The cycling of arsenic in the marine photosynthetic plants and algae was examined by analysing total arsenic concentrations and arsenic species in selected marine photosynthetic organisms from the south-east coast, NSW, Australia. A range of elements required for metabolism in photosynthetic organisms were also analysed to determine if any relationship between these elements and arsenic concentrations occurred. Organisms were selected from salt marsh and mangrove ecosystems, marine inter-tidal and estuarine environments, and two species of marine phytoplankton cultured, to represent the different marine environments that primary producers inhabit. Organisms selected were compared to species within their own environment and then a comparison made between the varying ecosystems. In the salt marsh and mangrove ecosystems, the leaves of four species, the mangrove Avicennia marina, the samphire Sarcocornia quinqueflora, the seablight Suaeda australis, and the seagrass Posidonia australis were sampled from three locations from the south-east coast of NSW using nested sampling. Mean total arsenic concentrations (mean ? sd) dry mass for all locations were A. marina (0.38 ? 0.18 ig g-1 to 1.2 ? 0.7 ig g-1),S. quinqueflora (0.13 ? 0.06 ig g-1 to 0.46 ? 0.22 ig g-1),S. australis (0.03 ? 0.06 ig g-1 to 0.05 ? 0.03 ig g-1)and P. australis (0.34 ? 0.10 ig g-1 to 0.65 ? 0.26 ig g-1). Arsenic concentrations were significantly different between species and locations but were consistently low compared to marine macroalgae species. Significant relationships between As and Fe concentrations for A. marina, S. quinqueflora and P. australis and negative relationship between As and Zn concentrations for S. quinqueflora could partially explain arsenic concentrations in these species. No relationship between As and P concentrations were found in this study. All terrestrial species contained predominantly inorganic arsenic in the water extractable and residue fractions with minor concentrations of DMA in the water-soluble fraction. P. australis also contained dimethylated glycerol and phosphate arsenoriboses. The presence of arsenobetaine, arsenocholine and trimethylated glycerol arsonioribose is most likely due to the presence of epiphytes on fronds on P. australis. In contrast, macroalgae contained higher total arsenic concentrations compared to marine terrestrial angiosperms. Total arsenic concentrations also varied between classes of algae: red macroalgae 4.3 ig g-1 to 24.7 ig g-1,green macroalgae 8.0 ig g-1 to 11.0 ig g-1 and blue green algae 10.4 ig g-1 and 18.4 ig g-1. No significant relations were found between As concentrations and concentrations of Fe, Co, Cu, Mn, Mo, Mg, P and Zn concentrations, elements that are required by macroalgae for photosynthesis and growth. Distinct differences between algal classes were found for the proportion of arsenic species present in the lipid and water-soluble fractions, with green algae having a higher proportion of As in lipids than red or estuarine algae. Acid hydrolysis of the lipid extract revealed DMA, glycerol arsenoribose and TMA based arsenolipids. Within water-soluble extracts, red and blue-green algae contained a greater proportion of arsenic as inorganic and simple methylated arsenic species compared to green algae, which contained predominantly glycerol arsenoribose. Arsenobetaine, arsenocholine and tetramethylarsonium was also present in water-soluble extracts but is not normally identified with macroalgae and is again likely due to the presence of attached epiphytes. Residue extracts contained predominantly inorganic arsenic, most likely associated with insoluble constituents of the cell. Mean arsenic concentrations in the green microalgae Dunaliella tertiolecta were 13.3 ig g-1 to 14.5 ig g-1,which is similar to arsenic concentrations found in green macroalgae in this study. Diatom Phaeodactylum tricornutum arsenic concentrations were 1.62 ig g-1 to 2.08 ig g-1. Varying the orthophosphate concentrations had little effect on arsenic uptake of microalgae. D. tertiolecta and P. tricornutum metabolised arsenic, forming simple methylated arsenic species and arsenic riboses. The ratio of phosphate to glycerol arsenoriboses was higher than that normally found in green macroalgae. The hydrolysed lipid fraction contained DMA arsenolipid (16-96%) with minor proportions of phosphate arsenoribose (4-23%). D. tertiolecta at f/10 phosphate concentration, however, contained glycerol arsenoribose and another arsenic lipid with similar retention as TMAO as well as DMA. The similarities between arsenic species in the water-soluble hydrolysed lipids and water-soluble extracts, especially for P. tricornutum, suggests that cells readily bind arsenic within lipids, either for membrane structure or storage, releasing arsenic species into the cytosol as degradation of lipids occurs. Inorganic arsenic was sequestered into insoluble components of the cell. Arsenic species present in D. tertiolecta at lower phosphate concentrations (f/10) were different to other phosphate concentrations (f/2,f/5),and require further investigation to determine whether this is a species-specific response as a result of phosphate deficiency. Although there are similarities in arsenic concentrations and arsenic species in marine photosynthetic organisms, it is evident that response to environmental concentrations of arsenic in uncontaminated environments is dependent on the mode of transfer from the environment, the influence of other elements in arsenic uptake and the ability of the organism to metabolise and sequester inorganic arsenic within the cell. It is not scientifically sound to generalise on arsenic metabolism in 'marine plants' when species and the ecosystem in which they exist may influence the transformation of arsenic in higher marine organisms. There is no evidence to suggest that angiosperms produce AB as arsenic is mostly present as inorganic As, with little or no arsenic present in the lipids. However, marine macro- and microalgae both contain lipids with arsenic moieties that may be precursors for AB transformation. Specifically, the presence of TMA and dimethylated arsenoribose based arsenolipids both can transform to AB via intermediates previously identified in marine organisms. Further identification and characterization of As containing lipids is required.
|Date of Award
|Bill Maher (Supervisor) & Ian MCNAUGHT (Supervisor)