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

Abstract

Symbiosis has evolved between a diversity of invertebrate taxa and chemosynthetic bacterial lineages. At the broadest level, these symbioses share primary function: the bacterial symbionts use the energy harnessed from the oxidation of reduced chemicals to power the fixation of inorganic carbon and/or other nutrients, providing the bulk of host nutrition. However, it is unclear to what extent the ecological niche of the host species is influenced by differences in symbiont traits, particularly those involved in chemoautotrophic function and interaction with the geochemical environment. Hydrothermal vents in the Lau Basin (Tonga) are home to four morphologically and physiologically similar snail species from the sister genera Alviniconcha and Ifremeria. Here, we assembled nearly complete genomes from their symbionts to determine whether differences in chemoautotrophic capacity exist among these symbionts that could explain the observed distribution of these snail species into distinct geochemical habitats. Phylogenomic analyses confirmed that the symbionts have evolved from four distinct lineages in the classes γ-proteobacteria or Campylobacteria. The genomes differed with respect to genes related to motility, adhesion, secretion, and amino acid uptake or excretion, though were quite similar in chemoautotrophic function, with all four containing genes for carbon fixation, sulfur and hydrogen oxidation, and oxygen and nitrate respiration. This indicates that differences in the presence or absence of symbiont chemoautotrophic functions does not likely explain the observed geochemical habitat partitioning. Rather, differences in gene expression and regulation, biochemical differences among these chemoautotrophic pathways, and/or differences in host physiology could all influence the observed patterns of habitat partitioning.

Keywords: Alviniconcha; Campylobacteria; Gammaproteobacteria; Ifremeria; chemosynthesis; gastropod; genomics; symbiosis.

FIGURE 1

Maximum-likelihood phylogenomic analysis of a 6,989 position concatenated protein alignment of 43 marker genes from the Alviniconcha γ-Lau symbiont, I. nautilei Ifr1 symbiont, and relatives using the LG + I + G + F model of protein evolution. Symbiont genomes from this study are highlighted in gray, and genomes derived from host-associated symbionts are shown in bold. Percent bootstrap support for each clade shown. The scale bar represents the mean number of nucleotide substitutions per site.

FIGURE 2

Maximum-likelihood phylogenomic analysis of a 6,989 position concatenated protein alignment of 43 marker genes from the Alviniconcha ε symbiont and its Sulfurimonas relatives using the LG + G + F model of protein evolution. The symbiont genome from this study is highlighted in gray. Percent bootstrap support for each clade shown. The scale bar represents the mean number of nucleotide substitutions per site.

FIGURE 3

Maximum-likelihood phylogenomic analysis of a 6,989 position concatenated protein alignment of 43 marker genes from Alviniconcha γ-1 and relatives using the LG + G + F model of protein evolution. The symbiont genome from this study is highlighted in gray, and genomes derived from host-associated symbionts are shown in bold. Percent bootstrap support for each clade shown. The scale bar represents the mean number of nucleotide substitutions per site.

FIGURE 4

Heatmap showing the number of genes annotated to each SEED category within each symbiont genome. Hierarchical clustering based on Euclidean distance with average linkage.

FIGURE 5

Heatmap showing the proportion of unique genes (i.e., those not present in any other genome) annotated to each SEED category from each symbiont genome. Hierarchical clustering based on Euclidean distance with average linkage.