Xue-Gong Li

Deep-sea hydrothermal vents emit geothermal light, yet its ecological role in shaping microbial adaptation remains largely unexplored. To investigate this, we designed a custom cultivation system that simultaneously applies high hydrostatic pressure (HHP) and light and used it to isolate 12 bacterial strains from active chimney fragments collected at the Kairei hydrothermal field. All 12 isolates exhibited enhanced growth under light exposure. Among them, strain SY138, identified as a novel Microbacterium species, was selected for mechanistic investigation. Our results demonstrate that light exposure directly induces carotenoid biosynthesis in SY138, which in turn reduces intracellular reactive oxygen species (ROS) levels. Inhibition of carotenoid synthesis using fosmidomycin abolished both the ROS-lowering effect and the light-dependent growth promotion, confirming that carotenoids are essential for this physiological response. Notably, while HHP severely inhibited growth by elevating intracellular ROS, light-induced carotenogenesis effectively counteracted this oxidative stress and alleviated HHP-induced growth inhibition. Collectively, these findings uncover a previously unrecognized adaptive strategy, wherein deep-sea hydrothermal vent bacteria exploit geothermal light as an environmental signal to activate carotenoid-based antioxidant defenses, thereby enhancing their survival under HHP conditions. This study highlights a previously underappreciated role of light in microbial stress tolerance in extreme deep-sea ecosystems. IMPORTANCE: Deep-sea hydrothermal vents harbor thriving ecosystems under extreme pressure and perpetual darkness, yet they have long been considered to be driven solely by chemosynthesis. The discovery of geothermal light has raised fundamental questions regarding its ecological role. Using a specialized cultivation system that simulates in situ high pressure and illumination, we isolated multiple light-responsive bacterial strains from a deep-sea vent, substantially expanding the known diversity of such microorganisms. Using Microbacterium sp. SY138 as a model, we uncovered a previously unrecognized adaptive strategy: these bacteria exploit light not as an energy source but as an environmental cue to preemptively activate carotenoid-based antioxidant defenses. This light-induced mechanism counteracts oxidative stress imposed by high pressure, a ubiquitous deep-sea stressor. Our findings reveal an unexpected interplay between light and pressure in the deep-sea environment, suggesting that light sensing could represent a more widespread and ecologically significant adaptive trait than previously recognized.

Despite its extreme conditions, the hadal environment harbors abundant but largely underexplored microbial resources. In this study, samples from the Kuril-Kamchatka Trench (KKT) were enriched at low temperature using R2A and 2216E media. Carotenoid-producing microorganisms (CPMs) were isolated from approximately one-third of the samples, yielding a total of 124 isolated strains spanning 4 phyla and 11 genera. Planococcus, Kocuria, Paracoccus, and Exiguobacterium collectively accounted for 75.8% of the isolates. The choice of culture medium significantly influenced CPM diversity at the family and genus levels, though not at the phylum or class level. Water depth, sample type, and sediment layer also significantly affected CPM community structure. Carotenoid spectral profiles correlated with phylogenetic lineage, and closer phylogenetic relationships corresponded to greater similarity in carotenoid biosynthesis gene clusters. Antioxidant assays (FRAP, ABTS, DPPH) demonstrated strong total antioxidant and radical scavenging capacities in carotenoid extracts from Citricoccus, Kocuria, Arthrobacter, and Olleya. Scavenging activity toward ABTS or DPPH radicals varied significantly among genera, suggesting genus-specific antioxidant mechanisms. These findings highlight the hadal zone as a promising reservoir of diverse CPMs and a valuable source of novel carotenoids and antioxidant-producing strains with potential biotechnological applications.

