The fate of nitrogen in the Orbulina universa foraminifera‐symbiont system determined by nitrogen isotope analyses of shell‐bound organic matter

Abstract

To trace the flow of nitrogen through the foraminifera-symbiont system, juvenile specimens of the symbiontbearing planktonic foraminifera, Orbulina universa were collected by SCUBA divers off the coast of Santa Catalina Island, California, and grown in filtered seawater solutions spiked with 15 N-labeled nitrate. Our work isolated each pathway of this symbiotic system to determine the amount of nitrogen translocated to the foraminifera from its endosymbionts and its captured diet. Our model results show that when the nitrate uptake by the symbionts is at a maximum, between 50 and 57% of the foraminiferal nitrogen was translocated from the symbionts and the remainder was derived from the captured diet. In nitrate-deficient environments, when the symbiont nitrate uptake was at a minimum, ϳ90-100% of the nitrogen was transferred to the foraminifer by the symbionts from the recycled nitrogen (NH ) pool. In nitrate-deficient conditions, the primary role of the captured diet may be to provide the system with recycled nitrogen (NH ) is a more important source of nitrogen to the symbionts and the foraminifera than nitrate; ϩ 4 therefore, the ␦ 15 N values of the foraminifera may not reflect the isotopic composition of the surface-water nutrients. Understanding the nitrogen flow within modern foraminifera-symbiont associations is also important to ancient marine systems, because symbiont-bearing foraminifera are ubiquitous in the fossil record. This study shows that analysis of individual, symbiont-bearing foraminifera species is a necessary first step toward the development of more reliable use of nitrogen isotopes for paleoceanographic reconstructions.

The acquisition of phototrophy: adaptive strategies of hosting endosymbionts and organelles

“…These data suggest that feeding may be more important for phosphorus acquisition under nitratelimited conditions (Uhle et al 1999). The role of AcPh and feeding in nutrient acquisition by foraminifera likely varies depending upon environmental conditions (e.g.…”

“…AcPh leads to enhanced growth efficiency (Skovgaard 1998), provides access to oxygen (Finlay et al 1996;Esteban et al 2009) or nitrogenous compounds (Uhle et al 1999;Grzymski et al 2002) in limiting environments, provides essential nutrients (Wang and Douglas 1999), and in a few cases, acts as the major nutritional source (Muscatine et al 1981;Mujer et al 1996;Johnson and Stoecker 2005 Muscatine andLenhoff 1963, 1965;Cernichiari et al 1969; c ter Kuile et al 1987, Caron et al 1995, Uhle et al 1999d Muscatine and Cernichiari 1969, Muscatine et al 1981, Titlyanov and Titlyanova 2002 A.…”

“…The amount of carbon fixed by O. universa cells can exceed daily carbon requirements for the host-endosymbiont consortium, and it has been suggested that excess excreted carbon may help to attract their zooplankton prey (Lombard et al 2009). Symbionts in O. universa appear to provide their hosts with >50 of their nitrogen requirements in nitrate replete conditions, the remainder of which is derived from feeding (Uhle et al 1999). In nitrogen-deficient environments, symbionts provide O.…”

“…universa with >90% of its nitrogen requirements from the combined recycled pool (NH 4 + ) (Uhle et al 1999). These data suggest that feeding may be more important for phosphorus acquisition under nitratelimited conditions (Uhle et al 1999).…”

Geochemical investigation of gametogenic calcite addition in the planktonic foraminifera Orbulina universa

“…Laboratory and field studies with modern/living foraminifera demonstrate that shell δ 18 O and δ 13 C are controlled by a variety of environmental and ecological parameters such as the carbon and oxygen isotopic composition of seawater, temperature, pH, seasonal and depth habitat preferences and a variety of other biologically-related processes such as symbiont photosynthesis, respiration and food geochemistry (Bemis et al, 1998;Bemis et al, 2000;Bijma and Hemleben, 1994;Bijma et al, 1999;Sautter and Thunell, 1991;Spero, 1992;Spero et al, 1997;Spero and Lea, 1993;Spero and Lea, 1996;Uhle et al, 1999). Constraining sources of intraspecific isotope variability and quantifying isotopic disequilibria among different species is an essential element in accurate reconstructions of past water column hydrography and climatic conditions.…”