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1. Potential virus-mediated nitrogen cycling in oxygen-depleted oceanic waters

   https://doi.org/10.1038/s41396-020-00825-6  

   Gazitúa, M. Consuelo ; Vik, Dean R. ; Roux, Simon ; Gregory, Ann C. ; Bolduc, Benjamin ; Widner, Brittany ; Mulholland, Margaret R. ; Hallam, Steven J. ; Ulloa, Osvaldo ; Sullivan, Matthew B. ( November 2020 , The ISME Journal)

   Viruses play an important role in the ecology and biogeochemistry of marine ecosystems. Beyond mortality and gene transfer, viruses can reprogram microbial metabolism during infection by expressing auxiliary metabolic genes (AMGs) involved in photosynthesis, central carbon metabolism, and nutrient cycling. While previous studies have focused on AMG diversity in the sunlit and dark ocean, less is known about the role of viruses in shaping metabolic networks along redox gradients associated with marine oxygen minimum zones (OMZs). Here, we analyzed relatively quantitative viral metagenomic datasets that profiled the oxygen gradient across Eastern Tropical South Pacific (ETSP) OMZ waters, assessing whether OMZ viruses might impact nitrogen (N) cycling via AMGs. Identified viral genomes encoded six N-cycle AMGs associated with denitrification, nitrification, assimilatory nitrate reduction, and nitrite transport. The majority of these AMGs (80%) were identified in T4-likeMyoviridaephages, predicted to infectCyanobacteriaandProteobacteria, or in unclassified archaeal viruses predicted to infectThaumarchaeota. Four AMGs were exclusive to anoxic waters and had distributions that paralleled homologous microbial genes. Together, these findings suggest viruses modulate N-cycling processes within the ETSP OMZ and may contribute to nitrogen loss throughout the global oceans thus providing a baseline for their inclusion in the ecosystem and geochemical models.
2. Viral elements and their potential influence on microbial processes along the permanently stratified Cariaco Basin redoxcline

   https://doi.org/10.1038/s41396-020-00739-3  

   Mara, Paraskevi ; Vik, Dean ; Pachiadaki, Maria G. ; Suter, Elizabeth A. ; Poulos, Bonnie ; Taylor, Gordon T. ; Sullivan, Matthew B. ; Edgcomb, Virginia P. ( August 2020 , The ISME Journal)

   Little is known about viruses in oxygen-deficient water columns (ODWCs). In surface ocean waters, viruses are known to act as gene vectors among susceptible hosts. Some of these genes may have metabolic functions and are thus termed auxiliary metabolic genes (AMGs). AMGs introduced to new hosts by viruses can enhance viral replication and/or potentially affect biogeochemical cycles by modulating key microbial pathways. Here we identify 748 viral populations that cluster into 94 genera along a vertical geochemical gradient in the Cariaco Basin, a permanently stratified and euxinic ocean basin. The viral communities in this ODWC appear to be relatively novel as 80 of these viral genera contained no reference viral sequences, likely due to the isolation and unique features of this system. We identify viral elements that encode AMGs implicated in distinctive processes, such as sulfur cycling, acetate fermentation, signal transduction, [Fe–S] formation, and N-glycosylation. These AMG-encoding viruses include two putative Mu-like viruses, and viral-like regions that may constitute degraded prophages that have been modified by transposable elements. Our results provide an insight into the ecological and biogeochemical impact of viruses oxygen-depleted and euxinic habitats.
3. Genomes from Uncultivated Pelagiphages Reveal Multiple Phylogenetic Clades Exhibiting Extensive Auxiliary Metabolic Genes and Cross-Family Multigene Transfers

   https://doi.org/10.1128/msystems.01522-21  

   Wittmers, Fabian ; Needham, David M. ; Hehenberger, Elisabeth ; Giovannoni, Stephen J. ; Worden, Alexandra Z. ( August 2022 , mSystems)

   Rappe, Michael S. (Ed.)

