Environmental viromes reveal the global distribution signatures of deep-sea DNA viruses.

INTRODUCTION: Viruses are abundant and ecologically significant in marine ecosystems. However, the virome of deep-sea sediments is not extensively investigated. OBJECTIVES: To explore the distribution pattern of deep-sea viruses on a global scale, the viromes of DNA viruses isolated from 138 sediments of 5 deep-sea ecosystems were characterized. METHODS: The viral particles were purified from each sediment sample. Then the viral DNAs were extracted and subjected to viral metagenomic analysis. RESULTS: Here, we constructed a global deep-sea environmental virome dataset by analyzing the viral DNA of 138 sediment samples. A total of 347,737 viral operational taxonomic units (vOTUs) were identified, of which 84.94% were hitherto unknown, indicating that deep sea was a reservoir of novel DNA viruses. Furthermore, circular viral genome analysis revealed 98,581 complete genomes. The classified vOTUs included eukaryotic (44.55%) and prokaryotic (25.75%) viruses, and were taxonomically assigned to 63 viral families. The composition and abundance of the deep-sea sediment viromes were dependent on the deep-sea ecosystem as opposed to geographical region. Further analysis revealed that the viral community differentiation in different deep-sea ecosystems was driven by the virus-mediated energy metabolism. CONCLUSION: Our findings showed that deep-sea ecosystems are a reservoir of novel DNA viruses and the viral community is shaped by the environmental characteristics of deep-sea ecosystems, thus presenting critical information for determining the ecological significance of viruses in global deep-sea ecosystems.

A dataset of micro biodiversity in benthic sediment at a global scale.

Microorganisms, occupying the largest biomass in deep sea, play essential roles in deep-sea ecosystem. It is believed that the microbes in deep-sea sediments are more representative of deep-sea microbial communities, the microbial composition of which is seldom affected by ocean currents. However, the community of benthic microbes on a global scale has not been adequately explored. Herein, we build a comprehensive global dataset determined by 16S rRNA gene sequencing to characterize the biodiversity of microorganisms in benthic sediment. The dataset comprised 212 records from 106 sites, included sequencing of bacteria and archaea for each site and yielded 4,766,502 and 1,562,989 reads, respectively. Through annotation, a total of 110,073 and 15,795 OTUs of bacteria and archaea were obtained, and 61 bacterial phyla and 15 archaeal phyla were identified, of which the dominant phyla were Proteobacteria and Thaumarchaeota in deep-sea sediment. Therefore, our findings provided a biodiversity data of microbial communities in deep-sea sediment at global-scale and laid a foundation to further reveal the structures of microorganism communities in deep sea.

Diversities and interactions of phages and bacteria in deep-sea sediments as revealed by metagenomics.

Phages are found virtually everywhere, even in extreme environments, and are extremely diverse both in their virion structures and in their genomic content. They are thought to shape the taxonomic and functional composition of microbial communities as well as their stability. A number of studies on laboratory culture and viral metagenomic research provide deeper insights into the abundance, diversity, distribution, and interaction with hosts of phages across a wide range of ecosystems. Although most of these studies focus on easily accessible samples, such as soils, lakes, and shallow oceans, little is known about bathypelagic phages. In this study, through analyzing the 16S rRNA sequencing and viral metagenomic sequencing data of 25 samples collected from five different bathypelagic ecosystems, we detected a high diversity of bacteria and phages, particularly in the cold seep and hydrothermal vent ecosystems, which have stable chemical energy. The relative abundance of phages in these ecosystems was higher than in other three abyssal ecosystems. The low phage/host ratios obtained from host prediction were different from shallow ecosystems and indicated the prevalence of prophages, suggesting the complexity of phage-bacteria interactions in abyssal ecosystems. In the correlation analysis, we revealed several phages-bacteria interaction networks of potential ecological relevance. Our study contributes to a better understanding of the interactions between bathypelagic bacteria and their phages.

Exosomes from WSSV-infected shrimp contain viral components that mediate virus infection.

Exosomes have been described as vesicles that mediate intercellular communication and thus affect normal and pathological processes. Furthermore, many viruses have been reported to deliver viral components to host cells through exosomes. However, the roles of exosomes in invertebrates response to virus infection are poorly understood. In this study, we found that exosomes purified from white spot syndrome virus (WSSV)-infected hemocytes of shrimp could promote viral replication. These exosomes contained WSSV genomic DNA and nucleocapsid protein VP15, suggesting that exosomes can transfer viral genetic materials between cells, although the exosomes did not have similar infection ability to viruses. Remarkably, in exosomes WSSV DNA was bound to VP15 protein, and moreover VP15 silencing significantly suppressed WSSV infection and reduced the WSSV genome fragments in exosomes, indicating that the presence of VP15 is required for the packing of WSSV DNA inside the exosomes and thereby assists virus to complete immune escape. The above results not only contribute to elucidation of the infection and transmission mechanisms of WSSV, but are also of great significance for further study of virus-host interaction and reasonable prevention measures. Taken together, our findings provide a novel insight into the regulation of virus transmission via exosomes and highlight potential therapeutic strategies.

