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

Abstract

The Bay of Bengal (BoB), the largest bay in the world, provides valuable ecosystem services such as fishing and recreation to millions of people living along its coast and has a significant economic value. The BoB is impacted by various environmental factors such as seasonal monsoons and multiple freshwater inputs, and this region is particularly vulnerable to sea-level rise and increased frequency of devastating cyclones that are predicted to be exacerbated due to global climate change. These factors are also compounded by anthropogenic influences from tourism and development, making it an important ecosystem to understand and study from a global change perspective. Despite its importance, microbial diversity and ecology have remained largely understudied in this region. In this study, we describe the diversity and putative functional importance of large and cell-associated (that is, originating from the cellular size fraction) viruses from two coastal sites in the BoB, with an emphasis on giant viruses and large phages. Sites chosen for this study include Coxs Bazar, a populated beach with multiple freshwater inputs, and Saint Martin Island, a resort island that has considerably less human influence compared to Coxs Bazar. Through metagenomic sequencing, we were able to identify a more abundant and more diverse viral community at Coxs Bazar consisting of many viruses that are indicators of freshwater intrusion and runoff. Overall, 1962 putative phage genome bins were obtained ranging from 10 - 655 kilobase pairs (kbp) in sizes. Of these genomes, 16 from Saint Martin were found to be larger than 100kbp which we deemed "large" phages, and we were able to reconstruct a phylogeny of these large phages using the TerL gene as a marker. This phylogeny revealed clades enriched in large phages and a high diversity of large phage candidates in the Bay of Bengal coast. Protein annotation analysis showed a wide variety of functionality from both sites with more auxiliary metabolic genes (AMGs) found in the Coxs Bazar viral community. Five giant virus (Phylum Nucleocytoviricota) genomes were also reconstructed from Coxs Bazar and identified as belonging to the orders Imitervirales and Pandoravirales. These genomes ranged from 83 - 876 kbp in size and contained a wide range of encoded functionalities. To the best of our knowledge, our study represents the first insights on the phylogenetic and functional diversity of viruses in the Bay of Bengal. These results thus provide an important foundation for further studies on the impact of host-virus interactions on biogeochemical cycles and microbial food web in this understudied marine environment.