Analysis of virus genomes from glacial environments reveals novel virus groups with unusual host interactions

Microbial communities in glacial ecosystems are diverse, active, and subjected to strong viral pressures and infection rates. In this study we analyse putative virus genomes assembled from three dsDNA viromes from cryoconite hole ecosystems of Svalbard and the Greenland Ice Sheet to assess the potential hosts and functional role viruses play in these habitats. We assembled 208 million reads from the virus-size fraction and developed a procedure to select genuine virus scaffolds from cellular contamination. Our curated virus library contained 546 scaffolds up to 230 Kb in length, 54 of which were circular virus consensus genomes. Analysis of virus marker genes revealed a wide range of viruses had been assembled, including bacteriophages, cyanophages, nucleocytoplasmic large DNA viruses and a virophage, with putative hosts identified as Actinobacteria, Alphaproteobacteria, Cyanobacteria, Firmicutes, Gammaproteobacteria, eukaryotic algae and amoebae. Whole genome comparisons revealed the majority of circular genome scaffolds formed 12 novel groups, two of which contained multiple phage members with plasmid-like properties, including a group of phage-plasmids possessing plasmid-like partition genes and toxin-antitoxin addiction modules to ensure their replication and a satellite phage-plasmid group. Surprisingly we also assembled a phage that not only encoded plasmid partition genes, but a clustered regularly interspaced short palindromic repeat (CRISPR)/Cas adaptive bacterial immune system. One of the spacers was an exact match for another phage in our virome, indicating that in a novel use of the system, the lysogen was potentially capable of conferring immunity on its bacterial host against other phage. Together these results suggest that highly novel and diverse groups of viruses are present in glacial environments, some of which utilise very unusual life strategies and genes to control their replication and maintain a long-term relationship with their hosts

Flexible genes establish widespread bacteriophage pan-genomes in cryoconite hole ecosystems

Bacteriophage genomes rapidly evolve via mutation and horizontal gene transfer to counter evolving bacterial host defenses; such arms race dynamics should lead to divergence between phages from similar, geographically isolated ecosystems. However, near-identical phage genomes can reoccur over large geographical distances and several years apart, conversely suggesting many are stably maintained. Here, we show that phages with near-identical core genomes in distant, discrete aquatic ecosystems maintain diversity by possession of numerous flexible gene modules, where homologous genes present in the pan-genome interchange to create new phage variants. By repeatedly reconstructing the core and flexible regions of phage genomes from different metagenomes, we show a pool of homologous gene variants co-exist for each module in each location, however, the dominant variant shuffles independently in each module. These results suggest that in a natural community, recombination is the largest contributor to phage diversity, allowing a variety of host recognition receptors and genes to counter bacterial defenses to co-exist for each phage

Supporting information for "Flexible genes establish widespread bacteriophage pan-genomes in cryoconite hole ecosystems"

Bacteriophage genomes rapidly evolve via mutation and horizontal gene transfer to counter evolving bacterial host defenses; such arms race dynamics should lead to divergence between phages from similar, geographically isolated ecosystems. However, near-identical phage genomes can reoccur over large geographical distances and several years apart, conversely suggesting many are stably maintained. Here, we show that phages with near-identical core genomes in distant, discrete aquatic ecosystems maintain diversity by possession of numerous flexible gene modules, where homologous genes present in the pan-genome interchange to create new phage variants. By repeatedly reconstructing the core and flexible regions of phage genomes from different metagenomes, we show a pool of homologous gene variants co-exist for each module in each location, however, the dominant variant shuffles independently in each module. These results suggest that in a natural community, recombination is the largest contributor to phage diversity, allowing a variety of host recognition receptors and genes to counter bacterial defenses to co-exist for each phage

Productivity, Wages, and Marriage: The Case of Major League Baseball

The effect of marriage on productivity and, consequently, wages has been long debated in economics. A primary explanation for the impact of marriage on wages has been through its impact on productivity, however, there has been no direct evidence for this. In this paper, we aim to fill this gap by directly measuring the impact of marriage on productivity using a sample of professional baseball players from 1871 - 2007. Our results show that only lower ability men see an increase in productivity, though this result is sensitive to the empirical specification and weakly significant. In addition, despite the lack of any effect on productivity, high ability married players earn roughly 16 - 20 percent more than their single counterparts. We discuss possible reasons why employers may favor married men

