Central carbon metabolism switching in lytic versus temperate coral reef viral communities

Coral reefs are declining globally due in part to bacterial overgrowth, a process known as microbialization. However, the role of bacteriophages that may inhibit microbialization by infecting and killing these bacteria remains poorly understood, especially their metabolic impacts on bacterial proliferation. To address this, we analyzed central carbon metabolism gene frequencies in viral communities from healthy (lytic-dominated) and degraded (temperate-dominated) Central Pacific coral reefs. We found that viral communities shifted broadly from enrichment in genes associated with reactions that build up pools of central intermediates on degraded, temperate-dominated reefs (‘anaplerotic’ reactions) to enrichment in genes associated with reactions that consume these pools to generate metabolic precursors for virion construction on healthy, lytic-dominated reefs (‘cataplerotic’ reactions). This switch was shown by the over-representation of Entner-Doudoroff (ED) glycolysis genes on degraded, temperate-dominated reefs and, on healthy, lytic-dominated reefs, by a cross-pathway enrichment of cataplerotic genes, including transaldolase and NADH-producing oxidoreductases. To explore the ecological implications of these observations, we incorporated them into a conceptual model with coral, algae, bacterial, and viral ‘populations’ and qualitative ‘high’ and ‘low’ rates linking them based on our findings and existing knowledge of healthy and degraded reefs. The model suggests two contrasting ecosystem scenarios: one in which lytic viral metabolism may enhance viral production and bacterial control, and another in which temperate viral metabolism may favor bacterial proliferation. This framework identifies viral metabolism as an important and underexplored dimension of coral reef ecology and a promising avenue for future conservation research.