Linking Aerobic Archaeal and Bacterial Ammonia Oxidation to Anammox in the Benguella Upwelling System.
Final Report Abstract
About 30-50% of total oceanic nitrogen loss occurs in marine suboxic water columns known as oxygen minimum zones (OMZs), including that associated with the Benguella Upwelling System. In the Benguella OMZ, as well as in the Peruvian OMZ and the Black Sea suboxic water column, we found that marine nitrogen loss was predominantly attributed to anammox instead of the canonical heterotrophic denitrification. In the anammox process, the dinitrogen gas is formed from a combination of NO2- and NH4+, as opposed to the sole NO3 source in denitrification. However, without detectable denitrification in the Benguella OMZ, it was unclear how anammox bacteria obtained their NO2 for N2 production. While previous 15N-incubation experiments indicated that nitrate reduction could have partly provided the required NO2-, we showed in this study that aerobic ammonia oxidation, the first step of nitrification, co-occurred with anammox and also provided the latter with an additional NO2- source. Ammonia monooxygenase gene subunit A (amoA), the functional gene biomarker encoding the key enzyme to the first step of aerobic ammonia oxidation, has been detected in a metagenomic library acquired from the Benguella OMZ. Some of these amoA genes were found to be originating from Crenarchaeota as well as from y-Proteobacteria, suggesting that ammonia oxidation in this OMZ involved representatives from both of these microbial groups. Quantitative real-time PCR (qPCR) assays have been developed for the functional gene biomarkers for various nitrogen cycling processes. As various nitrogen transformations could be occurring simultaneously in marine suboxic environments, these qPCR assays are particularly useful as activity diagnostic tools of such concurrent processes that are difficult to detect with conventional methods otherwise. Consequently, these qPCR assays have been successfully applied in the Black Sea suboxic water column, and showed that crenarchaeal ammonia-oxidizers were the major players in nitrite production in the lower oxic zone, whereas y-proteobacterial ammonia-oxidizers co-occurred with anammox bacteria in the suboxic zone and supplied the latter with an in situ NO2- source. Similarly, the same approach was extended for the detection of other functional gene biomarkers, including those for anammox (nirS), nitrate reduction (narG and napA), denitrification (nirS) and dissimilatory nitrate reduction to ammonium or DNRA (nrfA), on samples from the Peruvian OMZ. It was found in those waters that anammox bacteria obtained their NO2- from nitrate reduction and (micro)aerobic ammonia oxidation, while their NH4+ came from nitrate reduction, DNRA and (micro)aerobic respiration. The expression levels of these functional genes were also quantified, and the activities were further verified via 15N-stable-isotope-pairing experiments. Consistent with the Benguella OMZ, aerobic ammonia oxidation involved both crenarchaea and Proteobacteria in this OMZ. The significant findings of the above-mentioned studies formed an integral part ofa recently published article in the popular science magazine BlOspektrum ("Der Stickstoffkreislauf im Ozean", BlOspektrum June 2009, p368-373).
Publications
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(2007) Linking crenarchaeal and bacterial nitrification to anammox in the Black Sea, Proceedings of the National Academy of Sciences of the USA, 104, 7104-7109
Lam, P., Jensen, M.M. Lavik, G., McGinnis, D.F., Müller, B., Schubert, C.J., Amann, R., Thamdrup, B., and Kuypers, M.M.M.
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(2007). Fosmids of novel marine Planctomycetes from the Namibian and Oregon coast upwelling systems and their cross-comparison with planctomycete genomes, The ISME Journal, 1, 419-435
Woebken, D., Teeling, H., Wecker, P., Dumitriu, A., Kostadinov, I., DeLong, E.F., Amann, R., and Glöckner, F.O.
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(2007). Potential Interactions of Particle-Associated Anammox Bacteria with Bacterial and Archaeal Partners in the Namibian Upwelling,Svstem, Appl. Envir. Microbiol. 73: 4648-4657
Woebken, D., Fuchs, B. M., Kuypers, M. M. M., and Amann, R.
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(2009) Detoxification of sulphidic African shelf waters by blooming chemolithotrophs, Nature, 457, 581-584
Lavik, G., T. Stührmann, V. Brüchert, A. Van der Plas, V. Mohrholz, P. Lam, M. Mußmann, B.M. Fuchs, R. Amann, U. Lass, and M.M.M. Kuypers
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(2009) Revising the nitrogen cycle in the Peruvian oxygen minimum zone, Proceedings of the National Academy of Sciences of the USA, 106, 4752-4757
Lam, P., Jensen, M.M., Lavik, G., van de Vossenberg, J., Schmid, M., Woebken, D., Gutierrez, D., Amann, R., Jetten, M.S.M., and Kuypers, M.M.M.
