Sulfur-rich deposits associated with the deep submarine volcano Fani Maoré support broad microbial sulfur cycling communities.

Abstract

Background: In 2018, the island of Mayotte located in the western Indian ocean, has experienced a seismo-volcanic crisis linked to the birth of an impressive intraplate submarine volcano at the east of the island. This volcano, named Fani Maoré, which has not yet been the subject of microbiological studies, triggered the largest submarine eruptive event ever recorded. Close to the volcano's summit is a singular meter-size structure containing abundant native sulfur mineralizations. While a wide variety of ecosystems, with more or less well documented microbial communities, are found in active volcanoes on the ocean floor, knowledge on microbial communities hosted in habitats such as sulfur-rich intraplate volcanoes, that are not located on hotspots, remains limited. Genome-resolved metagenomics, culture-based functional approaches, geochemical and mineralogical analyses were combined to characterize the geological and physico-chemical constraints of the environment surrounding the yellow deposit part of this hotspot volcano and the composition and functions of its microbial community.

Results: Geological and geochemical analyses indicated that this volcanic habitat had high concentrations in various sulfur species, including native sulfur, hydrogen sulfide and sulfate. Twenty-three Metagenome Assembled Genomes (MAGs) belonging to 8 different bacterial phyla, mainly Pseudomonadota, Bacteroidota and Campylobacterota, were reconstructed from the sulfur-rich deposit and analyzed. The vast majority of MAGs encoded genes for complete sulfur cycling metabolic pathways, in particular sulfur oxidation. Estimation of the cultivable microbial fraction revealed a diversity of microorganisms, with high growth rates for sulfur reduction, sulfate reduction with dihydrogen, and sulfur oxidation. Sulfur compound (S⁰, SO₃^2- and S₂O₃^2-) disproportionation was also observed in cultures. The versatile genus Sulfurimonas was prevalent in culture at 6 and 20 °C, in the presence of different sulfur redox couples.

Conclusions: Microbial communities, including taxa commonly found in ridge hydrothermal systems, were composed of autotrophic, heterotrophic or mixotrophic taxa using a large range of electron donors and acceptors to fuel their catabolism, particularly sulfur compounds in all common oxidation states. They had the genetic potential and physiological capacity to carry out all the metabolic reactions of the microbial sulfur cycle using the abiotic sulfur compounds present in their habitat. Representatives of the Sulfurimonas genus were among the main chemoautotrophs, since they predominated in eleven different temperature-redox pair culture combinations. Based on the observations, a conceptual model was proposed to describe the interactions in this sulfur-rich deposit that may occur between the microorganisms, the physico-chemical conditions and the sulfur compounds supplied by the environment. Video Abstract.