Widespread occurrence of nitrate storage and denitrification among Foraminifera andGromiida

Abstract

Benthic foraminifers inhabit a wide range of aquatic environments including open marine, brackish, and freshwater environments. Here we show that several different and diverse foraminiferal groups (miliolids, rotaliids, textulariids) and Gromia , another taxon also belonging to Rhizaria, accumulate and respire nitrates through denitrification. The widespread occurrence among distantly related organisms suggests an ancient origin of the trait. The diverse metabolic capacity of these organisms, which enables them to respire with oxygen and nitrate and to sustain respiratory activity even when electron acceptors are absent from the environment, may be one of the reasons for their successful colonization of diverse marine sediment environments. The contribution of eukaryotes to the removal of fixed nitrogen by respiration may equal the importance of bacterial denitrification in ocean sediments.

Survival and life strategy of the foraminiferan Globobulimina turgida through nitrate storage and denitrification

“…Similar intracellular nitrate concentrations (up to 500 mM) have also been observed in white sulphur bacteria belonging to the family Beggiatoaceae (Beggiatoa, Thioploca and Thiomargarita;Fossing et al 1995, McHatton et al 1996, Schulz et al 1999, Sayama 2001), corresponding to 4000-fold higher concentration levels than in the ambient environment. These findings suggest that nitrate accumulation is a universal property of vacuolated, filamentous sulphur bacteria, as well as Foraminifera and Gromiida (Piña-Ochoa et al 2010). High variability was measured in the intracellular nitrate pool within each treatment (Figs.…”

“…Foraminifera were gently cleaned of sediment with a brush and rinsed in nitrate-free ASW. The specimens were then transferred to PCR tubes and analysed for nitrate content using the VCl 3 reduction method (Braman & Hendrix 1989) on a chemiluminescence detector (Model CLD 86, Eco Physics AG) as described by RisgaardPetersen et al (2006) and Høgslund et al (2008), with modification by Piña-Ochoa et al (2010). The analysis was carried out immediately when possible; alternatively, specimens were stored at -20°C until analysis within 1 wk of sampling.…”

“…Jorissen et al 1995, Fontanier et al 2003, Koho et al 2008a, which implies that they have either a fermentative or a respiratory metabolism based on electron acceptors other than oxygen. Recently, it has been demonstrated that many benthic foraminiferal species appear to be facultative anaerobes, allowing them to use both oxygen and nitrate for respiration (Risgaard-Petersen et al 2006, Høgslund et al 2008, Piña-Ochoa et al 2010. These species seem to respire nitrate through denitrification (i.e.…”

Spring-to-summer changes and regional variability of benthic processes in the western Canadian Arctic

“…The consistent negative effect of foraminiferan biomass on benthic carbon remineralisation in both spring and summer raises questions on the metabolic mechanisms in this group. Recently, Piña-Ochoa et al (2010) have described use of denitrification processes by many foraminiferan species. This could imply the respiration of nitrate rather than oxygen from the water phase, but it is still unclear, whether foraminiferan denitrification is restricted to anaerobic conditions (Høgslund et al 2008;Piña-Ochoa et al 2010).…”

“…Recently, Piña-Ochoa et al (2010) have described use of denitrification processes by many foraminiferan species. This could imply the respiration of nitrate rather than oxygen from the water phase, but it is still unclear, whether foraminiferan denitrification is restricted to anaerobic conditions (Høgslund et al 2008;Piña-Ochoa et al 2010). Depending on the oxygen penetration of sediments, which is generally deeper in greater water depths, foraminifera can be abundant down to more than 5 cm sediment depth (Fontanier et al 2005).…”