Temperate and filamentous bacteriophages as reservoirs of bacterial virulence in stony coral tissue loss disease

Abstract

Lysogenic conversion, in which bacteriophages (viruses that infect bacteria) integrate into bacterial genomes and confer new phenotypic traits on their hosts, is a well-established mechanism for the emergence of pathogens. While this process underpins many bacterial diseases in humans and other animals, its role in coral disease remains largely unexplored. Here, we investigate the potential role of lysogenic conversion in stony coral tissue loss disease (SCTLD), which has caused unprecedented mortality of Caribbean corals since 2014 and for which the etiological agent remains unknown. Across 27 original coral samples and 178 publicly available metagenomes from the Florida Reef Tract spanning seven coral species, we detected a greater number of unique viral genomes capable of lysogeny in diseased corals or visually healthy portions of diseased corals (DD and HD, respectively) compared to visually healthy (VH) corals. SCTLD-associated bacteriophages were primarily predicted to infect bacterial taxa previously implicated in the disease, such as Vibrionales, Rhodobacterales, and Flavobacteriia, and carried abundant and widespread virulence genes with the potential to enhance bacterial colonization, competition, or direct host damage, including homologs of Tse2, Zot, RTX, pneumolysin, and cytolytic delta-endotoxin. Although causal relationships remain unresolved, our findings indicate that phages capable of lysogenic conversion have the genomic capacity to laterally transfer bacterial virulence genes in SCTLD-affected corals. The acquisition of genes via lysogenic conversion could contribute to bacterial virulence while maintaining community taxonomic profiles, helping to explain previous community profiling observations and providing a mechanistic framework for disease pathogenesis.