Lake Pavin: A pioneer site for ecological studies of freshwater viruses

Abstract

Since the discovery, 2-3 decades ago, that viruses of microbes are abundant in marine ecosystems, aquatic viral ecology has grown increasingly to reach the status of a full scientific discipline in environmental sciences. A dedicated society, the International Society for Viruses of Microorganisms (ISVM) (http://www.isvm.org/), was recently launched. Increasing studies in aquatic viral ecology are a source of novel knowledge related to the biodiversity, the functioning of ecosystems and the evolution of the cellular world. This is because viruses are perhaps the most diverse, abundant, and ubiquitous biological entities in the world’s aquatic ecosystems. They exhibit various lifestyles that intimately depend on living cell metabolism, and are ultimately replicated by members of all three domains of life (Bacteria, Eukarya, Archaea). This establishes viruses as microbial killers and manipulators in the hydrosphere. Lake Pavin is one of the pioneer sites where original ecological data were first provided on the qualitative, quantitative and functional significance of both lytic and temperate viruses of prokaryotes in temperate freshwater lakes, taking into account both seasonal and depth-related variability in the water column and in the sediments. These data were acquired by means of original protocols we developed. In addition to these protocols, we herein provide a synthesis of Lake Pavin studies on viral ecology, focusing on: (i) spatio-temporal dynamics of the diversity of viral communities, (ii) the significance of seasonal and depth-related variations of viral abundance and lytic and lysogenic activities, and (iii) the relative importance of lytic viruses and grazers for bacterial mortality and the biogeochemical implications for the food web dynamics. Unexpected and novel putative viruses were discovered in the deep-aged, dark, and permanently anoxic monimolimnic waters and sediments of Lake Pavin, highlighting the possible endemicity of these habitats. Some of these original viruses resembled dsDNA viruses of hyperthermophilic and hyperhalophilic Archaea. Unusual types of spherical and cubic virus-like particles (VLPs) were also observed for the first time. Infected prokaryotic cells were detected in deep sediment cores, and their vertical distribution correlated with both viral and prokaryotic abundances. Pleomorphic ellipsoid VLPs were visible in filamentous cells tentatively identified as representatives of the archaeal genus Methanosaeta, a major group of methane producers on Earth.