Habitat- and lifestyle-dependent structural and functional characteristics of viruses in mangrove wetlands of different functional zonings

Abstract

Mangrove wetlands, as one of the natural ecosystems with the most ecological services, have garnered widespread attention about their microbial driven biogeochemical cycling. Urbanization have led to different spatial patterns of environmental conditions and microbial communities in mangroves. However, viruses, as the pivotal drivers of biogeochemical cycling in mangroves, remain inadequately explored in terms of how their ecological potential and complex interactions with host respond to functional zonings. To address this knowledge gap, we conducted a comprehensive investigation on the structural and functional properties of temperate and lytic viruses in mangrove wetlands from different functional zonings by jointly using high-throughput sequencing, prokaryotic and viral metagenomics. Multiple environmental factors were found to significantly influence the taxonomic and functional composition, as well as lysogen-lysis decision-making of mangrove viruses. Furthermore, enriched auxiliary metabolic genes (AMGs) involved in methane, nitrogen and sulfur metabolism, and heavy metal resistance were unveiled in mangrove viruses, whose community composition was closely related to lifestyle and host. The virus-host pairs with different lifestyles were also discovered to react to environmental changes in different ways, which provided an empirical evidence for how virus and bacteria dynamics were specific to viral lifestyles in nature. This study expands our comprehension of the intricate interactions among virus, prokaryotic host and the environment in mangrove wetlands from multiple perspectives, including viral lifestyles, virus-host interactions, and habitat dependence. Importantly, it provides a new ecological perspective on how mangrove viruses are adapted to the stress posed by urbanization.