Dataset Information

Genetic diversity and demographic instability in Riftia pachyptila tubeworms from eastern Pacific hydrothermal vents.

ABSTRACT: BACKGROUND:Deep-sea hydrothermal vent animals occupy patchy and ephemeral habitats supported by chemosynthetic primary production. Volcanic and tectonic activities controlling the turnover of these habitats contribute to demographic instability that erodes genetic variation within and among colonies of these animals. We examined DNA sequences from one mitochondrial and three nuclear gene loci to assess genetic diversity in the siboglinid tubeworm, Riftia pachyptila, a widely distributed constituent of vents along the East Pacific Rise and Galápagos Rift. RESULTS:Genetic differentiation (F(ST)) among populations increased with geographical distances, as expected under a linear stepping-stone model of dispersal. Low levels of DNA sequence diversity occurred at all four loci, allowing us to exclude the hypothesis that an idiosyncratic selective sweep eliminated mitochondrial diversity alone. Total gene diversity declined with tectonic spreading rates. The southernmost populations, which are subjected to superfast spreading rates and high probabilities of extinction, are relatively homogenous genetically. CONCLUSIONS:Compared to other vent species, DNA sequence diversity is extremely low in R. pachyptila. Though its dispersal abilities appear to be effective, the low diversity, particularly in southern hemisphere populations, is consistent with frequent local extinction and (re)colonization events.

SUBMITTER: Coykendall DK

PROVIDER: S-EPMC3100261 | biostudies-literature | 2011 Apr

REPOSITORIES: biostudies-literature

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Genetic diversity and demographic instability in Riftia pachyptila tubeworms from eastern Pacific hydrothermal vents.

Coykendall D Katharine DK Johnson Shannon B SB Karl Stephen A SA Lutz Richard A RA Vrijenhoek Robert C RC

BMC evolutionary biology 20110413

<h4>Background</h4>Deep-sea hydrothermal vent animals occupy patchy and ephemeral habitats supported by chemosynthetic primary production. Volcanic and tectonic activities controlling the turnover of these habitats contribute to demographic instability that erodes genetic variation within and among colonies of these animals. We examined DNA sequences from one mitochondrial and three nuclear gene loci to assess genetic diversity in the siboglinid tubeworm, Riftia pachyptila, a widely distributed ...[more]

PMID: 21489281

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Project description:BackgroundThe inhabitants of deep-sea hydrothermal vents occupy ephemeral island-like habitats distributed sporadically along tectonic spreading-centers, back-arc basins, and volcanically active seamounts. The majority of vent taxa undergo a pelagic larval phase, and thus varying degrees of geographical subdivision, ranging from no impedance of dispersal to complete isolation, often exist among taxa that span common geomorphological boundaries. Two lineages of Bathymodiolus mussels segregate on either side of the Easter Microplate, a boundary that separates the East Pacific Rise from spreading centers connected to the Pacific-Antarctic Ridge.ResultsA recent sample from the northwest flank of the Easter Microplate contained an admixture of northern and southern mitochondrial haplotypes and corresponding alleles at five nuclear gene loci. Genotypic frequencies in this sample did not fit random mating expectation. Significant heterozygote deficiencies at nuclear loci and gametic disequilibria between loci suggested that this transitional region might be a 'Tension Zone' maintained by immigration of parental types and possibly hybrid unfitness. An analysis of recombination history in the nuclear genes suggests a prolonged history of parapatric contact between the two mussel lineages. We hereby elevate the southern lineage to species status as Bathymodiolus antarcticus n. sp. and restrict the use of Bathymodiolus thermophilus to the northern lineage.ConclusionsBecause B. thermophilus s.s. exhibits no evidence for subdivision or isolation-by-distance across its 4000 km range along the EPR axis and Galápagos Rift, partial isolation of B. antarcticus n. sp. requires explanation. The time needed to produce the observed degree of mitochondrial differentiation is consistent with the age of the Easter Microplate (2.5 to 5.3 million years). The complex geomorphology of the Easter Microplate region forces strong cross-axis currents that might disrupt self-recruitment of mussels by removing planktotrophic larvae from the ridge axis. Furthermore, frequent local extinction events in this tectonically dynamic region might produce a demographic sink rather than a source for dispersing mussel larvae. Historical changes in tectonic rates and current patterns appear to permit intermittent contact and introgression between the two species.