   ABSTRACT For the abundant marine Alphaproteobacterium Pelagibacter (SAR11), and other bacteria, phages are powerful forces of mortality. However, little is known about the most abundant Pelagiphages in nature, such as the widespread HTVC023P-type, which is currently represented by two cultured phages. Using viral metagenomic data sets and fluorescence-activated cell sorting, we recovered 80 complete, undescribed Podoviridae genomes that form 10 phylogenomically distinct clades (herein, named Clades I to X) related to the HTVC023P-type. These expanded the HTVC023P-type pan-genome by 15-fold and revealed 41 previously unknown auxiliary metabolic genes (AMGs) in this viral lineage. Numerous instances of partner-AMGs (colocated and involved in related functions) were observed, including partners in nucleotide metabolism, DNA hypermodification, and Curli biogenesis. The Type VIII secretion system (T8SS) responsible for Curli biogenesis was identified in nine genomes and expanded the repertoire of T8SS proteins reported thus far in viruses. Additionally, the identified T8SS gene cluster contained an iron-dependent regulator (FecR), as well as a histidine kinase and adenylate cyclase that can be implicated in T8SS function but are not within T8SS operons in bacteria. While T8SS are lacking in known Pelagibacter , they contribute to aggregation and biofilm formation in other bacteria. Phylogenetic reconstructions of partner-AMGs indicatemore »derivation from cellular lineages with a more recent transfer between viral families. For example, homologs of all T8SS genes are present in syntenic regions of distant Myoviridae Pelagiphages, and they appear to have alphaproteobacterial origins with a later transfer between viral families. The results point to an unprecedented multipartner-AMG transfer between marine Myoviridae and Podoviridae. Together with the expansion of known metabolic functions, our studies provide new prospects for understanding the ecology and evolution of marine phages and their hosts. IMPORTANCE One of the most abundant and diverse marine bacterial groups is Pelagibacter . Phages have roles in shaping Pelagibacter ecology; however, several Pelagiphage lineages are represented by only a few genomes. This paucity of data from even the most widespread lineages has imposed limits on the understanding of the diversity of Pelagiphages and their impacts on hosts. Here, we report 80 complete genomes, assembled directly from environmental data, which are from undescribed Pelagiphages and render new insights into the manipulation of host metabolism during infection. Notably, the viruses have functionally related partner genes that appear to be transferred between distant viruses, including a suite that encode a secretion system which both brings a new functional capability to the host and is abundant in phages across the ocean. Together, these functions have important implications for phage evolution and for how Pelagiphage infection influences host biology in manners extending beyond canonical viral lysis and mortality.« less
4. Double-stranded DNA virioplankton dynamics and reproductive strategies in the oligotrophic open ocean water column

   https://doi.org/10.1038/s41396-020-0604-8  

   Luo, Elaine ; Eppley, John M. ; Romano, Anna E. ; Mende, Daniel R. ; DeLong, Edward F. ( May 2020 , The ISME Journal)

   Abstract Microbial communities are critical to ecosystem dynamics and biogeochemical cycling in the open oceans. Viruses are essential elements of these communities, influencing the productivity, diversity, and evolution of cellular hosts. To further explore the natural history and ecology of open-ocean viruses, we surveyed the spatiotemporal dynamics of double-stranded DNA (dsDNA) viruses in both virioplankton and bacterioplankton size fractions in the North Pacific Subtropical Gyre, one of the largest biomes on the planet. Assembly and clustering of viral genomes revealed a peak in virioplankton diversity at the base of the euphotic zone, where virus populations and host species richness both reached their maxima. Simultaneous characterization of both extracellular and intracellular viruses suggested depth-specific reproductive strategies. In particular, analyses indicated elevated lytic interactions in the mixed layer, more temporally variable temperate phage interactions at the base of the euphotic zone, and increased lysogeny in the mesopelagic ocean. Furthermore, the depth variability of auxiliary metabolic genes suggested habitat-specific strategies for viral influence on light-energy, nitrogen, and phosphorus acquisition during host infection. Most virus populations were temporally persistent over several years in this environment at the 95% nucleic acid identity level. In total, our analyses revealed variable distributional patterns and diverse reproductive and metabolicmore »strategies of virus populations in the open-ocean water column.« less
5. Highly diverse and unknown viruses may enhance Antarctic endoliths’ adaptability

   https://doi.org/10.1186/s40168-023-01554-6  

   Ettinger, Cassandra L. ; Saunders, Morgan ; Selbmann, Laura ; Delgado-Baquerizo, Manuel ; Donati, Claudio ; Albanese, Davide ; Roux, Simon ; Tringe, Susannah ; Pennacchio, Christa ; del Rio, Tijana G. ; et al ( May 2023 , Microbiome)

   Rock-dwelling microorganisms are key players in ecosystem functioning of Antarctic ice free-areas. Yet, little is known about their diversity and ecology, and further still, viruses in these communities have been largely unexplored despite important roles related to host metabolism and nutrient cycling. To begin to address this, we present a large-scale viral catalog from Antarctic rock microbial communities.

   We performed metagenomic analyses on rocks from across Antarctica representing a broad range of environmental and spatial conditions, and which resulted in a predicted viral catalog comprising > 75,000 viral operational taxonomic units (vOTUS). We found largely undescribed, highly diverse and spatially structured virus communities which had predicted auxiliary metabolic genes (AMGs) with functions indicating that they may be potentially influencing bacterial adaptation and biogeochemistry.

   This catalog lays the foundation for expanding knowledge of virosphere diversity, function, spatial ecology, and dynamics in extreme environments. This work serves as a step towards exploring adaptability of microbial communities in the face of a changing climate.