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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:Environment
Objective Group:Flora, Fauna and Biodiversity
Objective Field:Marine Flora, Fauna and Biodiversity
Author:Bates, AE (Dr Amanda Bates)
ID Code:76503
Year Published:2006
Web of Science® Times Cited:44
Deposited By:Sustainable Marine Research Collaboration
Deposited On:2012-03-07
Last Modified:2012-04-04
Downloads:0

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