Bacteriophage replication strategies are associated with organic matter energy content on coral reefs

Bacteriophages, viruses that infect bacteria, play a crucial role in carbon cycling within marine environments. In coral reefs, dissolved organic matter (DOM) released by benthic primary producers such as algae fuels heterotrophic microbial growth, which can be detrimental to corals. While this microbialization process has been associated with the abundance and replication strategies of bacteriophages, the direct relationship between reef DOM composition and bacteriophage communities remains unclear. Here, we combine metabolomics, metagenomes, and viromes to demonstrate that phage abundances have significant relationships with DOM composition on the reefs of Curacao, Southern Caribbean. By constructing co-occurrence networks between free or cell-associated viruses and exometabolites, we identified thousands of statistically significant associations between phages and organic compounds. While total viral abundances did not significantly correlate with overall dissolved organic carbon (DOC) concentration, cell-associated phages had significantly more positive associations with compounds that had a reduced nominal oxidative state of carbon (NOSC). Furthermore, temperate phages were more frequently correlated with metabolites exhibiting higher Gibbs energy than lytic phages. Six of the ten viruses with the highest number of positive associations with metabolites were temperate (i.e., encoded an integrase or were identified as a prophage), despite this network consisting of approximately 90% lytic viruses. These temperate viruses were predicted to infect members of the genus Sphingobium. Together, these findings reveal a connection between phage replication strategies and DOM energy availability with potential implications for coral reef biogeochemistry. SignificanceCoral reefs are highly dynamic ecosystems where microbial communities and organic matter cycles are intricately linked. This study provides new insights into how bacteriophages interact with dissolved organic matter (DOM) composition, revealing that cell-associated bacteriophages, particularly temperate phages, are associated with more energy-rich organic compounds. These findings suggest that DOM may have a bottom-up influence on the lysis-lysogeny decision of temperate phages infecting their host or that lysogeny may play an underappreciated role in shaping the reef carbon cycle. Energy-rich organic compounds have generally been associated with increased algal abundances and coral decline. By demonstrating significant connections between viral infection strategies and the energy content of DOM, our results highlight the potential for phages to influence coral reef biogeochemistry and health.