# Microbial sulfur disproportionation at deep-sea hydrothermal vents: what do we know?

Alain Karine, Yvenou Stéven, Novák Lukáš, Heidi Aronson, Amend Jan, Wang Sasha, Jiang Lijing, Shao Zongze, Hemon Marie, Allioux Maxime, et al.

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Alain Karine, Yvenou Stéven, Novák Lukáš, Heidi Aronson, Amend Jan, et al.. Microbial sulfur disproportionation at deep-sea hydrothermal vents: what do we know?. The 8th International Workshop on Deep-Sea Microbiology, Nov 2024, Xiamen, China. hal-05133528

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Submitted on 1 Jul 2025

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Distributed under a Creative Commons Attribution 4.0 International License
Microbial sulfur disproportionation at deep-sea hydrothermal vents: what do we know?

Alain Karine¹, Yvenou Stéven¹, Novák Lukáš V.F.¹, Aronson Heidi², Amend Jan²†,
Wang Sasha³, Jiang Lijing³, Shao Zongze³, Hemon Marie¹, Allioux Maxime¹,
Erwan Roussel¹ et alii

¹CNRS, Univ Brest, Ifremer, EMR 6002 BIOMEX, BEEP, Sino-French IRP MicrobSea, Plouzané, France

²Department of Biological Sciences, University of Southern California, Los Angeles, USA

³Key Laboratory of Marine Genetic Resources, Third Institute of Oceanography, Ministry of Natural Resources of China, Sino-French IRP MicrobSea, Xiamen, China

Although the anaerobic microbial sulfur disproportionation was discovered in the early 1980s, little is known about its importance in most natural environments. To date, its metabolic pathways have not been fully deciphered. In marine hydrothermal vents, where sulfur species in intermediate oxidation states are abundant, this metabolism might play a central role in microbial energy production. From calculations of the Gibbs energy (ΔGr) of sulfur disproportionation, performed using internally consistent thermodynamic properties and geochemical data from four different hydrothermal systems, we showed that Sº-disproportionation is sufficiently exergonic to allow growth in most niches of the hydrothermal ecosystems, regardless of the geological and geochemical context, and depth. In recent years, bacteria capable of disproportionating sulfur compounds have been isolated from hydrothermal vent systems, sometimes from phyla where this catabolic capacity was not previously documented, bringing the number of hydrothermal strains with this metabolic capacity to 24. Genomic analyses suggest that there are at least two different pathways for sulfur disproportionation in these taxa, and functional analyses are underway to confirm or refute this. Under certain conditions, sulfide mineral formation is observed in culture. We characterized the minerals formed by using X-ray diffraction, Raman spectroscopy and SEM-EDX, in parallel with monitoring growth and metabolic products, and showed that the rate of sulfide mineral formation is much faster in the presence of sulfur-disproportionating bacteria of hydrothermal vent origin than under abiotic conditions.

Genomic markers of microbial sulfur disproportionation potentially involved in
reaction steps not yet fully deciphered have been proposed on the basis of
comparative genomic analyses. We extended this work to the search for taxon-
-optimized HMM profiles, by studying the genomes of 102 strains capable and incapable of disproportionating sulfur compounds. A relationship was established between some of these gene clusters and the ability to disproportionate sulfur compounds in the phylum *Desulfobacterota*. Orthologous groups of these gene clusters were also found in the closely related lineages *Nitrospirota* and *Acidobacteriota*. If this combination of proteins is indeed responsible for microbial sulfur disproportionation, this metabolism could have evolved in a common ancestor of these three phyla, who lived ~3.5 Ga ago, in line with some previous estimates based on isotope signatures.

References:

* Wang, S., Jiang, L., Xie, S., Alain, K., Wang, Z., Wang, J., Liu, D. & Shao, Z. (2023). Disproportionation of inorganic sulfur compounds by mesophilic chemolithoautotrophic *Campylobacterota*. *mSystems*. 8(1), e0095422. https://doi.org/10.1128/msystems.00954-22

* Allioux, M., Yvenou, S., Godfroy, A., Shao, Z., Jebbar, M. & Alain, K. (2022). Genome analysis of a new sulphur disproportionating species *Thermosulfurimonas* strain F29 and comparative genomics of sulfur-disproportionating bacteria from marine hydrothermal vents. *Microbial Genomics*. 8, 000865. https://doi.org/10.1099/mgen.0.000865

* Alain, K., Aronson, H.D., Allioux, M., Yvenou, S. & Amend, A. (2022). Sulfur disproportionation is exergonic in the vicinity of marine hydrothermal vents. *Environmental Microbiology*. 24(5), 2210-2219. https://doi.org/10.1111/1462-2920.15975.

* Yvenou, S., Allioux, M., Slobodkin, A., Slobodkina, G., Jebbar, M. & Alain, K. (2022). Genetic potential of *Dissulfurimicrobium hydrothermale*, an obligate sulfur-disproportionating thermophilic microorganism. *Microorganisms*. 10, 60. https://doi.org/10.3390/microorganisms10010060.

* Allioux, M., Yvenou, S., Slobodkina, G., Slobodkin, A., Shao, Z., Jebbar, M., & Alain, K. (2020). Genomic characterization and environmental distribution of a thermophilic anaerobe *Dissulfurirhabdus thermomarina* SH388T involved in disproportionation of sulfur compounds in shallow sea hydrothermal vents. *Microorganisms*, 8(1132), 1-14. https://doi.org/10.3390/microorganisms8081132

Bio information:

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Microbiologist.

Contact: Karine.Alain@univ-brest.fr

Director of the EMR 6002 BIOMEX (Biology, Interactions and adaptations of Organisms in Extreme environments)- CNRS, UBO, Ifremer- Plouzané, FRANCE. Website: https://www.umr-beep.fr/EMR-BIOMEX

French director of the Sino-French IRP 1211 MicrobSea (Plouzané, FRANCE; Xiamen, CHINA)

https://www.univ-brest.fr/fr/membre/karine-alain

https://scholar.google.com/citations?user=PMHq01IAAAAJ&hl=fr