Project description:BackgroundChemolithoautotrophic primary production sustains dense invertebrate communities at deep-sea hydrothermal vents and hydrocarbon seeps. Symbiotic bacteria that oxidize dissolved sulfur, methane, and hydrogen gases nourish bathymodiolin mussels that thrive in these environments worldwide. The mussel symbionts are newly acquired in each generation via infection by free-living forms. This study examined geographical subdivision of the thiotrophic endosymbionts hosted by Bathymodiolus mussels living along the eastern Pacific hydrothermal vents. High-throughput sequencing data of 16S ribosomal RNA encoding gene and fragments of six protein-coding genes of symbionts were examined in the samples collected from nine vent localities at the East Pacific Rise, Galápagos Rift, and Pacific-Antarctic Ridge.ResultsBoth of the parapatric sister-species, B. thermophilus and B. antarcticus, hosted the same numerically dominant phylotype of thiotrophic Gammaproteobacteria. However, sequences from six protein-coding genes revealed highly divergent symbiont lineages living north and south of the Easter Microplate and hosted by these two Bathymodiolus mussel species. High heterogeneity of symbiont haplotypes among host individuals sampled from the same location suggested that stochasticity associated with initial infections was amplified as symbionts proliferated within the host individuals. The mussel species presently contact one another and hybridize along the Easter Microplate, but the northern and southern symbionts appear to be completely isolated. Vicariance associated with orogeny of the Easter Microplate region, 2.5-5.3 million years ago, may have initiated isolation of the symbiont and host populations. Estimates of synonymous substitution rates for the protein-coding bacterial genes examined in this study were 0.77-1.62%/nucleotide/million years.ConclusionsOur present study reports the most comprehensive population genetic analyses of the chemosynthetic endosymbiotic bacteria based on high-throughput genetic data and extensive geographical sampling to date, and demonstrates the role of the geographical features, the Easter Microplate and geographical distance, in the intraspecific divergence of this bacterial species along the mid-ocean ridge axes in the eastern Pacific. Altogether, our results provide insights into extrinsic and intrinsic factors affecting the dispersal and evolution of chemosynthetic symbiotic partners in the hydrothermal vents along the eastern Pacific Ocean.

Project description:Genome and proteome data predict the presence of both the reductive citric acid cycle (rCAC; also called the reductive tricarboxylic acid cycle) and the Calvin-Benson-Bassham cycle (CBB) in "Candidatus Endoriftia persephonae," the autotrophic sulfur-oxidizing bacterial endosymbiont from the giant hydrothermal vent tubeworm Riftia pachyptila. We tested whether these cycles were differentially induced by sulfide supply, since the synthesis of biosynthetic intermediates by the rCAC is less energetically expensive than that by the CBB. R. pachyptila was incubated under in situ conditions in high-pressure aquaria under low (28 to 40 μmol · h-1) or high (180 to 276 μmol · h-1) rates of sulfide supply. Symbiont-bearing trophosome samples excised from R. pachyptila maintained under the two conditions were capable of similar rates of CO2 fixation. Activities of the rCAC enzyme ATP-dependent citrate lyase (ACL) and the CBB enzyme 1,3-bisphosphate carboxylase/oxygenase (RubisCO) did not differ between the two conditions, although transcript abundances for ATP-dependent citrate lyase were 4- to 5-fold higher under low-sulfide conditions. δ13C values of internal dissolved inorganic carbon (DIC) pools were varied and did not correlate with sulfide supply rate. In samples taken from freshly collected R. pachyptila, δ13C values of lipids fell between those collected for organisms using either the rCAC or the CBB exclusively. These observations are consistent with cooccurring activities of the rCAC and the CBB in this symbiosis. IMPORTANCE Previous to this study, the activities of the rCAC and CBB in R. pachyptila had largely been inferred from "omics" studies of R. pachyptila without direct assessment of in situ conditions prior to collection. In this study, R. pachyptila was maintained and monitored in high-pressure aquaria prior to measuring its CO2 fixation parameters. Results suggest that ranges in sulfide concentrations similar to those experienced in situ do not exert a strong influence on the relative activities of the rCAC and the CBB. This observation highlights the importance of further study of this symbiosis and other organisms with multiple CO2-fixing pathways, which recent genomics and biochemical studies suggest are likely to be more prevalent than anticipated.

Dataset Information

Genetic diversity and demographic instability in Riftia pachyptila tubeworms from eastern Pacific hydrothermal vents.

Publications

Genetic diversity and demographic instability in Riftia pachyptila tubeworms from eastern Pacific hydrothermal vents.

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