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

Abstract

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.

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

“…High rates of N 2 fixation have been measured in reefs sediments, rocks and dead coral skeletons, as well as related to several benthic (cyanobacterial mats, macroalgae, sponges, corals) and pelagic (unicellular cyanobacteria, Trichodesmium species) organisms (reviewed by Davey et al, 2008;O'Neil and Capone, 2008;Cardini et al, 2014). Rates of N 2 fixation can either be expressed indirectly as ethylene (C 2 H 4 ) produced from acetylene (C 2 H 2 ) using the acetylene reduction assay (ARA), or directly as the amount of nitrogen assimilated using 15 N 2 tracer experiments (see Box 1).…”

“…The primary limitation to estimate reef-wide N 2 fixation is its spatial and temporal variability. N 2 fixation largely varies depending on the diazotroph community composition, itself varying within and between reefs, or according to seasons and nutrient concentrations in seawater (O'Neil and Capone, 2008;Cardini et al, 2014Cardini et al, , 2016a.…”

“…diazotrophs have colonized a wide range of habitats, such as the water column (Riemann et al, 2010;Turk-Kubo et al, 2015), the sediments and dead coral surfaces (Davey et al, 2008;Bednarz et al, 2015b), the algal turfs (Rohwer et al, 2001;Haan et al, 2014;Rix et al, 2015), microbial mats and seagrass meadows (Rohwer et al, 2001(Rohwer et al, , 2002Charpy et al, 2012;Cardini et al, 2014), as well as sponge and coral tissue (Rohwer et al, 2002;Lema et al, 2014a,b). Still, their contribution to nitrogen cycling in the coral reef ecosystem as a whole, their spatial-temporal variability, level of activity and dependence on environmental factors, are poorly understood.…”

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

“…Additionally, corals have evolved strategies to exploit any source of inorganic N [18], enabling them to survive in oligotrophic tropical waters where N is the most limiting nutrient to primary productivity [19,20]. However, the abundance of symbiotic Symbiodinium within the coral host is limited by N concentrations [4,21].…”

High sedimentary oxygen consumption indicates that sewage input from small islands drives benthic community shifts on overfished reefs

“…Once established, cyanobacterial mats release up to 79% of the total reef community's dissolved organic carbon (DOC) (Brocke et al 2015b), thus promoting further bacterial proliferation, which can indirectly result in declining reef health through mechanisms such as increasing coral disease prevalence (Kline et al 2006). Furthermore, cyanobacteria reduce coral recruitment (Kuffner & Paul 2004), supporting the observed juvenile coral densities, and they exhibit some of the highest reef nitrogen fixation rates (Cardini et al 2014), which may further favour reef degradation.…”