ABSTRACT
The oxygen minimum zone (OMZ) of the Eastern Tropical South Pacific (ETSP) is 1 of the 3 major regions in the world where oceanic nitrogen is lost in the pelagic realm. The recent identification of anammox, instead of denitrification, as the likely prevalent pathway for nitrogen loss in this OMZ raises strong questions about our understanding of nitrogen cycling and organic matter remineralization in these waters. Without detectable denitrification, it is unclear how NH(4)(+) is remineralized from organic matter and sustains anammox or how secondary NO(2)(-) maxima arise within the OMZ. Here we show that in the ETSP-OMZ, anammox obtains 67% or more of NO(2)(-) from nitrate reduction, and 33% or less from aerobic ammonia oxidation, based on stable-isotope pairing experiments corroborated by functional gene expression analyses. Dissimilatory nitrate reduction to ammonium was detected in an open-ocean setting. It occurred throughout the OMZ and could satisfy a substantial part of the NH(4)(+) requirement for anammox. The remaining NH(4)(+) came from remineralization via nitrate reduction and probably from microaerobic respiration. Altogether, deep-sea NO(3)(-) accounted for only approximately 50% of the nitrogen loss in the ETSP, rather than 100% as commonly assumed. Because oceanic OMZs seem to be expanding because of global climate change, it is increasingly imperative to incorporate the correct nitrogen-loss pathways in global biogeochemical models to predict more accurately how the nitrogen cycle in our future ocean may respond.
Subject(s)
Nitrogen/metabolism , Oxygen/metabolism , Bacteria/genetics , Gene Expression Regulation, Bacterial , Nitric Oxide/metabolism , Nitrites/metabolism , Oxidation-Reduction , Peru , Quaternary Ammonium Compounds/metabolismABSTRACT
Among prokaryotes, the large vacuolated marine sulphur bacteria are unique in their ability to store, transport and metabolize significant quantities of sulphur, nitrogen, phosphorus and carbon compounds. In this study, unresolved questions of metabolism, storage management and behaviour were addressed in laboratory experiments with Thioploca species collected on the continental shelf off Chile. The Thioploca cells had an aerobic metabolism with a potential oxygen uptake rate of 1760 micromol O2 per dm(3) biovolume per h, equivalent to 4.4 nmol O2 per min per mg protein. When high ambient sulphide concentrations (approximately 200 microM) were present, a sulphide uptake of 6220+/-2230 micromol H2S per dm(3) per h, (mean+/-s.e.m., n=4) was measured. This sulphide uptake rate was six times higher than the oxidation rate of elemental sulphur by oxygen or nitrate, thus indicating a rapid sulphur accumulation by Thioploca. Thioploca reduce nitrate to ammonium and we found that dinitrogen was not produced, neither through denitrification nor through anammox activity. Unexpectedly, polyphosphate storage was not detectable by microautoradiography in physiological assays or by staining and microscopy. Carbon dioxide fixation increased when nitrate and nitrite were externally available and when organic carbon was added to incubations. Sulphide addition did not increase carbon dioxide fixation, indicating that Thioploca use excess of sulphide to rapidly accumulate sulphur rather than to accelerate growth. This is interpreted as an adaptation to infrequent high sulphate reduction rates in the seabed. The physiology and behaviour of Thioploca are summarized and the adaptations to an environment, dominated by infrequent oxygen availability and periods of high sulphide abundance, are discussed.