The microbial control of phosphorus fluxes in marine sediments

Abstract

This thesis explores how microorganisms affect the release of the key nutrient phosphorus from marine sediments. A detailed understanding of the controls on regeneration of phosphorus from sediments is important because phosphorus availability in surface waters can regulate primary productivity. Oxygen depletion can enhance sediment phosphorus release and intensify phosphorus cycling between the sediment and overlying water, thereby sustaining eutrophication in marine systems. In addition, increased phosphorus release can exacerbate anoxic conditions, as the degradation of the subsequent higher flux of organic matter to the sediment places an extra demand on the oxygen supply. At present, many coastal ecosystems are facing the joint effects of hypoxia and eutrophication. As yet, our knowledge of benthic phosphorus cycling is insufficient to quantitatively predict future trends in the coupled cycles of carbon, phosphorus and oxygen in coastal systems and this strongly hampers the development of strategies for remediation and restoration. In this thesis we show that, although redox conditions have a profound impact on the phosphorus release from sediments, bacterial communities in Baltic Sea sediments from contrasting redox conditions show a large overlap. In addition, the bacteria in these carbon-limited sediments express phosphatase enzymes under both oxic and anoxic conditions. The role of phosphatases very likely is to relieve carbon limitation by removing phosphate groups from organic compounds prior to uptake of the remainder of the molecule. By labeling phosphatase-expressing cells, we determined that the phosphatase-expressing bacterial community coarsely reflects the total bacterial community. The expression of phosphatases by carbon-limited microorganisms provides a mechanism that explains the ongoing release of phosphate from anoxic sediments. The release of more phosphate from organic matter than is required by microorganisms can increase pore water phosphate concentrations, which can lead to a higher release of phosphate from the sediment to the overlying water. Because the phosphatase activity was lower in anoxic than in oxic sediments, phosphatase activity by itself cannot explain the higher release of P from anoxic sediments. However, phosphate is more efficiently retained in oxic sediments, for example by adsorption to, or co-precipitation with, iron and by microbial polyphosphate accumulation. We measured – to our knowledge for the first time – C:P ratios of individual sediment microorganisms (by X-Ray MicroAnalysis). Surprisingly, the microorganisms were phosphorus poor in comparison to the Redfield ratio (C:P ratio of approximately 400:1). The relative phosphorus content was the same for microorganisms from oxic and anoxic sediment incubations. The formation of new microbial biomass in sediments thus requires less phosphorus relative to carbon than would be needed for the growth of phosphorus-rich organisms, and less than supplied in incoming organic matter. The measured C:P ratios can explain up to approximately 70% of the enhanced phosphorus release observed in the study area, depending on microbial biomass accumulation. The results from this thesis need to be scaled up from the microbial realm to global cycles with the help of (mathematical) models. Further cooperation between microbiologists and geochemists is necessary to resolve the remaining questions regarding the microbial control of benthic phosphorus cyclin