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

Abstract 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. Significance Coral reefs are collapsing worldwide, exacerbated by ‘microbialization,’ where algae-fueled bacteria overgrow corals. Viruses that infect these bacteria can suppress this process through lysis, but on degraded reefs they often switch to nonlethal temperate lifestyles, accelerating decline. Here we show that similar shifts occur in virus-associated metabolic gene content. On healthy reefs, lytic-associated viral communities contained higher frequencies of genes known to drain host metabolites to fuel virus production. At the ecosystem level, this may enhance viral production, infection and lysis rates, thereby helping to limit bacterial overgrowth. On degraded reefs, temperate-associated viral communities contained higher frequencies of genes whose products are known to expand host metabolite pools, possibly providing the energetic substrate to support bacterial proliferation. Taken together, our findings allow us to propose a framework linking viral infection strategy, viral metabolism, and reef microbialization. Within this framework, viral metabolism may either reinforce reef resilience or exacerbate collapse, providing a foundation to guide future work on the role of viruses in coral reef function and conservation.

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