Investigating the effect of ballasting by CaCO₃ in Emiliania huxleyi, II: Decomposition of particulate organic matter

Abstract

The quantitative relationship between organic carbon and mineral contents of particles sinking below 1800 m in the ocean indicates that organisms with mineral shells such as coccolithophores are of special importance for transporting carbon into the deep sea. Several hypotheses about the mechanism behind this relationship between minerals and organic matter have been raised, such as mineral protection of organic matter or enhanced sinking rates through ballast addition. We examined organic matter decomposition of calcifying and non-calcifying Emiliania huxleyi cultures in an experiment that allowed aggregation and settling in rotating tanks. Biogenic components such as particulate carbon, particulate nitrogen, particulate volume, pigments, transparent exopolymer particles (TEP), and particulate amino acids in suspended particles and aggregates were followed over a period of 30 d. The overall pattern of decrease in organic matter, the amount of recalcitrant organic matter left after 30 d, and the compositional changes within particulate organic matter indicated that cells without a shell are more subject to loss than calcified cells. It is suggested that biogenic calcite helps in the preservation of particulate organic matter (POM) by offering structural support for organic molecules. Over the course of the experiment, half the particulate organic carbon in both calcifying and non-calcifying cultures was partitioned into aggregates and remained so until the end of the experiment. The partial protection of particulate organic matter from solubilization by biominerals and by aggregation that was observed in our experiment may help explain the robustness of the relationship between organic and mineral matter fluxes in the deep ocean.

Introduction

Recent findings suggest that the ratio of minerals, i.e. opal (biogenic silica), calcium carbonate, and quartz, to organic carbon (Min.:Corg) provides a means of understanding export fluxes of organic matter (OM) to the deep ocean (Armstrong et al., 2002; François et al., 2002; Klaas and Archer, 2002). This is based on the analysis of field data showing that the Min:Corg ratio in particulate matter is generally constant below a depth of 1800 m. There are several mechanisms that might cause such a relationship (Hedges and Keil, 1995; Armstrong et al., 2002; Klaas and Archer, 2002). First, organic compounds may be physically protected against microbial degradation by their association with minerals. In addition, OM may glue particles together, forming aggregates; if the particulate organic carbon content becomes too low, particles may disintegrate, removing both POC and minerals from observed fluxes. Or, the settling velocity of particles may increase when associated with more dense mineral material, leading to a faster export of the ballasted OM (Smayda, 1970; McCave, 1975; Ittekkot and Haake, 1990). Whereas the role of minerals in the preservation of OM has been studied extensively in marine sediments (Suess, 1973; Hedges and Keil, 1995; Mayer, 2004) and in soils (see review in Baldock and Skjemstad, 2000), only little is known about the effect of biologically produced minerals on the decomposition rates of settling OM during its transit through the water column. OM in seawater becomes associated with minerals through adsorption onto mineral surfaces, aggregation with clay sized particles or biologically by growth of cells that produce an outer mineral shell (e.g., the opal frustules of diatoms and radiolaria or calcium carbonate shells of foraminifera, pteropods and coccolithophores). Comparing the carrying capacity of different minerals, i.e. the organic carbon fraction associated with the mineral, Klaas and Archer (2002) showed that CaCO₃ and lithogenic material are more efficient than opal in the downward transport of organic carbon. The special role of CaCO₃ in chemical and physical protection of OM in soils has been summarized in Baldock and Skjemstad (2000). It is suggested that Ca²⁺ cations aid in the preservation of OM by the formation of Ca-organic linkages (Duchaufour, 1976). These linkages can alter the structure of organic macromolecules and the orientation of functional groups, with likely implications for the efficiency of enzymatic attack (Oades, 1988). Stabilization of OM by CaCO₃ during export to the deeper ocean will have large implications for understanding the ocean's capacity to store CO₂ and therefore needs to be included in numerical modeling that aims to quantify the marine carbon cycle. Moreover, since recent investigations have shown a decrease in biogenic calcification with ocean acidification (Riebesell et al., 1993; Delille et al., 2005), understanding the relationship between calcite and OM preservation will also be important to predict future changes in OM decomposition.

To investigate the effect of biogenic CaCO₃ on the preservation of and ballasting of OM, we compared the formation and settling velocities of aggregates (Engel et al., 2009) as well as the decomposition of particulate organic matter (POM) during laboratory incubations of a non-calcifying and a calcifying strain of the marine coccolithophore Emiliania huxleyi. Here, we report the changes in the chemistry of dissolved and particulate components during microbial decomposition and discuss the role of calcification for the preservation of OM. E. huxleyi is a widespread, bloom-forming coccolithophore in the ocean that participates in the export of calcite and organic matter to the deep sea. Since aggregates rather than single cells are the most likely carriers of particle flux in the deep ocean (Fowler and Knauer, 1986), we allowed cells to aggregate prior to and during the experiment and analyzed suspended and aggregated particles separately.