Dataset Information

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 ?-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.

SUBMITTER: Beinart RA

PROVIDER: S-EPMC6702916 | biostudies-literature | 2019

REPOSITORIES: biostudies-literature

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

Beinart Roxanne A RA Luo Chengwei C Konstantinidis Konstantinos T KT Stewart Frank J FJ Girguis Peter R PR

Frontiers in microbiology 20190814

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 t ...[more]

PMID: 31474946

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Project description:BACKGROUND: The deep-sea hydrothermal vent mussel Bathymodiolus azoricus harbors thiotrophic and methanotrophic symbiotic bacteria in its gills. While the symbiotic relationship between this hydrothermal mussel and these chemoautotrophic bacteria has been described, the molecular processes involved in the cross-talking between symbionts and host, in the maintenance of the symbiois, in the influence of environmental parameters on gene expression, and in transcriptome variation across individuals remain poorly understood. In an attempt to understand how, and to what extent, this double symbiosis affects host gene expression, we used a transcriptomic approach to identify genes potentially regulated by symbiont characteristics, environmental conditions or both. This study was done on mussels from two contrasting populations. RESULTS: Subtractive libraries allowed the identification of about 1000 genes putatively regulated by symbiosis and/or environmental factors. Microarray analysis showed that 120 genes (3.5% of all genes) were differentially expressed between the Menez Gwen (MG) and Rainbow (Rb) vent fields. The total number of regulated genes in mussels harboring a high versus a low symbiont content did not differ significantly. With regard to the impact of symbiont content, only 1% of all genes were regulated by thiotrophic (SOX) and methanotrophic (MOX) bacteria content in MG mussels whereas 5.6% were regulated in mussels collected at Rb. MOX symbionts also impacted a higher proportion of genes than SOX in both vent fields. When host transcriptome expression was analyzed with respect to symbiont gene expression, it was related to symbiont quantity in each field. CONCLUSIONS: Our study has produced a preliminary description of a transcriptomic response in a hydrothermal vent mussel host of both thiotrophic and methanotrophic symbiotic bacteria. This model can help to identify genes involved in the maintenance of symbiosis or regulated by environmental parameters. Our results provide evidence of symbiont effect on transcriptome regulation, with differences related to type of symbiont, even though the relative percentage of genes involved remains limited. Differences observed between the vent site indicate that environment strongly influences transcriptome regulation and impacts both activity and relative abundance of each symbiont. Among all these genes, those participating in recognition, the immune system, oxidative stress, and energy metabolism constitute new promising targets for extended studies on symbiosis and the effect of environmental parameters on the symbiotic relationships in B. azoricus.

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.

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Dataset Information

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

Publications

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

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