Metatranscriptional Response of Chemoautotrophic Ifremeria nautilei Endosymbionts to Differing Sulfur Regimes

Abstract

Endosymbioses between animals and chemoautotrophic bacteria are ubiquitous at hydrothermal vents. These environments are distinguished by high physico-chemical variability, yet we know little about how these symbioses respond to environmental fluctuations. We therefore examined how the γ-proteobacterial symbionts of the vent snail Ifremeria nautilei respond to changes in sulfur geochemistry. Via shipboard high-pressure incubations, we subjected snails to 105 μM hydrogen sulfide (LS), 350 μM hydrogen sulfide (HS), 300 μM thiosulfate (TS) and seawater without any added inorganic electron donor (ND). While transcript levels of sulfur oxidation genes were largely consistent across treatments, HS and TS treatments stimulated genes for denitrification, nitrogen assimilation, and CO2 fixation, coincident with previously reported enhanced rates of inorganic carbon incorporation and sulfur oxidation in these treatments. Transcripts for genes mediating oxidative damage were enriched in the ND and LS treatments, potentially due to a reduction in O2 scavenging when electron donors were scarce. Oxidative TCA cycle gene transcripts were also more abundant in ND and LS treatments, suggesting that I. nautilei symbionts may be mixotrophic when inorganic electron donors are limiting. These data reveal the extent to which I. nautilei symbionts respond to changes in sulfur concentration and species, and, interpreted alongside coupled biochemical metabolic rates, identify gene targets whose expression patterns may be predictive of holobiont physiology in environmental samples.

Stable isotope signatures and nutritional sources of some dominant species from the PACManus hydrothermal area and the Desmos caldera

“…On the basis of previous research showing symbiotic relationships of bacteria in gastropods, I . nautilei derived its nutrition from intracellular gill symbionts that can oxidize both sulfide and thiosulfate to fuel autotrophy [40, 76–78]. Methanotrophic bacteria may also be present, but in low abundance.…”

The Bacterial Symbionts of Closely Related Hydrothermal Vent Snails With Distinct Geochemical Habitats Show Broad Similarity in Chemoautotrophic Gene Content

“…The I. nautilei individual used for sequencing was part of a high-pressure physiological experiment (see Beinart et al, 2015). A the conclusion of the experiment, symbiont-containing gill tissue was dissected, homogenized in Trizol TM (Thermo Fisher Scientific, Inc.) preservative, and stored at −80°C until DNA extraction as described in Seston et al (2016).…”

“…Each Alviniconcha individual was dominated by only one of the three phylotypes of bacterial symbiont, as previously assessed via symbiont-specific quantitative PCR assays (see Beinart et al, 2012). The I. nautilei individual (Table 1) had been previously shown, via 16S rRNA gene amplicon sequencing, to be dominated by one major symbiont phylotype from the order Chromatiales (Ifr1), with a very small sub-population of a second phylotype from the family Methylococcaceae in some individuals (Ifr2) (Seston et al, 2016). Symbiont 16S rRNA gene sequence similarity is >98% among host individuals sharing the same symbiont phylotype (Beinart et al, 2012, 2015; Seston et al, 2016).…”

“…Since they represent different bacterial lineages and do not show a pattern of co-divergence with host species (Suzuki et al, 2006a; Beinart et al, 2012), the symbionts are thought to be acquired horizontally from the environment. However, there is strong specificity between each snail species and its symbiont phylotypes(s): surveys of hundreds of individuals across a range of habitats have demonstrated that each snail species associates with only one or two of the symbiont phylotypes, with individual snails usually dominated by just one symbiont phylotype at a time (Table 1; Beinart et al, 2012; Seston et al, 2016).…”

“…Physiological experiments have directly demonstrated that some of these species can oxidize hydrogen sulfide and thiosulfate to support high rates of carbon fixation (Henry et al, 2008; Beinart et al, 2015). In addition, studies of gene transcription in situ and in laboratory experiments have demonstrated differences in expression of genes for sulfur oxidation, hydrogen oxidation, and both assimilatory and dissimilatory nitrate reduction (Sanders et al, 2013; Seston et al, 2016). These studies provide an understanding of metabolic pathway use and rates under conditions at the time of sampling and treatment, but do not allow for a comparison of the full metabolic and physiological potential of each symbiont.…”