Ulisse Cardini

Benthic N2 fixation in coral reefs and the potential effects of human-induced environmental change

Tropical coral reefs are among the most productive and diverse ecosystems, despite being surrounded by ocean waters where nutrients are in short supply. Benthic dinitrogen (N2) fixation is a significant internal source of “new” nitrogen (N) in reef ecosystems, but related information appears to be sparse. Here, we review the current state (and gaps) of knowledge on N2 fixation associated with coral reef organisms and their ecosystems. By summarizing the existing literature, we show that benthic N2 fixation is an omnipresent process in tropical reef environments. Highest N2 fixation rates are detected in reef-associated cyanobacterial mats and sea grass meadows, clearly showing the significance of these functional groups, if present, to the input of new N in reef ecosystems. Nonetheless, key benthic organisms such as hard corals also importantly contribute to benthic N2 fixation in the reef. Given the usually high coral coverage of healthy reef systems, these results indicate that benthic symbiotic associations may be more important than previously thought. In fact, mutualisms between carbon (C) and N2 fixers have likely evolved that may enable reef communities to mitigate N limitation. We then explore the potential effects of the increasing human interferences on the process of benthic reef N2 fixation via changes in diazotrophic populations, enzymatic activities, or availability of benthic substrates favorable to these microorganisms. Current knowledge indicates positive effects of ocean acidification, warming, and deoxygenation and negative effects of increased ultraviolet radiation on the amount of N fixed in coral reefs. Eutrophication may either boost or suppress N2 fixation, depending on the nutrient becoming limiting. As N2 fixation appears to play a fundamental role in nutrient-limited reef ecosystems, these assumptions need to be expanded and confirmed by future research efforts addressing the knowledge gaps identified in this review.

Functional significance of dinitrogen fixation in sustaining coral productivity under oligotrophic conditions

Functional traits define species by their ecological role in the ecosystem. Animals themselves are host–microbe ecosystems (holobionts), and the application of ecophysiological approaches can help to understand their functioning. In hard coral holobionts, communities of dinitrogen (N2)-fixing prokaryotes (diazotrophs) may contribute a functional trait by providing bioavailable nitrogen (N) that could sustain coral productivity under oligotrophic conditions. This study quantified N2 fixation by diazotrophs associated with four genera of hermatypic corals on a northern Red Sea fringing reef exposed to high seasonality. We found N2 fixation activity to be 5- to 10-fold higher in summer, when inorganic nutrient concentrations were lowest and water temperature and light availability highest. Concurrently, coral gross primary productivity remained stable despite lower Symbiodinium densities and tissue chlorophyll a contents. In contrast, chlorophyll a content per Symbiodinium cell increased from spring to summer, suggesting that algal cells overcame limitation of N, an essential element for chlorophyll synthesis. In fact, N2 fixation was positively correlated with coral productivity in summer, when its contribution was estimated to meet 11% of the Symbiodinium N requirements. These results provide evidence of an important functional role of diazotrophs in sustaining coral productivity when alternative external N sources are scarce.

Chemosynthetic symbionts of marine invertebrate animals are capable of nitrogen fixation

Chemosynthetic symbioses are partnerships between invertebrate animals and chemosynthetic bacteria. The latter are the primary producers, providing most of the organic carbon needed for the animal hosts nutrition. We sequenced genomes of the chemosynthetic symbionts from the lucinid bivalve Loripes lucinalis and the stilbonematid nematode Laxus oneistus. The symbionts of both host species encoded nitrogen fixation genes. This is remarkable as no marine chemosynthetic symbiont was previously known to be capable of nitrogen fixation. We detected nitrogenase expression by the symbionts of lucinid clams at the transcriptomic and proteomic level. Mean stable nitrogen isotope values of Loripes lucinalis were within the range expected for fixed atmospheric nitrogen, further suggesting active nitrogen fixation by the symbionts. The ability to fix nitrogen may be widespread among chemosynthetic symbioses in oligotrophic habitats, where nitrogen availability often limits primary productivity.

Microbial dinitrogen fixation in coral holobionts exposed to thermal stress and bleaching.

