Microbes support enhanced nitrogen requirements of coral holobionts in a high CO₂ environment

Ocean acidification is posing a threat to calcifying organisms due to the increased energy requirements of calcification under high CO₂ conditions. The ability of scleractinian corals to cope with future ocean conditions will thus depend on their ability to fulfil their carbon requirement. However, the primary productivity of coral holobionts is limited by low nitrogen (N) availability in coral reef waters. Here, we employed CO₂ seeps of Tutum Bay (Papua New Guinea) as a natural laboratory to understand how coral holobionts offset their increased energy requirements under high CO₂ conditions. Our results demonstrate for the first time that under high pCO₂ conditions, N assimilation pathways of Pocillopora damicornis are jointly modified. We found that diazotroph-derived N assimilation rates in the Symbiodiniaceae were significantly higher in comparison to an ambient CO₂ control site, concomitant with a restructured diazotroph community and the specific prevalence of an alpha-proteobacterium. Further, corals at the high CO₂ site also had increased feeding rates on picoplankton and in particular exhibited selective feeding on Synechococcus sp., known to be rich in N. Given the high abundance of picoplankton in oligotrophic waters at large, our results suggest that corals exhibiting flexible diazotrophic communities and capable of exploiting N-rich picoplankton sources to offset their increased N requirements may be able to cope better in a high pCO₂ world.