Importance of coccolithophore‐associated organic biopolymers for fractionating particle‐reactive radionuclides (²³⁴Th, ²³³Pa, ²¹⁰Pb, ²¹⁰Po, and ⁷Be) in the ocean

Abstract

Laboratory incubation experiments using the coccolithophore Emiliania huxleyi were conducted in the presence of 234Th, 233Pa, 210Pb, 210Po, and 7Be to differentiate radionuclide uptake to the CaCO3 coccosphere from coccolithophore‐associated biopolymers. The coccosphere (biogenic calcite exterior and its associated biopolymers), extracellular (nonattached and attached exopolymeric substances), and intracellular (sodium‐dodecyl‐sulfate extractable and Fe‐Mn‐associated metabolites) fractions were obtained by sequentially extraction after E. huxleyi reached its stationary growth phase. Radionuclide partitioning and the composition of different organic compound classes, including proteins, total carbohydrates (TCHO), and uronic acids (URA), were assessed. 210Po was closely associated with the more hydrophobic biopolymers (high protein/TCHO ratio, e.g., in attached exopolymeric substances), while 234Th and 233Pa showed similar partitioning behavior with most activity being distributed in URA‐enriched, nonattached exopolymeric substances and intracellular biopolymers. 234Th and 233Pa were nearly undetectable in the coccosphere, with a minor abundance of organic components in the associated biopolymers. These findings provide solid evidence that biogenic calcite is not the actual main carrier phase for Th and Pa isotopes in the ocean. In contrast, both 210Pb and 7Be were found to be mostly concentrated in the CaCO3 coccosphere, likely substituting for Ca2+ during coccolith formation. Our results demonstrate that even small cells (E. huxleyi) can play an important role in the scavenging and fractionation of radionuclides. Furthermore, the distinct partitioning behavior of radionuclides in diatoms (previous studies) and coccolithophores (present study) explains the difference in the scavenging of radionuclides between diatom‐ and coccolithophore‐dominated marine environments.

Incorporation of Hydroxamate Siderophore and Associated Fe Into Marine Particles in Natural Seawater

“…Considering our incubation medium only included the bacteria, the incorporation of the particulate siderophore compounds could have become cumulatively more important in a more complex natural oceanic system that involves the interplay between bacteria, phytoplankton, zooplankton, and mineral particles. Phytoplankton are well-known to excrete a high abundance of expolymeric substances (EPS), enriched in proteins and polysaccharides, to the surrounding seawaters during their growth (Hassler et al, 2011;Quigg et al, 2016;Lin et al, 2017Lin et al, , 2020. Particle aggregation can occur by hydrostatic interaction of EPS containing a variety of negatively charged functional groups, resulting in hydrogen and metal ion bonding, as well as hydrophobic interactions that can lead to physicochemical cross linking (e.g., resulting in the protein/carbohydrate ratio being predictive for particle aggregation; Santschi et al, 2020).…”

Molecular Level Characterization of Diatom and Coccolithophore-Associated Biopolymers That Are Binding 210Pb and 210Po in Seawater

“…Although most of these tracer applications are generally resting on inferences from correlations of isotopic ratios with bulk particle properties, experimental evidence reveals organic compound-specific scavenging and partitioning for different radionuclides, either in particulate or in colloidal phases (Hayes et al, 2015a,b;Lam et al, 2015;Lin et al, 2015). Furthermore, while previous focus was on inorganic matter as the main binding agents (e.g., opal, carbonate, and lithogenic; Chase et al, 2002;Guo et al, 2002;Roy-Barman et al, 2009;Lin et al, 2014), more recent experimental studies reveal the role of specific organic matter compounds in the scavenging of different radionuclides in marine environments (Roberts et al, 2009;Xu et al, 2011a;Chuang et al, 2014Chuang et al, , 2015aLin et al, 2017).…”

“…In the global oceans, diatom and coccolithophores serve as the most important contributors to global oceanic primary production and to carbon flux (Nelson et al, 1995;Armbrust, 2009), whereby in-situ production and excretion of biogenic materials account for the majority of natural organic matter in the water column. During phytoplankton growth, secretion of fresh biopolymers (Chin et al, 1998;Santschi et al, 1998;Quigg et al, 2016) was shown to provide the strongest binding agents for different radionuclides compared with the naked diatom frustule (Chuang et al, 2014) or coccosphere (Lin et al, 2017(Lin et al, , 2020. Furthermore, particle-reactive radionuclides can partition differently between diatom-and coccolithophore-predominated systems or among different biopolymer fractions of diatom or coccolithophore cells, which were attributed to different organic composition between different biopolymer fractions, and thus, to different affinities of the radionuclides to these fractions (Chuang et al, 2015b;Lin et al, 2017).…”

“…During phytoplankton growth, secretion of fresh biopolymers (Chin et al, 1998;Santschi et al, 1998;Quigg et al, 2016) was shown to provide the strongest binding agents for different radionuclides compared with the naked diatom frustule (Chuang et al, 2014) or coccosphere (Lin et al, 2017(Lin et al, , 2020. Furthermore, particle-reactive radionuclides can partition differently between diatom-and coccolithophore-predominated systems or among different biopolymer fractions of diatom or coccolithophore cells, which were attributed to different organic composition between different biopolymer fractions, and thus, to different affinities of the radionuclides to these fractions (Chuang et al, 2015b;Lin et al, 2017). However, the chemical composition of radionuclide-carrying biopolymer compounds derived from diatoms and coccolithophores are typically only quantified and characterized in terms of few groups of organic components, such as proteins, uronic acids, and carbohydrates.…”

“…However, the chemical composition of radionuclide-carrying biopolymer compounds derived from diatoms and coccolithophores are typically only quantified and characterized in terms of few groups of organic components, such as proteins, uronic acids, and carbohydrates. To fill this knowledge gap, the diatom P. tricornutum and coccolithophore Emiliania huxleyi were incubated for later separation of different biopolymer fractions, including extracellular fractions (non-attached and attached exopolymeric substances), frustule/coccosphere-associated biopolymers and intracellular biopolymers from cell lysis (Chuang et al, 2015b;Lin et al, 2017). In order to characterize the diatom/coccolithophore-derived biopolymers, specific organic compounds likely responsible for the scavenging and partitioning of 210 Pb and 210 Po in the water column, and examine their differences at the molecular level, Electrospray Ionization Fourier-Transform Ion Cyclotron Resonance Mass Spectrometry (ESI-FTICRMS) (Xu et al, 2020) was applied in the present study.…”