The microbial impact on Fe&S cycling at oxic-anoxic interfaces: a single-cell view

Abstract

At oxic-anoxic interfaces, competing biotic and abiotic reactions drive the rapid turnover of elements involved in biogeochemical cycles. As a result of the complexity of interactions between biological and chemical processes, the contribution of microorganisms to biogeochemical element cycling is still poorly constrained. Understanding the role of microorganisms at oxic-anoxic interfaces is important because they link the carbon cycle to other element cycles via carbon fixation and degradation using inorganic electron donors and acceptors, respectively. The aim of this thesis was to elucidate the microbial impact on the cycling of two of these elements a Fe and S a at oxic-anoxic interfaces. In combination with conventional analytical techniques in biogeochemistry, state-of-the-art single-cell instruments were used to investigate biogeochemical cycling on the level of single microbial cells, enabling novel insights into extremely rapid, even cryptic, microbial processes with transient intermediates. This approach was first applied to laboratory cultures to investigate sulfur metabolism in large, colorless sulfur bacteria under controlled laboratory conditions. Confocal Raman spectroscopy of living Beggiatoa sp. cells revealed that the chemical nature of stored zero valent sulfur reflects the physiological state of the bacteria. Zero-valent sulfur was present in the form of both cyclooctasulfur rings (S8) and inorganic polysulfide chains (Sx2-), the latter appearing to serve as intermediates during both the accumulation and the breakdown of sulfur storage globules. In the environment, the factors controlling the speciation of iron and sulfur were investigated in Lake Cadagno, a stratified lake in Switzerland. Despite low, 1-2 I molA l-1 iron concentrations, significant rates of microbially-driven iron turnover were measured within the chemocline. The oxidation of iron by anoxygenic phototrophic bacteria could potentially contribute to up to 10% of primary production in this anoxic zone. The coupling of iron oxidation to iron reduction by heterotrophic bacteria generated a closed, a cryptica iron cycle. These results suggest that rapid microbial redox cycling of iron may thus far have been overlooked in shallow, low-iron redoxclines which are globally widespread. Although sulfur cycling in Lake Cadagno has already been extensively studied, our high resolution time profiles combined with single-cell analyses revealed surprising insights into the metabolism of the sulfide oxidizing bacteria there. Anoxygenic phototrophic purple sulfur bacteria were actually highly active in the dark and respired sulfur aerobically under both light and dark conditions. To bridge spatially separated gradients of electron donors and acceptors, these bacteria utilized a novel mechanism of storage and transport that is not yet fully understood. Because we could not completely close the sulfur budget in the Lake Cadagno chemocline, the existence of yet-unknown sulfide oxidation mechanisms could not be excluded, presenting exciting possibilities for future research. In the course of these studies, the challenge of linking microbial identity with function using non-fluorescent-based, single-cell instruments led to the development of a new method (silver-DISH) for the targeted identification of environmental bacteria with nanometer secondary ion mass spectrometry (nanoSIMS), scanning electron microscopy energy-dispersive X-ray spectroscopy (SEM-EDS), and confocal Raman spectroscopy. This technique may be extremely useful for future environmental microbiology studies, especially for correlative imaging. Microorganisms evidently play an important role in biogeochemical cycling at oxic-anoxic interfaces in spite of competition with spontaneous chemical reactions. Overall, the results presented in this thesis may help to constrain and quantify the impact of microbes on carbon fixation and degradation processes in such environments.