Evidence for the role of endosymbionts in regional-scale habitat partitioning by hydrothermal vent symbioses

Abstract

Deep-sea hydrothermal vents are populated by dense communities of animals that form symbiotic associations with chemolithoautotrophic bacteria. To date, our understanding of which factors govern the distribution of host/symbiont associations (or holobionts) in nature is limited, although host physiology often is invoked. In general, the role that symbionts play in habitat utilization by vent holobionts has not been thoroughly addressed. Here we present evidence for symbiont-influenced, regional-scale niche partitioning among symbiotic gastropods (genus Alviniconcha) in the Lau Basin. We extensively surveyed Alviniconcha holobionts from four vent fields using quantitative molecular approaches, coupled to characterization of high-temperature and diffuse vent-fluid composition using gastight samplers and in situ electrochemical analyses, respectively. Phylogenetic analyses exposed cryptic host and symbiont diversity, revealing three distinct host types and three different symbiont phylotypes (one ε-proteobacteria and two γ-proteobacteria) that formed specific associations with one another. Strikingly, we observed that holobionts with ε-proteobacterial symbionts were dominant at the northern fields, whereas holobionts with γ-proteobacterial symbionts were dominant in the southern fields. This pattern of distribution corresponds to differences in the vent geochemistry that result from deep subsurface geological and geothermal processes. We posit that the symbionts, likely through differences in chemolithoautotrophic metabolism, influence niche utilization among these holobionts. The data presented here represent evidence linking symbiont type to habitat partitioning among the chemosynthetic symbioses at hydrothermal vents and illustrate the coupling between subsurface geothermal processes and niche availability.

Fig. 1.

(A) Map of ELSC depicting the four vent fields sampled herein. (Inset) Location of ELSC in the South Pacific. (B) A typical assemblage of Alviniconcha (Al) and other vent animals in the Lau Basin (Image courtesy of James Childress, University of California, Santa Barbara). (C) An individual Alviniconcha snail.

Fig. 2.

Bayesian inference phylogeny of the Alviniconcha host mitochondrial CO1 haplotypes from this and previous studies and sequences from the sister genus Ifremeria. Boxes show the three Alviniconcha host types reported here. The haplotype ID number is shown at the tip of each branch, and the gray bars represent the total number of individuals recovered for each haplotype. Accession numbers for haplotypes found in this study are given in Table S2. Posterior probabilities are indicated above the nodes if >0.7.

Fig. 3.

Bayesian inference phylogenies of 16S rRNA sequences showing the three Alviniconcha symbiont phylotypes found at the ELSC. All Alviniconcha symbionts, from this study and others, are shown in bold. Gray highlighting indicates the representative sequences from this study. Boxes show the Alviniconcha symbiont phylotypes defined here and in other studies. Posterior probabilities are indicated above the nodes if >0.7. (A) γ-proteobacterial phylogeny, with β-proteobacteria as the outgroup. (B) ε-proteobacterial phylogeny, with δ-proteobacteria as the outgroup.

Fig. 4.

Ternary plots of the symbiont composition of each Alviniconcha host type, with each point showing the symbiont composition of a single individual. The vertices of the triangle represent 100% of each symbiont phylotype, and the tick marks on the axes represent decreasing intervals of 10%. The symbiont phylotypes are indicated by γ-1 (γ-proteobacteria type 1), γ-Lau (γ-proteobacteria type Lau), and ε (ε-proteobacteria). Vent fields are indicated by ● (Kilo Moana), □ (Tow Cam), X (ABE), and ▽ (Tu’i Malila).

Fig. 5.

The distribution of Alviniconcha host types and dominant symbiont type across the ELSC, with each individual colored according to dominant symbiont phylotype (>67% of the total detected 16S rRNA genes) and shaped according to host type. The four vent fields are separated by solid lines, and distinct collections from within each vent field are divided by dashed lines, with the collection ID indicated (Table S1). Symbiont phylotypes are indicated as follows: green, γ-proteobacteria type 1 (γ-1); yellow, γ-proteobacteria type Lau (γ-Lau); blue, ε-proteobacteria (ε).The individuals that had relatively equal proportions of two of the symbiont phylotypes are shown as two colors. Host types are indicated by shapes: ●, host type 1 (HT-I); ■, host type II (HT-II); ▲, host type III (HT-III); ◆, host type undetermined.

Fig. 6.

Cyclic voltammetry measurements made on the cleared substratum after Alviniconcha collections, showing (A) temperature, (B) free sulfide concentration (sulfide), and (C) oxygen concentration at northern collections versus the southern collections. North (N) includes the vent fields Kilo Moana (KM) and Tow Cam (TC); South (S) includes ABE and Tu’i Malila (TM). Symbols with horizontal lines represent samples from diffuse vent flows; symbols without lines represent chimney wall habitats. Median values for each region are indicated by a dashed horizontal line.

Fig. 7.

The end-member fluid concentrations of (A) H₂, (B) H₂S, (C) CH₄, and (D) DIC at the four vent fields along the ELSC from which Alviniconcha were collected. Symbols indicate year of sampling: X, 2005; ●, 2009. DIC and H₂S data from 2005 were published previously by Mottl et al. (44).

Fig. P1.

The distribution of Alviniconcha snails along the regional-scale geochemical gradient at the ELSC corresponds to symbiont type. (A) A typical assemblage of Alviniconcha (Al) and other vent animals in the Lau Basin (image courtesy of J. Childress, University of California, Santa Barbara, CA). (B) An individual Alviniconcha snail. (C) Map of the ELSC, with four sampled vent fields shown across the ∼300-km range. The wedges graphically represent the relative decrease in the concentrations of H₂ and H₂S in hydrothermal vent fluids from north to south. (D) The distribution of Alviniconcha host types and dominant symbiont type across the ELSC. Snail host types (HT-I, HT-II, and HT-III) are indicated by the shape of each symbol. The dominant symbiont phylotypes [γ-proteobacteria type 1 (γ-1), γ-proteobacteria type Lau (γ-Lau), and ε-proteobacteria (ε)] within a host are indicated by the color of each symbol.