Nitrogen and sulfur metabolisms encoded in prokaryotic communities associated with sea ice algae

Sea ice habitats harbour seasonally abundant microalgal communities, which can be highly productive in the spring when the availability of light increases. An active, bloom-associated prokaryotic community relies on these microalgae for their organic carbon requirements, however an analysis of the encoded metabolic pathways within them is lacking. Hence, our understanding of biogeochemical cycling within sea ice remains incomplete. Here, we generated metagenomic assembled genomes from the bottom of first-year sea ice in northwestern Hudson Bay, during a spring diatom bloom. We show that the prokaryotic community had the metabolic potential to degrade algal derived dimethylsulphoniopropionate and oxidise sulfur. Facultative anaerobic metabolisms, specifically, dissimilatory nitrate reduction and denitrification were also prevalent here, suggesting some sea ice prokaryotes are metabolically capable of adapting to fluctuating oxygen levels during algal bloom conditions. Such denitrification could be an important loss of fixed-N2 in the changing Arctic marine system

Viral impacts on bacterial communities in Arctic cryoconite

The surfaces of glaciers are extreme ecosystems dominated by microbial communities. Viruses are found in abundance here, with a high frequency of bacteria displaying visible virus infection. In this study, viral and bacterial production was measured in Arctic cryoconite holes to address the control that viruses play in these highly truncated ecosystems. Mean bacterial carbon production in the sediments of cryoconite holes was found to be 57.8 ± 12.9 ng C g ^−1 dry wt. h ^−1 , which predicted a mean of 1.89–5.41 × 10 ^6  cells g ^−1 dry wt. h ^−1 based on a range of conversion factors. Relative to this, virus production was found to be high, up to 8.98 × 10 ^7 virus like particles g ^−1 dry wt. h ^−1 were produced, which is comparable to virus production in sediments around the globe. The virus burst size was assessed by transmission electron microscopy and found to be amongst the lowest recorded in the literature (mean 2.4). Hence, to account for the measured virus production, the viral induced bacterial mortality was calculated to be more than capable of accounting for the mortality of all bacterial production. The data presented here, therefore, suggests that viral induced mortality is a dominant process for the release and recycling of carbon and nutrients in supraglacial ecosystems

Giant viral signatures on the Greenland ice sheet

Dark pigmented snow and glacier ice algae on glaciers and ice sheets contribute to accelerating melt. The biological controls on these algae, particularly the role of viruses, remain poorly understood. Giant viruses, classified under the nucleocytoplasmic large DNA viruses (NCLDV) supergroup (phylum Nucleocytoviricota), are diverse and globally distributed. NCLDVs are known to infect eukaryotic cells in marine and freshwater environments, providing a biological control on the algal population in these ecosystems. However, there is very limited information on the diversity and ecosystem function of NCLDVs in terrestrial icy habitats. In this study, we investigate for the first time giant viruses and their host connections on ice and snow habitats, such as cryoconite, dark ice, ice core, red and green snow, and genomic assemblies of five cultivated Chlorophyta snow algae. Giant virus marker genes were present in almost all samples; the highest abundances were recovered from red snow and the snow algae genomic assemblies, followed by green snow and dark ice. The variety of active algae and protists in these GrIS habitats containing NCLDV marker genes suggests that infection can occur on a range of eukaryotic hosts. Metagenomic data from red and green snow contained evidence of giant virus metagenome-assembled genomes from the orders Imitervirales, Asfuvirales, and Algavirales. Our study highlights NCLDV family signatures in snow and ice samples from the Greenland ice sheet. Giant virus metagenome-assembled genomes (GVMAGs) were found in red snow samples, and related NCLDV marker genes were identified for the first time in snow algal culture genomic assemblies; implying a relationship between the NCLDVs and snow algae. Metatranscriptomic viral genes also aligned with metagenomic sequences, suggesting that NCLDVs are an active component of the microbial community and are potential "top-down" controls of the eukaryotic algal and protistan members. This study reveals the unprecedented presence of a diverse community of NCLDVs in a variety of glacial habitats dominated by algae