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.

Discovery of several novel, widespread, and ecologically distinct marine Thaumarchaeota viruses that encode amoC nitrification genes

“…AMGs have been previously described for several enzymes involved in the biochemical cycles for most of the major elements comprising life including C, P, and S [23,[60][61][62]. Notably missing from this list were prominent N-related AMGs, but the discovery the nitrogen regulators ntcA in cyanophage [63]; P II and ammonia transporters (amt) on viral contigs [21]; amoC AMGs (in [21] and here); and more recently nitrate reductase genes in deep-sea vent viromes [64], have expanded the known set of key biogeochemical pathways impacted by viral AMGs. Viral infection should generally limit the abundance and thus contribution of Thaumarchaeota to nitrification, but cells infected by amoC-carrying viruses presumably still can contribute to nitrification.…”

Diverse viruses in deep-sea hydrothermal vent fluids have restricted dispersal across ocean basins

“…Previous work has suggested that viruses in hydrothermal systems have the genomic 561 capacity to alter their hosts' microbial metabolism through harboring auxiliary metabolic genes 562 (AMGs) [17][18][19]. We found a higher percentage of microbial genomes with putative viral 563 sequences (40%) than has been previously reported for single-cell genomes (SAGs, 10%) in 564 diffuse flow hydrothermal fluids [15].…”

Genome analysis of Crassaminicella sp. SY095, an anaerobic mesophilic marine bacterium isolated from a deep-sea hydrothermal vent on the Southwest Indian Ridge

“…[14,15]. In addition to acting as microbial predators, phages might confer an enhanced level of fitness to the microbial host, enhancing host survival in the extreme environment [16]. In the strain SY095 genome, four putative prophages were identified, named CTV1 to CTV4.…”