Decoding microbial diversity, biogeochemical functions, and interaction potentials in red sea hydrothermal vents

Abstract

Background: Hydrothermal vents along mid-ocean ridges host diverse microbial communities and are crucial to global elemental cycling. The Red Sea, known for its unique environmental conditions-including low nutrient levels, high year-round temperatures, bottom-water temperatures of 21 °C, and elevated salinity-hosts recently discovered active low-temperature hydrothermal vent fields at the axial Hatiba Mons volcano. These vents, characterized by large iron oxide mounds and abundant microbial mats, offer an extreme environment for studying the diversity and functions of prokaryotes involved in elemental cycling in this system. In this study, we used 16S rRNA sequencing and shotgun metagenomics to examine the microbial diversity and metabolic capabilities of precipitates and microbial mats from five vent sites.

Results: We recovered 314 non-redundant metagenome-assembled genomes (MAGs), including 250 bacterial and 64 archaeal MAGs, representing 34 bacterial and 11 archaeal phyla. Functional annotations revealed diverse nutrient and metal cycling potentials, with notable enrichment in iron redox genes. Key players include Bathyarchaeia and Chloroflexi in the precipitates (contributing to carbon, nitrogen, sulfur, and metal cycling potentials) and Pseudomonadota members in the microbial mats and upper precipitates (involved in iron and sulfur metabolism and carbon fixation through the CBB cycle). Carbon fixation in precipitate potentials primarily occurs through the Wood-Ljungdahl pathway. Sulfur and nitrogen cycling genes are distributed across various genomes, indicating collaborative cycling.

Conclusion: Our genome-resolved analysis positions the Hatiba Mons vents as an iron-rich system that provides new insights into oligotrophic hydrothermal environments, with potential relevance for understanding novel metabolic pathways, extremophilic adaptations, and their roles in element cycling and biotechnological applications.

Keywords: Biogeochemical cycling; Carbon fixation; Extremophiles; Hatiba mons; Hydrothermal vents; Iron metabolism; Metagenome-assembled genomes; Microbial diversity; Red sea; Shotgun metagenomics.

Fig. 1

Regional map and sampling locations of the Hatiba Mons hydrothermal vent fields. (A) Regional map showing the location of the Hatiba Mons in the Red Sea, marked by a white square. (B) Close-up view of the Hatiba Mons summit, highlighting sampling points across the major large active hydrothermal vent fields—Farwah Safraa ridges (FS), Kabir Field (KF), Majarrah Mounds (MM), Beacon Field (BF), and Baja’ah Mounds (BM). Sampling methods and sample types are indicated by colored circles: yellow circles represent ROV sampling for microbial mats, while blue and green circles indicate gravity core and box core samples for precipitates, respectively. Confirmed low-temperature vent fields are shown in dark orange, and inferred low-temperature vent fields in light orange. Map after [8]. Inset: Hatiba Mons dome volcano; the white square indicates the area in the main Fig. of B

Fig. 2

Microbial community structure and diversity in Hatiba hydrothermal vent precipitates. (A) Relative abundance of dominant bacterial and archaeal classes in surface and 1 m depth precipitates. (B) PCoA of prokaryotic beta diversity (Bray–Curtis dissimilarity) by hydrothermal activity. Each data point represents a replicate precipitate sample collected from gravity cores. Red and blue ellipses indicate 95% confidence intervals around group centroids, shown as visual aids to illustrate clustering by hydrothermal activity. (C) Box plots of Shannon diversity for surface and 1 m depth precipitates

Fig. 3

Phylogenomic trees of bacterial and archaeal MAGs from Hatiba vent samples. (A) Maximum-likelihood phylogenomic tree of bacterial MAGs from Hatiba vent precipitates and microbial mats, constructed using 400 universal marker genes in PhyloPhlAn. Major taxonomic groups are highlighted, and MAG quality is shown in the outer ring. The tree is midpoint-rooted in iTOL. (B) Maximum-likelihood phylogenomic tree of archaeal MAGs from the same sites, constructed and annotated as in (A)

Fig. 4

Overview of predominant metabolic functions in Hatiba vent microbial mats and precipitates. Normalized abundances of predicted pathways from unbinned contigs are shown across hydrothermal activity levels and sample types. A continuous color gradient indicates abundance, with blue denoting lower and red higher values

Fig. 5

Major bacterial taxa and their biogeochemical functions in Hatiba vent metagenomes. Overview of major bacterial taxa (> 80% completion) and their key biogeochemical processes by phylum, including orders and their genomic potentials in carbon (C), nitrogen (N), iron (Fe), sulfur (S), arsenate (As), and manganese (Mn) cycling. Pseudomonadota taxa are shown at the class level. Colored circles indicate the presence of processes, while empty circles indicate their absence. For detailed gene-level presence and phylogenetic context of these MAGs, see Supplementary Fig. S7

Fig. 6

Functional potential of archaeal genomes from Hatiba Mons metagenomes. Functional potential of medium- and high-quality archaeal genomes assembled from Hatiba Mons metagenomes, highlighting their roles in the carbon, nitrogen, hydrogen (H), iron, sulfur, and arsenic (As) cycles. Colored squares indicate the presence of each function; empty squares indicate their absence