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

Abstract

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.

Highly Variable and Non-complex Diazotroph Communities in Corals From Ambient and High CO2 Environments

“…Sample collection took place during the boreal spring, between May 26th and June 7th 2018, aboard the R/V Alis, as described in Meunier et al (2021b). At a hydrothermal vent area at Tutum Bay (Ambitle Island, New Ireland Province, Papua New Guinea), samples were collected from one site exposed to high pCO 2 (4 • 3 44.82 S 153 • 34 56.09 E) and one reference (control) site with ambient pCO 2 (4 • 4 0.60 S 153 • 34 41.43 E) located ca.…”

“…Samples were immersed in DNA/RNA Shield (Zymo, Freiburg, Germany) and shipped on dry ice for DNA extraction, nifH amplification, and sequencing. The P. damicornis samples are the same as those analyzed in Meunier et al (2021b).…”

Regulation of the Coral-Associated Bacteria and Symbiodiniaceae in Acropora valida Under Ocean Acidification

“…The diameter of each circle is proportional to the abundance of the group. Baghdasarian et al, 2017;Krueger et al, 2017;Meunier et al, 2021;Zhou et al, 2021). For example, Noonan and Fabricius (2015) studied the response of Seriatopora hystrix and Acropora millepora to ocean acidification, finding that elevated CO 2 partial pressure (pH 7.79) had no adverse effects on both coral (Noonan and Fabricius, 2015).…”

“…The increase in Cyanobacteria is likely to provide compensation for the photosynthesis of coral holobiont, ensuring the energy supply that is needed by corals in low pH environments. A new study by Meunier et al (2021) found that at the CO 2 seeps of Tutum Bay (PNG), P. damicornis modified its N assimilation pathways by utilizing picoplanktonsized unicellular Cyanobacteria (Synechococcus sp.) in oligotrophic waters to offset the increasing N requirements under high CO 2 (Meunier et al, 2021).…”

“…Several studies addressed the impact of high-temperature stress on coral holobionts (Thurber et al, 2009;Yu et al, 2020Yu et al, , 2021, whereas relatively few studies investigated the impact of ocean acidification on coral holobionts. Furthermore, the research on coral holobiont by ocean acidification has mainly focused on bacteria, which demonstrated that ocean acidification affects the community composition of adult coralassociated bacteria (Meron et al, 2011;Morrow et al, 2015;O'Brien et al, 2016;Meunier et al, 2021), which will further affect the acidification tolerance of the coral (Liang et al, 2017;Torda et al, 2017). Meron et al (2011) found that the diversity of Acropora eurystoma-associated bacteria significantly increased when seawater pH dropped from 8.2 to 7.3.…”