Off‐axis symbiosis found: characterization and biogeography of bacterial symbionts of Bathymodiolus mussels from Lost City hydrothermal vents

Amanda E Bates,Colleen M Cavanaugh,Timothy M Shank,Eric G Dechaine

doi:10.1111/j.1462-2920.2005.01113.x

Amanda E Bates, Colleen M Cavanaugh + Show 2 more

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https://doi.org/10.1111/j.1462-2920.2005.01113.x

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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.

Highlights

Recent evidence suggests that microbial populations in spatially and chemically fragmented habitats exhibit geographic structure (Whitaker et al, 2003; Papke et al., 2003) rather than being distributed ubiquitously as previously hypothesized
Characterization of the Lost City symbiosis. This characterization, which constitutes the first description of a symbiosis from the LC, revealed two morphologically distinct Gram negative bacteria in the mussel bacteriocytes, gill epithelial cells specialized for housing symbiotic bacteria (Fig. 2a)
Sequence alignments revealed that the symbiont phylotypes from the Lost City (Genbank accession numbers A and B) were identical to two phylogenetically distinct lineages of γ-Proteobacteria, a chemoautotroph and a methanotroph, previously found in both B

Summary

Introduction

Recent evidence suggests that microbial populations in spatially and chemically fragmented habitats exhibit geographic structure (Whitaker et al, 2003; Papke et al., 2003) rather than being distributed ubiquitously as previously hypothesized (see Finlay2002; Fenchel 2003). 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 bacteria-vent invertebrate symbioses, and the assemblage of hydrothermal vent communities. 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)

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