HHP plays a critical role in these habitats. Around a hundred prokaryotes, isolated from various temperature regimes of the deep biosphere, have been found to be piezophilicmeaning they require HHP for optimal growth. Several major questions remain unanswered: What is the origin of piezophiles? What are the molecular mechanisms underlying their adaptation to pressure? The nine articles of this research topic expand current knowledge on cellular, molecular, and adaptive responses to HHP in piezosensitive and piezophilic prokaryotes.Cui et al., investigated how HHP disrupts cell division in model microorganisms. Through analysis of the hadal piezophile Shewanella benthica DB21MT-2, five critical residues in the N-terminal GTPase domain of FtsZ were identified as essential for high-pressure adaptation, underscoring the functional importance of this domain. These findings advance our understanding of microbial cell division under extreme conditions. Coffin et al., focus on the pressure-dependent heat shock response in E. coli strains using GFP promoter fusions and single-cell fluorescence microscopy. They quantified the transcriptional upregulation of rpoH, rpoE, dnaK, and groEL following pressure shock in both piezosensitive E. coli and the piezotolerant strain AN62. The results reveal distinct responses in the pressure-adapted strain, suggesting RpoE may act as a pressure sensor. These findings link pressure adaptation to RNA polymerase function and highlight stochasticity in stress responses. Tamby et al., investigate how bacterial and archaeal ether-bonded lipids affect E. coli membrane robustness under high temperature and HHP. Only bacterial ether lipids enhance robustness, especially under combined stress. The results emphasize that temperature and HHP together critically affect survival, advancing understanding of membrane adaptation and the "lipid divide". This suggests such abiotic factors may have influenced early marine evolution. Moalic et al., showed in the piezophilic hyperthermophilic archaeon Thermococcus barophilus that the redox regulator SurR and HHP co-regulate energy metabolism genes. Pressure modulates gene expression, while SurR activates hydrogenogenic genes regardless of sulfur availability. Unlike non-piezophilic species, T. barophilus uses a sulfur-independent SurR mechanism for deep-sea adaptation. Also, Jiao et al., show that HHP enhances both sulfur reduction and growth in Thermococcus aciditolerans SY113 independently of SurR, highlighting the essential role of sulfur reduction to pressure adaptation. These findings advance our understanding of extremophile biology and provide insights for biotechnological and astrobiological applications under high-pressure conditions. Qiu and Tang, examine how the deep-sea bacterium Shewanella eurypsychrophilus YLB-09 adapts metabolically to HHP. Through combined metabolomics and transcriptomics, they found that HHP markedly reshapes energy, amino acid, and glycerolipid metabolism. Key adaptations include a switch to TMAO respiration, altered amino acid profiles, and adjusted membrane fluidity and composition. These metabolic adjustments enable YLB-09 to thrive under extreme pressure, offering insights into microbial survival strategies and supporting the development of industrially useful enzymes from extremophiles. Li et al., studied the piezotolerant fungus Purpureocillium lilacinum FDZ8Y1 from the Mariana Trench. Strain FDZ8Y1 withstands pressures up to 110 MPa and shows antibacterial, antitumor, and nematicidal activity. Genomic and transcriptomic analyses reveal its metabolic versatility in carbon, nitrogen, and sulfur cycling, along with the activation of fatty acid metabolism, antioxidant defenses, and secondary metabolite biosynthesis under HHP. These findings reveal the significant potential of hadal fungi for producing novel bioactive compounds. Zhang et al., compared sediment microbial communities in the Diamantina and Kermadec trenches using high-throughput sequencing. They found that both trenches exhibit distancedecay patterns, stochastic community assembly processes, and complex interspecific interactions that likely maintain community stability. Functional redundancy was also observed across taxonomic groups. These findings highlight the important roles of stochastic processes and functional redundancy in hadal ecosystems, advancing our understanding of microbial community assembly in extreme environments. Del Moral et al., focus on Europa's potentially habitable sub-ice ocean, using Earth-based analogues to assess habitability. They employed Canada's Basque Lake No.2,-a cold, hypersaline, Mg-Na-SO₄-rich environment-as an analogue for Europa's ice-ocean interface. Lake microorganisms were cultured in Europa-like fluid under progressively higher pressures (0.2-30 MPa), leading to the isolation of Pseudodesulfovibrio sp. OU_01 at 30 MPa. These findings advance our understanding of potential habitability and biosignature formation on icy moons.In conclusion, the deep biosphere is marked by extreme pressure, temperature, and nutrient scarcity, hosting most of Earth's bacteria and archaea, revealing a hidden biosphere adapted to challenging conditions (Jebbar et al., 2020). Recent research has uncovered how microbes thrive under high hydrostatic pressure (HHP) (Ando et al., 2021;Peters et al., 2025). The studies presented in this research topic reveal that Piezophilic species, which require HHP for growth, have evolved distinctive molecular adaptations. Notably, specific residues in essential cell division proteins like FtsZ enhance pressure tolerance, while heat shock responses and transcriptional regulators (e.g., RpoE) help manage stress. Membrane composition also matters, with certain lipids improving robustness under combined HHP and high temperature. In deep-sea archaea, pressure and redox regulators co-control energy metabolism, particularly sulfur reduction, which is vital for survival in these...

Thermococcus species are ubiquitously distributed across both shallow and deep-sea hydrothermal vent ecosystems. Elemental sulfur (S°) reduction plays a pivotal role in their energy metabolism. While extensive characterization of the MBS and MBH pathways, along with their SurR-dependent regulatory network, has been established in shallow-water model strains, understanding of the high hydrostatic pressure (HHP) and sulfur-responsive regulation of these pathways in deep-sea Thermococcus lineages remains limited. In this study, we investigated the effects of HHP on both growth and S° reduction in the deep-sea SY113 strain, as well as its regulatory impact on mbs and mbh expression. Our results demonstrate that HHP enhances both S° reduction and growth in SY113 strain, independent of the general regulator SurR. Genetic disruption of mbsL significantly impaired H₂S production and growth under HHP conditions, establishing the essential role of S° reduction in HHP adaptation. Furthermore, disrupted mbhL1 gene confirmed that a single MBS complex is sufficient to maintain pressure-stimulated growth. The gene expression analysis revealed that the expression of mbsL gene is primarily promoted by S°, while the expression of mbhL1 gene is induced by HHP. Moreover, the expression of these genes exhibits correlation. Additionally, we found that the expression of mbsL gene, mbhL1 gene, and mbhL2 gene in SY113 strain is not only regulated by SurR, and HHP also plays a role in modulating the expression of these genes. Overall, the sulfur responsive regulation of gene expression in SY113 strain distinguishes from that in the shallow model strains, which implies an adaptive strategy for Thermococcus species used to dwell in the deep-sea hydrothermal vent.

