Deep-sea corals near cold seeps associate with sulfur-oxidizing chemoautotrophs in the family Ca. Thioglobaceae

Microbiome (2025) 13:232 Vohsen et al. Microbiome https://doi.org/10.1186/s40168-025-02254-z Open Access RESEARCH Deep‑sea corals near cold seeps associate with sulfur‑oxidizing chemoautotrophs in the family Ca. Thioglobaceae Samuel A. Vohsen1, Harald R. Gruber‑Vodicka2,3, Eslam O. Osman1,4, Matthew A. Saxton5, Samantha B. Joye5, Nicole Dubilier2, Charles R. Fisher1 and Iliana B. Baums1,6,7,8* Abstract Background Corals are known for their symbiotic relationships, yet there is limited evidence of chemoautotrophic associations. This is despite some corals occurring near cold seeps where chemosymbiotic fauna abound includ‑ ing mussels that host sulfur-oxidizing chemoautotrophs from the SUP05 cluster (family Ca. Thioglobaceae). We investigated whether corals near cold seeps associate with related bacteria and report here that these associations are widespread. Results We screened corals, water, and sediment for Thioglobaceae using 16S metabarcoding and found ASVs asso‑ ciated with corals at high relative abundance (10 – 91%). These ASVs were specific to coral hosts, absent in water sam‑ ples, and rare or absent in sediment samples. Using metagenomics and transcriptomics, we assembled the genome of one phylotype associated with Paramuricea sp. B3 (ASV 4) which contained the genetic potential to oxidize sulfur and fix carbon, and confirmed that these pathways were transcriptionally active. Furthermore, its relative abundance was negatively correlated with the stable isotopic composition of its host coral’s tissue suggesting some contribution of chemoautotrophy to the coral holobiont. Conclusions We propose that some lineages of Thioglobaceae may facultatively supplement the diet of their host corals through chemoautotrophy at seeps or may provide essential amino acids or vitamins. This is the first docu‑ mented association between chemoautotrophic symbionts and corals at seeps and suggests that the footprint of chemosynthetic environments is wider than currently understood. Keywords SUP05, Thioglobaceae, Deep-sea, Cold seep, Deep-sea corals, Chemoautotrophy, Symbiosis, Sulfur oxidation, Carbon fixation *Correspondence: Iliana B. Baums 1 Biology Department, The Pennsylvania State University, University Park, PA 16802, USA 2 Symbiosis Department, Max Planck Institute for Marine Microbiology, Bremen, Germany 3 Zoological Institute, Christian-Albrecht University of Kiel, Kiel, Schleswig‑Holstein, Germany 4 Marine Science Program, Division of Biological and Environmental Science and Engineering, King Abdullah University of Science and Technology (KAUST), Thuwal, Saudi Arabia 5 Department of Marine Sciences, University of Georgia, Athens, GA 30602, USA 6 Helmholtz-Institute for Functional Marine Biodiversity at the University of Oldenburg (HIFMB), Im Technologiepark 5, Oldenburg 26129, Germany 7 Alfred Wegener Institute, Helmholtz-Centre for Polar and Marine Research (AWI), Am Handelshafen 12, Bremerhaven 27570, Germany 8 Institute for Chemistry and Biology of the Marine Environment (ICBM), School of Mathematics and Science, Carl Von Ossietzky Universität Oldenburg, Ammerländer Heerstraße 114‑118, Oldenburg 26129, Germany © The Author(s) 2025. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. Vohsen et al. Microbiome (2025) 13:232 Background Deep-sea corals are important foundation species that support a diverse community of animals that rivals the diversity of shallow, tropical reefs and includes many commercially important fish species [1–5]. Deep-sea coral communities can be found along all continental margins from the Arctic to the Antarctic and on seamounts worldwide [6, 7]. In the deep Gulf of Mexico and in other locations, they overlap with cold seeps characterized by elevated concentrations of hydrogen sulfide and/or hydrocarbons [4, 8–13]. At cold seeps, some animals associate with chemotrophic symbionts which provide them with nutrition from the oxidation of these reduced chemical species [14–16]. Bathymodiolin mussels and vestimentiferan tubeworms obtain the bulk of their nutrition from these symbionts and form dense assemblages which in turn support highly productive animal communities [17–19]. The symbionts of mussels belong to the widespread SUP05 cluster which includes sulfur-oxidizing symbionts associated with various faunal hosts from reducing habitats such as cold seeps, hydrothermal vents, and organic falls [20–23]. Their hosts span many invertebrate phyla and include vesicomyid clams [24], scallops [25], snails [26], several groups of sponges [27, 28], terebellid polychaetes [20], and anemones [29]. The SUP05 cluster, along with the Arctic96-BD19 clade, comprise the family Ca. Thioglobaceae (Class Gammaproteobacteria) which also includes many free-living species that are abundant at oxygen minimum zones and hydrothermal vents where they dominate dark carbon fixation [23, 30–34]. Whether corals form associations with similar bacteria at chemosynthetic habitats has been a focus of research for several decades. Early work in the Gulf of Mexico explored the trophic dynamics of fauna at cold seeps using stable isotopic compositions and found that some anemones and stoloniferous corals had tissues with low δ13C and δ15N values suggesting they receive significant nutrition from chemotrophic sources [35]. Further work with the deepsea, scleractinian coral, Desmophyllum pertusum (formerly Lophelia pertusa [36]), found that they formed mounds near cold seeps where methane concentrations in the sediment were elevated. Thus, it was initially hypothesized that corals host chemotrophic symbionts or otherwise incorporate chemosynthetic primary productivity [37, 38]. Indeed, a relative of Thioglobaceae was detected in D. pertusum from Norway and the Gulf of Mexico using 16S metabarcoding [39, 40] and incubation experiments with D. pertusum detected carbon fixation [41]. However, these bacteria could not be located with FISH microscopy and showed no evidence that they were abundant in corals [42]. Other work analyzing available Page 2 of 15 particulate matter and bulk stable isotopic compositions of coral tissues demonstrated that D. pertusum does not receive detectable nutrit (...truncated)