Top‐heavy trophic structure within benthic viral dark matter

Abstract

AbstractA better understanding of system‐specific viral ecology in diverse environments is needed to predict patterns of virus–host trophic structure in the Anthropocene. This study characterised viral‐host trophic structure within coral reef benthic cyanobacterial mats—a globally proliferating cause and consequence of coral reef degradation. We employed deep longitudinal multi‐omic sequencing to characterise the viral assemblage (ssDNA, dsDNA, and dsRNA viruses) and profile lineage‐specific host–virus interactions within benthic cyanobacterial mats sampled from Bonaire, Caribbean Netherlands. We recovered 11,012 unique viral populations spanning at least 10 viral families across the orders Caudovirales, Petitvirales, and Mindivirales. Gene‐sharing network analyses provided evidence for extensive genomic novelty of mat viruses from reference and environmental viral sequences. Analysis of coverage ratios of viral sequences and computationally predicted hosts spanning 15 phyla and 21 classes revealed virus–host abundance (from DNA) and activity (from RNA) ratios consistently exceeding 1:1, suggesting a top‐heavy intra‐mat trophic structure with respect to virus–host interactions. Overall, our article contributes a curated database of viral sequences found in Caribbean coral reef benthic cyanobacterial mats (vMAT database) and provides multiple lines of field‐based evidence demonstrating that viruses are active members of mat communities, with broader implications for mat functional ecology and demography.