Ocean acidification rapidly reduces dinitrogen fixation associated with the hermatypic coral Seriatopora hystrix

Abstract

Since productivity and growth of coral-associated dinoflagellate algae is nitrogen (N)-limited, dinitrogen (N 2 ) fixation by coral-associated microbes is likely crucial for maintaining the coral−dinoflagellate symbiosis. It is thus essential to understand the effects future climate change will have on N 2 fixation by the coral holobiont. This laboratory study is the first to investigate short-term effects of ocean acidification on N 2 fixation activity associated with the tropical, hermatypic coral Seriatopora hystrix using the acetylene reduction assay in combination with calcification measurements. Findings reveal that simulated ocean acidification ( pCO 2 1080 µatm) caused a rapid and significant decrease (53%) in N 2 fixation rates associated with S. hystrix compared to the present day scenario ( pCO 2 486 µatm). In addition, N 2 fixation associated with the coral holobiont showed a positive exponential relationship with its calcification rates. This suggests that even small declines in calcification rates of hermatypic corals under high CO 2 conditions may result in decreased N 2 fixation activity, since these 2 processes may compete for energy in the coral holobiont. Ultimately, an intensified N limitation in combination with a decline in skeletal growth may trigger a negative feedback loop on coral productivity exacerbating the negative long-term effects of ocean acidification.

Nitrogen cycling in corals: the key to understanding holobiont functioning?

“…This input of new fixed nitrogen into the reef ecosystem helps to sustain net productivity under oligotrophic conditions and to compensate for net nitrogen export from the system, for instance by currents [44]. Nitrogen fixation in hermatypic corals has been reported for several different species [45][46][47][48], suggesting a high relevance of this process for the coral holobiont. However, reported nitrogen fixation rates in corals are about a magnitude lower than those found in reef sediments and bare rock [43].…”

“…It is thus likely that similar regulatory mechanisms to reduce nitrogen fixation rates at times of excess nitrogen availability exist in coral-associated diazotrophs ( Figure 1). Nitrogen fixation activity in corals is highly dynamic and can be rapidly affected by changes in environmental conditions [46,48]. Consequently, nitrogen fixation may serve as a mechanism to counteract shortages of environmental nitrogen availability, and maintain a constant nitrogen supply for symbiont-based primary production in corals.…”

“…It has been shown that environmental conditions can affect nitrogen cycling in corals [46], and that nitrogen fixation in soft corals can supplement reduced nutrient availability in the Red Sea [97]. It is likely that these alterations in nitrogen-cycling capacity are the results of shifts within the coral microbiome.…”

Diazotrophs: Overlooked Key Players within the Coral Symbiosis and Tropical Reef Ecosystems?

“…Likewise, Davey et al (2008) showed that coral death as a result of thermal bleaching enhanced N 2 fixation through production of organic matter followed by the decay of coral tissue, which induced an increase in the development of microbial epiphytic and epilithic communities on coral skeletons. Finally, a recent study showed that low pH (decreased pCO 2 ) significantly decreased N 2 fixation associated with some coral species, likely due to a competition for energy between coral calcification or photosynthesis and N 2 fixation (Rädecker et al, 2014). Taken altogether, these observations suggest that more studies have to be undertaken to assess N 2 fixation rates in reefs under diverse environmental conditions, including climate change ones, because most of the knowledge comes from other systems and cannot be always applied to reef diazotrophs.…”

“…In such a scenario, it is likely that nutrient-limited corals will increasingly rely on DDN to meet their nitrogen metabolic requirements. Conversely, increased pCO 2 has been reported to decrease coral-associated N 2 fixation, suggesting that nitrogen starvation of the coral host may exacerbate the long-term effects of ocean acidification (Rädecker et al, 2014). Although we are just beginning to understand the effect of single stressors on N 2 fixation, additional multiple stressor studies are needed to assess synergistic or antagonistic climate change effects on coral-associated N 2 fixation and its responsible diazotroph communities.…”