Physiological dynamics of chemosynthetic symbionts in hydrothermal vent snails

Abstract

Symbioses between invertebrate animals and chemosynthetic bacteria form the basis of hydrothermal vent ecosystems worldwide. In the Lau Basin, deep-sea vent snails of the genus Alviniconcha associate with either Gammaproteobacteria (A. kojimai, A. strummeri) or Campylobacteria (A. boucheti) that use sulfide and/or hydrogen as energy sources. While the A. boucheti host-symbiont combination (holobiont) dominates at vents with higher concentrations of sulfide and hydrogen, the A. kojimai and A. strummeri holobionts are more abundant at sites with lower concentrations of these reductants. We posit that adaptive differences in symbiont physiology and gene regulation might influence the observed niche partitioning between host taxa. To test this hypothesis, we used high-pressure respirometers to measure symbiont metabolic rates and examine changes in gene expression among holobionts exposed to in situ concentrations of hydrogen (H₂: ~25 µM) or hydrogen sulfide (H₂S: ~120 µM). The campylobacterial symbiont exhibited the lowest rate of H₂S oxidation but the highest rate of H₂ oxidation, with fewer transcriptional changes and less carbon fixation relative to the gammaproteobacterial symbionts under each experimental condition. These data reveal potential physiological adaptations among symbiont types, which may account for the observed net differences in metabolic activity and contribute to the observed niche segregation among holobionts.

Fig. 1. Oxidation and respiration rates for Alviniconcha species.

Mean mass-specific oxidation rates for (a) H₂ and (b) H₂S, as well as the mass-specific O₂ respiration rates for Alviniconcha species while oxidizing (c) H₂ or (d) H₂S. All mass-specific rates are expressed as per gram of wet gill tissue and their standard error are given.

Fig. 2. Carbon incorporation rates for Alviniconcha.

Mass-specific carbon incorporation rates (¹³C_inc) for Alviniconcha individuals when oxidizing (a) H₂ or (b) H₂S. Horizontal bars show the mean for each experiment and error bars show the 95% confidence intervals. All mass-specific rates are expressed as per gram of wet gill tissue.

Fig. 3. Transcriptome profiles for Alviniconcha species.

Transcriptome profiles for the (a) A. kojimai, (b) A. strummeri and (c) A. boucheti symbiont. Hypothetical genes are excluded from this plot for better visibility of gene expression status in other categories (see also Supplementary Fig. S6). Plotted values are TMM normalized TPMs.

Fig. 4. Differential gene expression in the sulfide treatment.

Differential gene expression in the sulfide treated symbionts of (a) A. kojimai, (b) A. strummeri, and (c) A. boucheti based on an adjusted p-value of 0.05. Hypothetical genes are excluded from this plot for better visibility of gene expression changes in other categories (see also Supplementary Fig. S7). Comparisons are relative to the acclimation control samples.

Fig. 5. Differential gene expression for selected functional categories in the sulfide treatment.

Differential gene expression for metabolic subcategories in the sulfide treated symbionts of (a) A. kojimai, (b) A. strummeri, and (c) A. boucheti based on an adjusted p-value of 0.05. Comparisons are relative to the acclimation control samples.

Fig. 6. Differential gene expression in the hydrogen treatment.

Differential gene expression in the hydrogen treated symbionts of (a) A. kojimai, (b) A. strummeri, and (c) A. boucheti based on an adjusted p-value of 0.05. Hypothetical genes are excluded from this plot for better visibility of gene expression changes in other categories (see also Supplementary Fig. S8). Comparisons are relative to the acclimation control samples.

Fig. 7. Differential gene expression for selected functional categories in the hydrogen treatment.

Differential gene expression for metabolic subcategories in the hydrogen treated symbionts of (a) A. kojimai and (b) A. strummeri based on an adjusted p-value of 0.05. No significant changes in expression were seen in the A. boucheti symbiont for these categories. Comparisons are relative to the acclimation control samples.