Rulong Liu

Members of the class Campylobacteria are microaerophilic bacteria widely distributed across diverse environments and are abundant in hydrothermal systems. However, cultivated representatives, particularly from shallow-water vents, remain limited. Here, we investigated the genomic diversity and environmental adaptation of the genus Sulfurospirillum. Phylogenomic analysis revealed a clear separation between terrestrial and marine clades, with relatively few cultured representatives in the marine lineage. Strain 1307, isolated from shallow-water hydrothermal vents, expands the genomic representation of this underexplored clade. Pan-genome analyses based on complete genomes revealed an open pan-genome, indicating ongoing diversification of genus Sulfurospirillum. Further comparison between hydrothermal vent (HTV) and non-HTV lineages identified distinct adaptive features. Vent-associated strains are enriched in genes involved in sulfur metabolism, carbon fixation, the glycine cleavage system (GCS), and the biosynthesis of key cofactors (spermidine, thiamine, lipoate, and heme), reflecting metabolic adaptation to hydrothermal environments. Beyond well-established processes such as sulfur metabolism and autotrophic carbon fixation, the widespread presence of the GCS in vent-associated lineages suggests its potential role as an auxiliary carbon fixation pathway under anaerobic conditions. Overall, this study expands the phylogenetic and genomic diversity of Sulfurospirillum and offers new insights into the mechanisms underlying environmental adaptation and niche differentiation in vent-associated Campylobacteria.

The discharge of pollutants into rivers has been increasing with the rapid industrial development and extensive agricultural use of pesticides and herbicides. Halogenated organic compounds (HOCs) represent a significant class of environmental pollutants. It has been found that microorganisms have the ability not only to degrade HOCs but also to synthesize them. Little is known about the halogenation and dehalogenation potential of microorganisms in river waters. In this study, we investigated the halogenation and dehalogenation potentials of microorganisms in the Yangtze River, which originates from the Tibetan Plateau, flows through southwestern, central and eastern China, and finally joins the East China Sea. A systematic metagenomic and bioinformatics analysis identified and quantified genes encoding four dehalogenases and two halogenases, providing fundamental data for the halogen cycle in the Yangtze River water body. The study showed that the microbial community in the Yangtze water body was mainly associated with dehalogenation potential, and the relative abundance of dehalogenase genes was higher than that of halogenase genes. Among the microorganisms with halogenation and dehalogenation potentials, Pseudomonadota and Actinomycetota dominated. Some microorganisms possessed both halogenation and dehalogenation functions, suggesting a potential adaptive strategy to environmental fluctuations. The presence of diverse and complete dehalogenation metabolic pathways highlights the microbial potential for bioremediation. These microorganisms not only contribute to the degradation of halogenated organic matter but also play crucial roles in carbon, nitrogen, and sulfur cycling. This study provides essential data for understanding microbial halogenation and dehalogenation potential in the Yangtze River, offering insights into the microbial-driven biogeochemical cycling mechanisms in its waters.

The hadal trenches, the deepest regions of the ocean, serve as the final resting place for marine particles and as "tunnels" for material exchange between the ocean and Earth's interior. Despite their extreme conditions, the trenches contain high content of organic carbon (OC) and active microbial carbon turnover, are hotspots for deep-sea OC degradation and unique microbial processes. However, little is known about the OC components and microbial metabolisms driving the OC degradation in the trenches. This study reveals unexpectedly high concentrations of halogenated organic compounds (HOCs) in the Mariana Trench sediments, with about 1 halogen per 58 carbon atoms in the OC pool. Systematic analysis of deep-sequenced metagenomes and metagenome-assembled-genomes from the global ocean shows significantly higher abundance of the genes for biodegradation of HOCs (dehalogenation) in trench microbes, with microorganisms capable of dehalogenation belonging to 16 phyla and 52 orders, 75% of which identified as HOCs degraders for the first time. Microcosms simulating trench conditions showed rapid degradation of typical HOCs and transcription of genes related with HOCs metabolisms, demonstrating the active HOCs degradation by the trench microorganisms. The findings suggest the HOCs metabolism as an important process in the OC remineralization of deep-sea trenches, advancing understanding of deep-sea carbon cycling and microbial survival strategies.

The hadal trenches, the deepest regions of the ocean, serve as the final sinks for marine particles and “tunnels” for material exchange between the ocean and Earth's interior. Despite their extreme conditions, the trench sediments contain high content of organic carbon and active microbial carbon turnover, are hotspots for deep-sea organic carbon degradation and unique microbial processes. However, little is known about the organic carbon components and microbial metabolisms driving their degradation in trench sediments. This study provides the first comprehensive quantification of total halogenated organic compounds (organohalides) in Mariana Trench sediments. The measured bulk organic halogen concentrations exceeded all previously reported individual compounds by orders of magnitude, with a mean stoichiometric ratio of 1:49 (halogen:carbon) in the sedimentary organic carbon pool. These findings suggest the trench sediments may represent a significant reservoir for organohalides. Metagenomic analysis of global ocean data shows significant enrichment of the genes for organohalides biodegradation (dehalogenation) in trench microbiomes than those in other marine environments. Putative dehalogenating microorganisms in trench sediments encompassed 16 phyla and 52 orders, capable of metabolizing 18 structurally diverse organohalide compounds, revealing an unexpectedly broad phylogenetic distribution of organohalides metabolism and versatile substrate specificity among trench microbial communities. High pressure microcosm experiments demonstrated rapid degradation of typical organohalide compounds and transcription of genes related to organohalides metabolisms, confirming an active organohalides degradation by trench microorganisms. These findings underscore the role of organohalides metabolism in organic carbon remineralization in hadal trenches, advancing our understanding of deep-sea carbon cycling and microbial survival.

