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Hologenome analysis reveals dual symbiosis in the deep-sea hydrothermal vent snail Gigantopelta aegis.

ABSTRACT: Animals endemic to deep-sea hydrothermal vents often form obligatory symbioses with bacteria, maintained by intricate host-symbiont interactions. Most genomic studies on holobionts have not investigated both sides to similar depths. Here, we report dual symbiosis in the peltospirid snail Gigantopelta aegis with two gammaproteobacterial endosymbionts: a sulfur oxidiser and a methane oxidiser. We assemble high-quality genomes for all three parties, including a chromosome-level host genome. Hologenomic analyses reveal mutualism with nutritional complementarity and metabolic co-dependency, highly versatile in transporting and using chemical energy. Gigantopelta aegis likely remodels its immune system to facilitate dual symbiosis. Comparisons with Chrysomallon squamiferum, a confamilial snail with a single sulfur-oxidising gammaproteobacterial endosymbiont, show that their sulfur-oxidising endosymbionts are phylogenetically distant. This is consistent with previous findings that they evolved endosymbiosis convergently. Notably, the two sulfur-oxidisers share the same capabilities in biosynthesising nutrients lacking in the host genomes, potentially a key criterion in symbiont selection.

SUBMITTER: Lan Y

PROVIDER: S-EPMC7895826 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundMarine animals often exhibit complex symbiotic relationship with gut microbes to attain better use of the available resources. Many animals endemic to deep-sea chemosynthetic ecosystems host chemoautotrophic bacteria endocellularly, and they are thought to rely entirely on these symbionts for energy and nutrition. Numerous investigations have been conducted on the interdependence between these animal hosts and their chemoautotrophic symbionts. The provannid snail Alviniconcha marisindica from the Indian Ocean hydrothermal vent fields hosts a Campylobacterial endosymbiont in its gill. Unlike many other chemosymbiotic animals, the gut of A. marisindica is reduced but remains functional; yet the contribution of gut microbiomes and their interactions with the host remain poorly characterised.ResultsMetagenomic and metatranscriptomic analyses showed that the gut microbiome of A. marisindica plays key nutritional and metabolic roles. The composition and relative abundance of gut microbiota of A. marisindica were different from those of snails that do not depend on endosymbiosis. The relative abundance of microbial taxa was similar amongst three individuals of A. marisindica with significant inter-taxa correlations. These correlations suggest the potential for interactions between taxa that may influence community assembly and stability. Functional profiles of the gut microbiome revealed thousands of additional genes that assist in the use of vent-supplied inorganic compounds (autotrophic energy source), digest host-ingested organics (carbon source), and recycle the metabolic waste of the host. In addition, members of five taxonomic classes have the potential to form slime capsules to protect themselves from the host immune system, thereby contributing to homeostasis. Gut microbial ecology and its interplay with the host thus contribute to the nutritional and metabolic demands of A. marisindica.ConclusionsThe findings advance the understanding of how deep-sea chemosymbiotic animals use available resources through contributions from gut microbiota. Gut microbiota may be critical in the survival of invertebrate hosts with autotrophic endosymbionts in extreme environments.

Project description:Since deep-sea hydrothermal vent fluids are enriched with toxic metals, it was hypothesized that (i) the biota in the vicinity of a vent is adapted to life in the presence of toxic metals and (ii) metal toxicity is modulated by the steep physical-chemical gradients that occur when anoxic, hot fluids are mixed with cold oxygenated seawater. We collected bacterial biomass at different distances from a diffuse flow vent at 9 degrees N on the East Pacific Rise and tested these hypotheses by examining the effect of mercuric mercury [Hg(II)] on vent bacteria. Four of six moderate thermophiles, most of which were vent isolates belonging to the genus Alcanivorax, and six of eight mesophiles from the vent plume were resistant to >10 microM Hg(II) and reduced it to elemental mercury [Hg(0)]. However, four psychrophiles that were isolated from a nearby inactive sulfide structure were Hg(II) sensitive. A neighbor-joining tree constructed from the deduced amino acids of a PCR-amplified fragment of merA, the gene encoding the mercuric reductase (MR), showed that sequences obtained from the vent moderate thermophiles formed a unique cluster (bootstrap value, 100) in the MR phylogenetic tree, which expanded the known diversity of this locus. The temperature optimum for Hg(II) reduction by resting cells and MR activity in crude cell extracts of a vent moderate thermophile corresponded to its optimal growth temperature, 45 degrees C. However, the optimal temperature for activity of the MR encoded by transposon Tn501 was found to be 55 to 65 degrees C, suggesting that, in spite of its original isolation from a mesophile, this MR is a thermophilic enzyme that may represent a relic of early evolution in high-temperature environments. Results showing that there is enrichment of Hg(II) resistance among vent bacteria suggest that these bacteria have an ecological role in mercury detoxification in the vent environment and, together with the thermophilicity of MR, point to geothermal environments as a likely niche for the evolution of bacterial mercury resistance.

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Hologenome analysis reveals dual symbiosis in the deep-sea hydrothermal vent snail Gigantopelta aegis.

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