Three psychrophilic bacteria, designated as strains SQ149^T, SQ345^T, and S1-1^T, were isolated from deep-sea sediment from the South China Sea. All three strains were the most closely related to Thalassotalea atypica RZG4-3-1^T based on the 16S rRNA gene sequence analysis (similarity ranged from 96.45 to 96.67 %). Phylogenetic analysis based on the 16S rRNA gene and core-genome sequences showed that three strains formed a cluster within the genus Thalassotalea. The average amino acid identity, average nucleotide identity, and digital DNA–DNA hybridization values among the three strains and closest Thalassotalea species were far below the cut-off value recommended for delineating species, indicating they each represented a novel species. All three strains were Gram-stain-negative, rod-shaped, and contained summed feature 3 (C_16 : 1 ω7c and/or C_16 : 1 ω6c) as the predominant fatty acid, Q-8 as the major respiratory quinone, and phosphatidylethanolamine and phosphatidylglycerol as predominant polar lipids. Based on the genomic, phylogenetic, and phenotypic characterizations, each strain is considered to represent a novel species within the genus Thalassotalea, for which the names Thalassotalea psychrophila sp. nov. (type strain SQ149^T=MCCC 1K04231^T=JCM 33807^T), Thalassotalea nanhaiensis sp. nov. (type strain SQ345^T=MCCC 1K04232^T=JCM 33808^T), and Thalassotalea fonticola sp. nov. (type strain S1-1^T=MCCC 1K06879^T=JCM 34824^T) are proposed.

A novel anaerobic heterotrophic bacterium, designated strain SWIR-1T, was isolated from a deep-sea hydrothermal vent field sample collected from the Southwest Indian Ridge at a depth of 2700 m. Phylogenetic analysis indicated that strain SWIR-1T belongs to the genus Tepidibacter , and the most closely related species are Tepidibacter mesophilus B1T (99.1 % 16S rRNA gene sequence similarity), Tepidibacter formicigenes DV1184T (94.6 %) and Tepidibacter thalassicus SC562T (93.9 %). Strain SWIR-1T shares 77.3–87.2 % average nucleotide identity and 21.5–35.7 % digital DNA–DNA hybridization values with the three type strains of Tepidibacter species. Cells of strain SWIR-1T were Gram-stain-positive, motile, short straight rods. Endospores were observed in stationary-phase cells when grown on Thermococcales rich medium. Strain SWIR-1T grew at 15–45 °C (optimum, 30°C), at pH 5.5–8.0 (optimum, pH 7.0) and with 1.0–6.0 % (w/v) NaCl (optimum, 2.0 %). Substrates utilized by strain SWIR-1T included complex proteinaceous, chitin, starch, lactose, maltose, fructose, galactose, glucose, rhamnose, arabinose, ribose, alanine, glycine and glycerol. The major fermentation products from glucose were acetate, lactate, H2 and CO2. Elemental sulphur, sulphate, thiosulphate, sulphite, fumarate, nitrate, nitrite and FeCl3 are not used as terminal electron acceptors. The main cellular fatty acids consisted of iso-C15 : 0 (28.4 %), C15 : 1 iso F (15.4 %) and C16 : 0 (9.8 %). The major polar lipids were phospholipids and glycolipids. No respiratory quinones were detected. Genomic comparison revealed a distinctive blended gene cluster comprising hyb-tat-hyp genes, which play a crucial role in the synthesis, maturation, activation and export of NiFe-hydrogenase. Based on the phylogenetic analysis, genomic, physiologic and chemotaxonomic characteristics, strain SWIR-1T is considered to represent a novel species within the genus Tepidibacter , for which the name Tepidibacter hydrothermalis sp. nov. is proposed. The type strain is strain SWIR-1T (=DSM 113848T=MCCC 1K07078T)

A novel bacterium, strain QS115T, was isolated from deep-sea sediment collected from the South China Sea at a depth of 1151 m. Phylogenetic analyses based on 16S rRNA gene sequences indicated that QS115T was most closely related to Parasedimentitalea marina W43T, with similarity of 98.21 %. Strain QS115T shared 82.39 % average nucleotide identity, 26.3 % digital DNA–DNA hybridization and 85.32 % average amino acid identity with P. marina W43T. Cells of strain QS115T were Gram-stain-negative, rod-shaped and grew optimally at 10 °C, pH 7.5 and 2 % (w/v) NaCl. The principal fatty acids were summed feature 8 (C18 : 1 ω7c/ω6c), the major respiratory quinone was ubiquinone-10 and predominant polar lipids were diphosphatidylglycerol, phosphatidylethanolamine, glycophospholipid, phosphatidylglycerol and phosphatidylcholine. Polyphasic analyses of physiological and phenotypic characteristics and genomic studies suggested that strain QS115T represents a novel species of the genus Parasedimentitalea , for which the name Parasedimentitalea psychrophila sp. nov. is proposed (type strain QS115T=MCCC 1K04395T=JCM 34219T).