Phylogenetic proximity drives temporal succession of marine giant viruses in a five-year metagenomic time-series.

Nucleocytoplasmic Large DNA Viruses (NCLDVs, also called giant viruses) are widespread in marine systems and infect a broad range of microbial eukaryotes (protists). Recent biogeographic work has provided global snapshots of NCLDV diversity and community composition across the world's oceans, yet little information exists about the guiding 'rules' underpinning their community dynamics over time. We leveraged a five-year monthly metagenomic time-series to quantify the community composition of NCLDVs off the coast of Southern California and characterize these populations' temporal dynamics. NCLDVs were dominated by Algavirales (Phycodnaviruses, 59%) and Imitervirales (Mimiviruses, 36%). We identified clusters of NCLDVs with distinct classes of seasonal and non-seasonal temporal dynamics. Overall, NCLDV population abundances were often highly dynamic with a strong seasonal signal. The Imitervirales group had highest relative abundance in the more oligotrophic late summer and fall, while Algavirales did so in winter. Generally, closely related strains had similar temporal dynamics, suggesting that evolutionary history is a key driver of the temporal niche of marine NCLDVs. However, a few closely-related strains had drastically different seasonal dynamics, suggesting that while phylogenetic proximity often indicates ecological similarity, occasionally phenology can shift rapidly, possibly due to host-switching. Finally, we identified distinct functional content and possible host interactions of two major NCLDV orders-including connections of Imitervirales with primary producers like the diatom Chaetoceros and widespread marine grazers like Paraphysomonas and Spirotrichea ciliates. Together, our results reveal key insights on season-specific effect of phylogenetically distinct giant virus communities on marine protist metabolism, biogeochemical fluxes and carbon cycling.

Active prokaryotic and eukaryotic viral ecology across spatial scale in a deep-sea brine pool.

Deep-sea brine pools represent rare, extreme environments, providing unique insight into the limits of life on Earth, and by analogy, the plausibility of life beyond it. A distinguishing feature of many brine pools is presence of thick microbial mats that develop at the brine-seawater interface. While these bacterial and archaeal communities have received moderate attention, viruses and their host interactions in these environments remain underexplored. To bridge this knowledge gap, we leveraged metagenomic and metatranscriptomic data from three distinct zones within the NEOM brine pool system (Gulf of Aqaba) to reveal the active viral ecology around the pools. We report a remarkable diversity and activity of viruses infecting microbial hosts in this environment, including giant viruses, RNA viruses, jumbo phages, and Polinton-like viruses. Many of these form distinct clades-suggesting presence of untapped viral diversity in this ecosystem. Brine pool viral communities exhibit zone-specific differences in infection strategy-with lysogeny dominating the bacterial mat further away from the pool's center. We linked viruses to metabolically important prokaryotes-including association between a jumbo phage and a key manganese-oxidizing and arsenic-metabolizing bacterium. These foundational results illuminate the role of viruses in modulating brine pool microbial communities and biogeochemistry through revealing novel viral diversity, host associations, and spatial heterogeneity in viral dynamics.

Phylogenetic diversity and functional potential of large and cell-associated viruses in the Bay of Bengal.

IMPORTANCE: The BoB, the world's largest bay, is of significant economic importance to surrounding countries, particularly Bangladesh, which heavily relies on its coastal resources. Concurrently, the BoB holds substantial ecological relevance due to the region's high vulnerability to climate change-induced impacts. Yet, our understanding of the BoB's microbiome in relation to marine food web and biogeochemical cycling remains limited. Particularly, there are little or no data on the viral diversity and host association in the BoB. We examined the viral community in two distinct BoB coastal regions to reveal a multitude of viral species interacting with a wide range of microbial hosts, some of which play key roles in coastal biogeochemical cycling or potential pathogens. Furthermore, we demonstrate that the BoB coast harbors a diverse community of large and giant viruses, underscoring the importance of investigating understudied environments to discover novel viral lineages with complex metabolic capacities.

Phylogenetic diversity and functional potential of the microbial communities along the Bay of Bengal coast.

The Bay of Bengal, the world's largest bay, is bordered by populous countries and rich in resources like fisheries, oil, gas, and minerals, while also hosting diverse marine ecosystems such as coral reefs, mangroves, and seagrass beds; regrettably, its microbial diversity and ecological significance have received limited research attention. Here, we present amplicon (16S and 18S) profiling and shotgun metagenomics data regarding microbial communities from BoB's eastern coast, viz., Saint Martin and Cox's Bazar, Bangladesh. From the 16S barcoding data, Proteobacteria appeared to be the dominant phylum in both locations, with Alteromonas, Methylophaga, Anaerospora, Marivita, and Vibrio dominating in Cox's Bazar and Pseudoalteromonas, Nautella, Marinomonas, Vibrio, and Alteromonas dominating the Saint Martin site. From the 18S barcoding data, Ochrophyta, Chlorophyta, and Protalveolata appeared among the most abundant eukaryotic divisions in both locations, with significantly higher abundance of Choanoflagellida, Florideophycidae, and Dinoflagellata in Cox's Bazar. The shotgun sequencing data reveals that in both locations, Alteromonas is the most prevalent bacterial genus, closely paralleling the dominance observed in the metabarcoding data, with Methylophaga in Cox's Bazar and Vibrio in Saint Martin. Functional annotations revealed that the microbial communities in these samples harbor genes for biofilm formation, quorum sensing, xenobiotics degradation, antimicrobial resistance, and a variety of other processes. Together, these results provide the first molecular insight into the functional and phylogenetic diversity of microbes along the BoB coast of Bangladesh. This baseline understanding of microbial community structure and functional potential will be critical for assessing impacts of climate change, pollution, and other anthropogenic disturbances on this ecologically and economically vital bay.

Virologs, viral mimicry, and virocell metabolism: the expanding scale of cellular functions encoded in the complex genomes of giant viruses.

The phylum Nucleocytoviricota includes the largest and most complex viruses known. These "giant viruses" have a long evolutionary history that dates back to the early diversification of eukaryotes, and over time they have evolved elaborate strategies for manipulating the physiology of their hosts during infection. One of the most captivating of these mechanisms involves the use of genes acquired from the host-referred to here as viral homologs or "virologs"-as a means of promoting viral propagation. The best-known examples of these are involved in mimicry, in which viral machinery "imitates" immunomodulatory elements in the vertebrate defense system. But recent findings have highlighted a vast and rapidly expanding array of other virologs that include many genes not typically found in viruses, such as those involved in translation, central carbon metabolism, cytoskeletal structure, nutrient transport, vesicular trafficking, and light harvesting. Unraveling the roles of virologs during infection as well as the evolutionary pathways through which complex functional repertoires are acquired by viruses are important frontiers at the forefront of giant virus research.