Coral holobionts (i.e., coral-algal-prokaryote symbioses) exhibit dissimilar thermal sensitivities that may determine which coral species will adapt to global warming. Nonetheless, studies simultaneously investigating the effects of warming on all holobiont members are lacking. Here we show that exposure to increased temperature affects key physiological traits of all members (herein: animal host, zooxanthellae and diazotrophs) of both Stylophora pistillata and Acropora hemprichii during and after thermal stress. S. pistillata experienced severe loss of zooxanthellae (i.e., bleaching) with no net photosynthesis at the end of the experiment. Conversely, A. hemprichii was more resilient to thermal stress. Exposure to increased temperature (+ 6°C) resulted in a drastic increase in daylight dinitrogen (N2 ) fixation, particularly in A. hemprichii (threefold compared with controls). After the temperature was reduced again to in situ levels, diazotrophs exhibited a reversed diel pattern of activity, with increased N2 fixation rates recorded only in the dark, particularly in bleached S. pistillata (twofold compared to controls). Concurrently, both animal hosts, but particularly bleached S. pistillata, reduced both organic matter release and heterotrophic feeding on picoplankton. Our findings indicate that physiological plasticity by coral-associated diazotrophs may play an important role in determining the response of coral holobionts to ocean warming.

37 Years later: revisiting a Red Sea long-term monitoring site

Biodiversity and species abundance in coral reef ecosystems are controlled by structural complexity (Graham and Nash 2013), which is being impacted by reduced net reef framework accretion resulting from anthropogenic stressors (Kennedy et al. 2013). However, evidence verifying changes in benthic reef communities via long-term visual monitoring is rare. In 2013, during an expedition to the northern Red Sea, we revisited a permanent reef quadrat (Fig. 1a, b) located on a fringing reef near Aqaba (Jordan), which was established in 1976 as one of the earliest long-term reef monitoring sites (Mergner and Schuhmacher 1981). High-resolution, sectional photographs were combined to generate a current overview of the benthic community in the entire quadrat (Fig. 1a; Electronic Supplementary Materials, ESM, 1) for a comparison to the initial record (Fig. 1b; ESM 2). The majority of large branching (i.e., Pocilloporidae and Acroporidae) and massive (i.e., Poritidae and Faviidae) hermatypic coral colonies disappeared (Fig. 1b) and were only partially replaced by new ones (ESM 1). Although some massive corals grew noticeably, colony growth in the few persisting branching corals was insubstantial. Overall, hermatypic coral cover declined by ~10 %, and ahermatypic cover (mostly Xeniidae) increased by ~15 %. These changes were accompanied by a conspicuous increase in sand area (~10 %) and substantial decrease in bare reef framework (~20 %), suggesting major structural habitat loss with implications for net reef accretion and associated biodiversity.

Contrasting seasonal responses in dinitrogen fixation between shallow and deep-water colonies of the model coral Stylophora pistillata in the northern Red Sea

Tropical corals are often associated with dinitrogen (N2)-fixing bacteria (diazotrophs), and seasonal changes in key environmental parameters, such as dissolved inorganic nitrogen (DIN) availability and seawater temperature, are known to affect N2 fixation in coral-microbial holobionts. Despite, then, such potential for seasonal and depth-related changes in N2 fixation in reef corals, such variation has not yet been investigated. Therefore, this study quantified seasonal (winter vs. summer) N2 fixation rates associated with the reef-building coral Stylophora pistillata collected from depths of 5, 10 and 20 m in the northern Gulf of Aqaba (Red Sea). Findings revealed that corals from all depths exhibited the highest N2 fixation rates during the oligotrophic summer season, when up to 11% of their photo-metabolic nitrogen demand (CPND) could be met by N2 fixation. While N2 fixation remained seasonally stable for deep corals (20 m), it significantly decreased for the shallow corals (5 and 10 m) during the DIN-enriched winter season, accounting for less than 2% of the corals’ CPND. This contrasting seasonal response in N2 fixation across corals of different depths could be driven by 1) release rates of coral-derived organic matter, 2) the community composition of the associated diazotrophs, and/or 3) nutrient acquisition by the Symbiodinium community.

Ocean Acidification and Related Indicators

Ocean acidification is one of the main consequences of global climate change. It is caused by the increasing input of atmospheric CO2 in the world ocean, which in turn is affecting the marine carbonate system and resulting by now in a measurable decline in seawater pH. Thus, several key water quality parameters (alkalinity, partial pressure of CO2, concentration of dissolved inorganic carbon – DIC, and the seawater pH) serve as environmental indicators for ocean acidification. In addition, many pelagic and benthic marine organisms, particularly those that are calcifying, negatively or positively respond to acidification so that their physiological parameters (calcification, photosynthesis, growth) may also act as indicators of this phenomenon. On the ecosystem level, potential environmental indicators for acidification can be found in the sedimentary record (mineralogy, crystallography), in the benthic community (relative abundance of calcifying versus non-calcifying organisms, rugosity), or in the overall production, cementation, and erosion of inorganic carbon.

Author Correction: Chemosynthetic symbionts of marine invertebrate animals are capable of nitrogen fixation

In this Article, the completeness and number of contigs for draft genomes from two individuals of Laxus oneistus are incorrect in the main text, although the correct information is included in Table 1. The original and corrected versions of the relevant sentence are shown in the correction notice.