Characteristics and ecological functions of deep-sea viruses

Abstract

Believed to be the most abundant (~1030) biological agents in the ocean, viruses play an important role in microbial metabolism, prokaryotic mortality, and nutrient recycling in marine ecosystems, thereby significantly influencing the geochemical cycles of our planet. The importance of viruses in the surface ocean has been well recognized, however we are just beginning to understand the viral role and the underlying mechanism in the deep ocean. As an essential part of the marine environment, the abyssal ocean has extensive material and energy exchanges with the upper ocean and the deep biosphere, and they constitute an integral whole of the marine ecosystem. With an average depth of approximately 3800 m, the benthic environment is characterized by total darkness, low temperature ( (>10 MPa). The deep-sea inhabited microorganisms, including viruses, are believed to develop unique strategy to survive under multiple extreme environmental stresses. Studies on deep-sea viruses have revealed their abundance, diversity, and important ecological functions. In this review, advances in research on deep-sea viruses are summarized into four parts: general features, relationship between environmental factors and deep-sea viruses, isolation and characterization of representative viruses, and significant influences of the viriobenthos on the physiological and ecological function of deep-sea microorganisms. In general, the functions of viruses in the deep-sea environment mainly include two aspects: First, the regulation of material and energy cycle (viral shunt) and the dynamic change in ecosystem composition (balance of microbial communities) modulated by viral lysis; second, the expression of viral metabolic related genes (auxiliary metabolism) and the effect of viruses on host physiological activities (environmental adaptability). The former has been widely recognized, but the influence and molecular mechanism of the latter in the extreme deep-sea environment need to be further investigated. Here, we propose research directions and challenges in this field to undertake in future studies. Notably, the relationship between environmental factors and deep-sea viruses remains poorly understood. A deep-sea viral-host model system must be developed to investigate the underlying regulatory mechanism of gene expression and the interaction between deep-sea viruses and their hosts under extreme environmental conditions. At present, the number of isolated deep-sea viruses is less than 30, which is below 1% of the total number of viruses in the International Virus Classification Database. In terms of classification, most of the isolated deep-sea viruses belong to Caudovirales , and nearly no representatives have been identified yet from other viral orders. Furthermore, deep-sea viruses have been rarely subjected to in-depth study possibly because of very few benthic microorganisms with genetic operating system. In addition to maximizing the use of existing virus-host systems, scholars must focus on isolating other representative deep-sea viruses. Although our understanding on viriobenthos is still far from complete, data provided here encourage us to hypothesize that viruses are the key component of the benthic ecosystem and play an indispensable role in the deep ocean and deep biosphere.