Deep-Sea Hydrothermal Vent Viruses Compensate for Microbial Metabolism in Virus-Host Interactions

Abstract

Viruses are believed to be responsible for the mortality of host organisms. However, some recent investigations reveal that viruses may be essential for host survival. To date, it remains unclear whether viruses are beneficial or harmful to their hosts. To reveal the roles of viruses in the virus-host interactions, viromes and microbiomes of sediment samples from three deep-sea hydrothermal vents were explored in this study. To exclude the influence of exogenous DNAs on viromes, the virus particles were purified with nuclease (DNase I and RNase A) treatments and cesium chloride density gradient centrifugation. The metagenomic analysis of viromes without exogenous DNA contamination and microbiomes of vent samples indicated that viruses had compensation effects on the metabolisms of their host microorganisms. Viral genes not only participated in most of the microbial metabolic pathways but also formed branched pathways in microbial metabolisms, including pyrimidine metabolism; alanine, aspartate, and glutamate metabolism; nitrogen metabolism and assimilation pathways of the two-component system; selenocompound metabolism; aminoacyl-tRNA biosynthesis; and amino sugar and nucleotide sugar metabolism. As is well known, deep-sea hydrothermal vent ecosystems exist in relatively isolated environments which are barely influenced by other ecosystems. The metabolic compensation of hosts mediated by viruses might represent a very important aspect of virus-host interactions.IMPORTANCE Viruses are the most abundant biological entities in the oceans and have very important roles in regulating microbial community structure and biogeochemical cycles. The relationship between virus and host microbes is broadly thought to be that of predator and prey. Viruses can lyse host cells to control microbial population sizes and affect community structures of hosts by killing specific microbes. However, viruses also influence their hosts through manipulation of bacterial metabolism. We found that viral genes not only participated in most microbial metabolic pathways but also formed branched pathways in microbial metabolisms. The metabolic compensation of hosts mediated by viruses may help hosts to adapt to extreme environments and may be essential for host survival.

Keywords: deep-sea hydrothermal vent; marine virus; metabolic compensation; microbial metabolism.

FIG 1

Bacterial OTUs (operational taxonomic units) for sediments from three deep-sea hydrothermal vents in the Southwest Indian Ocean. (A) Rarefaction curves of the bacterial 16S rRNA genes from three samples. (B) Venn diagram of bacterial OTU distributions in the three samples.

FIG 2

Relative abundance of bacterial families of sediments from three deep-sea hydrothermal vents in the Southwest Indian Ocean. The category “Others” represents the bacterial families with less than 1% of reads.

FIG 3

Viral and microbial metagenomes in deep-sea hydrothermal vents. (A) Taxonomic composition of the sequence contigs in SWIR-S004, SWIR-S021, and SWIR-S024 samples from deep-sea hydrothermal vents. (B) Examination of exogenous DNA contamination in the virome samples. The SYBR green-stained virome samples were examined by fluorescence microscopy (left). Bar, 5 μm. At the same time, the amplified bacterial 16S rRNA genes from the virome samples and the microbiome samples were analyzed by agarose gel electrophoresis (right). M, DNA marker. (C) TEM image of virus particles from deep-sea hydrothermal vent sediments. The arrows indicate the virus particles. Bar, 200 nm. (D) Taxonomic composition of sequence contigs in virome libraries (SWIR-S004, SWIR-S021, and SWIR-S024). The relative abundance of the sequence contigs was classified by the taxonomic grouping based on BLASTx similarity search (E value, <10⁻³).

FIG 4

Functional genes of viromes and microbiomes from deep-sea hydrothermal vents. (A) Classification of predicted genes of viromes. (B) Classification of predicted genes of microbiomes. Each letter on the abscissa axis represents an eggNOG functional category. Genes with eggNOG orthology but without functional description were referred to as “function unknown.”

FIG 5

Classification of metabolic pathways of viromes and microbiomes from three samples. The classification of metabolic pathways was obtained according to KEGG pathway databases. “Shared” represents the metabolic pathways shared by the virome and microbiome.

FIG 6

Metabolic compensation of viral genes in microbial metabolic pathways. (A) Pyrimidine metabolism pathway of microbes compensated by viral genes. EC 1.8.1.9, thioredoxin reductase; EC 1.17.4.1, ribonucleotide reductase, class II; EC 1.17.4.2, ribonucleoside-triphosphate reductase. (B) Microbial l-aspartate metabolism compensated by virus. EC 4.3.1.1, aspartate ammonia-lyase; EC 4.3.2.1, argininosuccinate lyase; EC 4.3.2.2, adenylosuccinate lyase; EC 6.3.4.4, adenylosuccinate synthase; EC 6.3.4.5, argininosuccinate synthase. (C) Metabolic compensation of viral genes in microbial two-component regulatory system. NarG, NarH, NarJ, and NarI, four subunits of nitrate reductase; NarX, nitrate-nitrite sensor histidine kinase; NarL, nitrate-nitrite response regulator; UhpC, sugar phosphate sensor protein. (D) Requirement of viral genes in selenocompound metabolism of microorganisms. CTH, cystathionine gamma-lyase; EC 2.9.1.1, l-seryl-tRNA (Ser) selenium transferase. (E) Crucial role of viral genes in aminoacyl-tRNA biosynthesis of microbes. EC 2.9.1.1, l-seryl-tRNA (Ser) selenium transferase. (F) Requirement for viral genes in amino sugar and nucleotide sugar metabolism. EC 2.6.1.102, perosamine synthetase; EC 1.1.1.281, GDP-4-dehydro-6-deoxy-d-mannose reductase; EC 2.6.1.87, UDP-4-amino-4-deoxy-l-arabinose-oxoglutarate aminotransferase. In all panels, the red, green, blue, and black boxes represent microbial genes, viral genes, genes shared by microbe and virus, and genes undetected in our work, respectively. The pathway compensated by virus is indicated with a dashed box.