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

ABSTRACT The Bay of Bengal (BoB) is the world’s largest bay, offering essential services like fishing and recreation while holding significant economic value for coastal communities. However, the BoB faces environmental challenges from monsoons, freshwater inputs, rising sea levels, and intensified cyclones due to climate change. Human activities such as tourism and development also impact the region, necessitating a global change perspective. Despite its importance, microbial diversity and ecology in the BoB remain largely unexplored. We focused on large and cell-associated viruses (i.e., originating from the cellular size fraction), particularly giant viruses and large phages in two BoB coastal sites: Cox’s Bazar, a populated beach with freshwater influences, and Saint Martin Island, a less affected resort island. Metagenomic sequencing reveals a higher abundance and diversity of viruses in Cox’s Bazar and presence of viruses that suggest freshwater intrusion and runoff. We identified 1962 putative phage genomes (10–655 kbp). Notably, 16 “large” phages >100 kbp were found in Saint Martin, and a terminase large subunit marker gene phylogeny revealed substantial diversity of large phages along the BoB coast. The BoB virome encodes diverse functionalities, with a greater presence of auxiliary metabolic genes in the Cox’s Bazar viral community. Additionally, five giant virus genomes (phylum Nucleocytoviricota) encoding various functionalities are reconstructed from Cox’s Bazar (83–876 kbp). This pioneering study revealing the viral diversity and host interactions in coastal BoB lays the foundation for future investigations into viral impact on biogeochemical cycles and the microbial food web in this understudied environment. 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.