Bacteria in the phylum Gemmatimonadota are globally distributed and abundant in microbial communities of various environments, playing an important role in driving biogeochemical cycling on Earth. Although high diversities in taxonomic composition and metabolic capabilities have been reported, little is known about the environmental preferences and associated functional features that facilitate adaptation among different Gemmatimonadota lineages. This study systematically analyzed the relationships between the environments, taxonomy, and functions of Gemmatimonadota lineages, by using a comparative genomics approach based on 1356 Gemmatimonadota genomes (213 high-quality and non-redundant genomes) available in a public database (NCBI). The taxonomic analysis showed that the 99.5% of the genomes belong to the class Gemmatimonadetes, and the rest of the genomes belong to the class Glassbacteria. Functional profiling revealed clear environmental preference among different lineages of Gemmatimonadota, and a marine group and two non-marine groups were identified and tested to be significantly different in functional composition. Further annotation and statistical comparison revealed a large number of functional genes (e.g., amiE, coxS, yfbK) that were significantly enriched in genomes from the marine group, supporting enhanced capabilities in energy acquisition, genetic information regulation (e.g., DNA repair), electrolyte homeostasis, and growth rate control. These genomic features are important for their survival in the marine environment, which is oligotrophic, variable, and with high salinity. The findings enhanced our understanding of the metabolic processes and environmental adaptation of Gemmatimonadota, and further advanced the understanding of the interactions of microorganisms and their habitats.

Enhancing the availability of representative isolates from hydrothermal vents (HTVs) is imperative for comprehending the microbial processes that propel the vent ecosystem. In recent years, Campylobacteria have emerged as the predominant and ubiquitous taxon across both shallow and deep-sea vent systems. Nevertheless, only a few isolates have been cultured, primarily originating from deep-sea HTVs. Presently, no cultivable isolates of Campylobacteria are accessible in shallow water vent systems (Sulfurospirillum , Campylobacteria) from shallow-water HTVs of Kueishan Island. Genomic and physiological analysis revealed that this novel Campylobacteria species grows on a variety of substrate and carbon/energy sources. The pan-genome and phenotypic comparisons with 12 previously isolated Sulfurospirillum species from different environments supported the identification of functional features in Sulfurospirillum genomes crucial for adaptation to vent environments, such as sulfur oxidation, carbon fixation, biofilm formation, and benzoate/toluene degradation, as well as diverse genes related with signal transportation. To conclude, the metabolic characteristics of this novel Campylobacteria augment our understanding of Campylobacteria spanning from deep-sea to shallow-water vent systems. IMPORTANCE: Campylobacteria emerge as the dominant and ubiquitous taxa within vent systems, playing important roles in the vent ecosystems. However, isolated representatives of Campylobacteria have been mainly from the deep-sea hydrothermal fields, leaving a significant knowledge gap regarding the functions, activities, and adaptation strategies of the vent microorganisms in shallow-water hydrothermal vents (HTVs). This study bridges this gap by providing insights into the phenomics and genomic diversity of genus Sulfurospirillum (order Campylobacterales, class Campylobacteria) based on data derived from a novel isolate obtained from shallow-water HTVs. Our mesophilic isolate of Sulfurospirillum not only augments the genus diversity of Campylobacteria pure cultures derived from vent systems but also serves as the inaugural reference isolate for Campylobacteria in shallow-water environments.

The deep-sea harbors abundant prokaryotic biomass is a major site of organic carbon remineralization and long-term carbon burial in the ocean. Deep-sea trenches are the deepest part of the ocean, and their special geological and morphological features promoting the accumulation of organic matter and active organic carbon turnover. Despite the expanding reports about the organic matter inputs, limited information is known regarding microbial processes in deep-sea trenches. In this study, we investigated the species composition and metabolic potential in surface sediment of the New Britain Trench (NBT), using a metagenomic approach. The predominant microbial taxa in NBT sediment include Proteobacteria, Acidobacteria, Planctomycetes, Actinobacteria and Chloroflexota. The microbial communities showed highly diverse metabolic potentials. Particularly, genes encoding enzymes for degradation of aromatic compounds, as well as those encoding haloalkane dehalogenase and haloacetate dehalogenase were annotated in the NBT surface sediment, which indicate the potential of microorganisms to degrade different types of refractory organic matter. The functional genes encoding enzymes for dissimilatory nitrate reduction, denitrification, and nitrification were also represented in the NBT metagenome. Overall, the microbial communities show high diversity of heterotrophic lineages and metabolic features, supporting their potential contributions in organic carbon metabolism. Meanwhile, Nitrosopumilus, a dominant genus in the surface sediment of the NBT, is a typical ammonia-oxidizing archaea (AOA), with autotrophic CO₂ fixation pathways including the 3-hydroxypropionate/4-hydroxybutylate (3HP/4HB) cycle, the reductive TCA (rTCA) cycle. The results demonstrate that autotrophic metabolic processes also play an important role in the surface sediment, by providing newly synthesized organic matter.