Core Gut Microbiota of Shrimp Function as a Regulator to Maintain Immune Homeostasis in Response to WSSV Infection.

The gut microbiota is an integral part of the host and has a functional potential in host physiology. Numerous scientific efforts have opened new horizons in gut microbiota research and enhanced the understanding of host-microbe interactions in vertebrates. However, evidence on the association between the gut microbiota and immunity in invertebrates, especially in shrimp, which is an important aquatic animal, is limited. Herein, we conducted a comprehensive analysis based on 16S rRNA gene sequencing and liquid chromatography-coupled mass spectrometry (LC-MS) to investigate the correlation between them. Comparing the gut microbiota among the four different species of shrimp, we found huge variations and determined a core gut microbiota composed of 55 microbes. The environmental challenge of white spot syndrome virus (WSSV) infection led to changes in core microbial structures, but the alteration of core microbiota among different shrimp followed the same trend and showed immune-related function in the prediction of its metabolic potential. In metabolomic analysis, nine significantly upregulated metabolites found after viral infection indicated that they have antiviral potential. Moreover, we found a tight correlation between them and almost half of the core microbiota. These data demonstrate that these metabolites are responsible for maintaining the immune homeostasis of the host and prove the function of the gut microbiota and the related metabolome in antiviral immunity of shrimp. IMPORTANCE Abundant gut microorganisms constitute a complex microecosystem with the intestinal environment of the host, which plays a critical role in the adjustment of various physiological states of the organism. Sequencing and mass spectrometry data collected from intestinal samples of shrimp after virus infection helped to investigate the special function of the microecosystem and suggested that the gut microbiota has a functional potential in maintaining immune homeostasis of the host under environmental challenge.

Artificial construction of the biocoenosis of deep-sea ecosystem via seeping methane.

Deep-sea ecosystems, such as cold seeps and hydrothermal vents, have high biomass, even though they are located in the benthic zone, where no sunlight is present to provide energy for organism proliferation. Based on the coexistence of the reduced gases and chemoautotrophic microbes, it is inferred that the energy from the reduced gases supports the biocoenosis of deep-sea ecosystems. However, there is no direct evidence to support this deduction. Here, we developed and placed a biocoenosis generator, a device that continuously seeped methane, on the 1000-m deep-sea floor of the South China Sea to artificially construct a deep-sea ecosystem biocoenosis. The results showed that microorganisms, including bacteria and archaea, appeared in the biocoenosis generator first, followed by jellyfish and Gammaridea arthropods, indicating that a biocoenosis had been successfully constructed in the deep sea. Anaerobic methane-oxidizing archaea, which shared characteristics with the archaea of natural deep-sea cold seeps, acted as the first electron acceptors of the emitted methane; then, the energy in the electrons was transferred to downstream symbiotic archaea and bacteria and finally to animals. Nitrate-reducing bacteria served as partners to complete anaerobic oxidation of methane process. Further analysis revealed that viruses coexisted with these organisms during the origin of the deep-sea biocoenosis. Therefore, our study mimics a natural deep-sea ecosystem and provides the direct evidence to show that the chemical energy of reduced organic molecules, such as methane, supports the biocoenosis of deep-sea ecosystems.

A Novel Benzoquinone Compound Isolated from Deep-Sea Hydrothermal Vent Triggers Apoptosis of Tumor Cells.

Microorganisms are important sources for screening bioactive natural products. However, natural products from deep-sea microbes have not been extensively explored. In this study, the metabolites of bacteriophage GVE2 -infected (Geobacillus sp. E263 virus) thermophilic bacterium Geobacillus sp. E263, which was isolated from a deep-sea hydrothermal vent, were characterized. A novel quinoid compound, which had anti-tumor activity, was isolated from the phage-challenged thermophile. The chemical structure analysis showed that this novel quinoid compound was 2-amino-6-hydroxy-[1,4]-benzoquinone. The results indicated that 2-amino-6-hydroxy-[1,4]-benzoquinone and its two derivatives could trigger apoptosis of gastric cancer cells and breast cancer cells by inducing the accumulation of intracellular reactive oxygen species. Therefore, our study highlighted that the metabolites from the phage-challenged deep-sea microbes might be a kind of promising sources for anti-tumor drug discovery, because of the similarity of metabolic disorder between bacteriophage-infected microbes and tumor cells.