Dual energy metabolism of the Campylobacterota endosymbiont in the chemosynthetic snail Alviniconcha marisindica

Abstract

Some deep-sea chemosynthetic invertebrates and their symbiotic bacteria can use molecular hydrogen (H 2 ) as their energy source. However, how much the chemosynthetic holobiont (endosymbiont-host association) physiologically depends on H 2 oxidation has not yet been determined. Here, we demonstrate that the Campylobacterota endosymbionts of the gastropod Alviniconcha marisindica in the Kairei and Edmond fields (kAlv and eAlv populations, respectively) of the Indian Ocean, utilize H 2 in response to their physical and environmental H 2 conditions, although the 16S rRNA gene sequence of both the endosymbionts shared 99.6% identity. A thermodynamic calculation using in situ H 2 and hydrogen sulfide (H 2 S) concentrations indicated that chemosynthetic symbiosis could be supported by metabolic energy via H 2 oxidation, particularly for the kAlv holobiont. Metabolic activity measurements showed that both the living individuals and the gill tissues consumed H 2 and H 2 S at similar levels. Moreover, a combination of fluorescence in situ hybridization, quantitative transcript analyses, and enzymatic activity measurements showed that the kAlv endosymbiont expressed the genes and enzymes for both H 2 -and sulfur-oxidations. These results suggest that both H 2 and H 2 S could serve as the primary energy sources for the kAlv holobiont. The eAlv holobiont had the ability to utilize H 2 , but the gene expression and enzyme activity for hydrogenases were much lower than for sulfur-oxidation enzymes. These results suggest that the energy acquisitions of A. marisindica holobionts are dependent on H 2 -and sulfur-oxidation in the H 2 -enriched Kairei field and that the mechanism of dual metabolism is controlled by the in situ H 2 concentration. * Junichi Miyazaki miyazaki11@jamstec.go.jp 1 Super-cutting-edge Grand and Advanced Research (SUGAR) Program,

Physiological dynamics of chemosynthetic symbionts in hydrothermal vent snails

“…We observed no change in expression for hydrogen oxidation genes in the A. boucheti symbiont under the experimental H 2 conditions. These findings differ from a recent study by Miyazaki et al [ 31 ], which showed that the campylobacterial symbiont of A. marisindica strictly regulates the expression of hydrogenases depending on the environmental hydrogen concentrations. Compared to Miyazaki et al [ 31 ], who provided 100 µM H 2 in their experiments, we only provided 25 µM H 2 .…”

Classical and computed tomographic anatomical analyses in a not-so-cryptic Alviniconcha species complex from hydrothermal vents in the SW Pacific

“…The authors argue that these host distribution patterns likely reflect distinct metabolic capabilities or physiological needs of their symbionts. A recently confirmed capacity for H 2 oxidation in Alviniconcha campylobacterotal symbionts [25], first suggested by [23], appears to support this hypothesis. This would enable the use of discrete abundant energy resources in a highly limiting spatial environment.…”

“…Most Alviniconcha species, including A. kojimai and A. strummeri, host Gammaproteobacteria-dominated symbioses that are closely related to known chemoautotrophic [9-11, 14, 15], sulphur-oxidising bacteria that predominantly use the Calvin-Benson-Bassham cycle for carbon fixation [20]. In the remaining two species, A. boucheti and A. marisindica, symbioses are dominated by sulphur-oxidising bacteria from a separate phylum, the Campylobacterota [9,10] formerly known as the Epsilonproteobacteria [21,22] that also utilise H 2 -oxidation [23][24][25] under high-H 2 concentrations (several mM, [25]) and likely fix carbon through the Reverse Tricarboxylic Acid cycle [20]. Thus, one hypothesis that might explain the small-scale habitat partitioning observed in SW Pacific Alviniconcha species, is that optimal conditions for chemosynthesis differ for each host species, as a function of the unique metabolic capabilities or physiological requirements of their symbiont assemblages.…”

“…Interestingly, phylogenetic analyses of recently published symbiont genomes from SW pacific Alviniconcha species indicate that chemoautotrophic function in symbiotic bacteria is similar irrespective of host species [24], suggesting differences relating to gene expression (e.g. [25]) and regulation and/or differences in host physiology may mediate habitat partitioning.…”

Metatranscriptomics by In Situ RNA Stabilization Directly and Comprehensively Revealed Episymbiotic Microbial Communities of Deep-Sea Squat Lobsters

“…During deep-sea sampling and onboard recovery, which usually takes more than an hour, the composition and activity of microbial communities can change considerably, while RNAs can be degraded (25), which means that true RNA profiles in the deep sea can be missed if experimental procedures are conducted after retrieval (26,27). To solve these problems, in situ RNA stabilization (i.e., stabilization before retrieval by remote control) instead of onboard RNA stabilization (i.e., stabilization after retrieval) is desirable (16,(28)(29)(30)(31)(32); however, these two approaches have been neither systematically compared nor applied to metatranscriptomic analyses of deep-sea symbiotic microbial communities.…”