (Mytilidae,
Bathymodiolinae) that were discovered at the Lost
City. Here we show that Lost City mussels harbour
chemoautotrophic and methanotrophic endosymbionts
simultaneously. Furthermore, populations of
the chemoautotrophic symbionts from the Lost City
and two sites along the MAR are genetically distinct
from each other, which suggests spatial isolation of
bacteria in the deep sea. These findings provide new
insights into the processes that drive diversification
of bacteria and evolution of symbioses at hydrothermal
vents.
Introduction
Recent evidence suggests that microbial populations in
spatially and chemically fragmented habitats exhibit geographic
structure (Papke et al., 2003; Whitaker et al.,
2003) rather than being distributed ubiquitously as previously
hypothesized (see Finlay, 2002; Fenchel, 2003).
The patchy mosaic of populations in heterogeneous environments
restricts gene flow, while promoting genetic differentiation
and local adaptation (Slatkin, 1987). Due to
the heterogeneous nature of hydrothermal vent environments,
chemosynthetic bacteria inhabiting vents probably
have geographically structured populations as well. If so,
this would have direct implications for how topographic
features of the seafloor, deep-ocean currents, and chemically
variable environments impact the evolution and
diversity of bacteria, the origin and evolution of bacteriavent
invertebrate symbioses, and the assemblage of
hydrothermal vent communities.
The fragmented distribution of deep-sea hydrothermal
vents lies in stark contrast to the uniform conditions of the
marine abyssal zone (Tunnicliffe, 1988; 1991; Tunnicliffe
and Fowler, 1996; Van Dover, 2000). Discrete hydrothermal
vent fields are comparable to islands, distributed in a
spatially, chemically and temporally patchy chain along
the deep-sea ridges and remote, off-axis sites (Tunnicliffe,
1988; 1991; Tunnicliffe and Fowler, 1996; Tunnicliffe
et al., 1998; Van Dover et al., 2002). Differences between
ridges in geography, tectonic activity, age of spreading
centre, and connectedness of ridge segments likely play a
major role in regulating gene flow among populations
(Vrijenhoek, 1997; Van Dover et al., 2002; Hurtado et al.,
2003), the distribution of vent macrofauna (Van Dover,
1995; Tunnicliffe and Fowler, 1996; Juniper and Tunnicliffe,
1997), and the composition of ecological communities
(Tunnicliffe, 1991). For example, ‘fracture zones’
(Fig. 1) likely inhibit dispersal of larvae by separating ridge
segments that are undergoing independent volcanic evolution
(Van Dover et al., 2002). Though associations
between chemosynthetic bacteria and their invertebrate
hosts provide the basis for macrofaunal production at
deep-sea hydrothermal vents, almost nothing is known
about the distribution of genetic variation in the symbionts
and how population structure of bacteria affects
Item Details
Item Type: | Refereed Article |
---|---|
Research Division: | Biological Sciences |
Research Group: | Evolutionary biology |
Research Field: | Host-parasite interactions |
Objective Division: | Environmental Management |
Objective Group: | Marine systems and management |
Objective Field: | Marine biodiversity |
UTAS Author: | Bates, AE (Dr Amanda Bates) |
ID Code: | 76503 |
Year Published: | 2006 |
Web of Science® Times Cited: | 49 |
Deposited By: | Sustainable Marine Research Collaboration |
Deposited On: | 2012-03-07 |
Last Modified: | 2012-04-04 |
Downloads: | 0 |
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