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The role of benthic foraminifera in the global N-cylcle
Program coordinator(s): Prof. dr. ir. M. S. M. Jetten
Theme(s): 1
Funding date: 10-jan-07

Abstract
The anaerobic respiration with nitrate as an electron acceptor is generally regarded as a bacterial process. Recently however, we have found that at least three species of benthic foraminifera (unicellular eukaryotes) were able to respire nitrate completely to dinitrogen gas. In addition, these species accumulated and stored high concentrations of nitrate in their cell. This stored nitrate is sufficient to support anaerobic respiration for over a month. Benthic foraminifera are unicellular eukaryotes, which can be abundant in anoxic environments. This suggests that their role in the global N-cycle might be significant. The evolution of foraminiferal taxa that prefer these anoxic conditions accelerated since the Middle Miocene (16 to 12 million years ago). The aim of this project is to investigate the newly discovered foraminiferal nitrate respiration in more depth along the questions: (1) how broadly distributed is the trait to respire nitrate?; (2) how substantial is the contribution of foraminiferal denitrification to the global N-cycle?; (3) how did this anaerobic function evolve; (4) how is it related to the occupation and regulation of infaunal niches?; and (5) can these foraminifera be used as index-fossils for the evolution of infaunal niches, and the related evolution of biogeochemical processes?

This program contains the following projects:
1091: Nitrate respiration by benthic foraminifera
1092: Infaunal benthic foraminifera: ecology, evolution and their role in the evolution of the global N-cycle

Publications
Schmid, M.C., Risgaard-Petersen, N., van de Vossenberg, J., Kuypers, M.M.M., Lavik, G., Petersen, J., Hulth, S., Thamdrup, B., Canfield, D., Dalsgaard, T., Rysgaard, S., Sejr, M.K., Strous, M., Op den Camp H.J.M., & Jetten, M.S.M. (2007). Anaerobic ammonium-oxidizing bacteria in marine environments: widespread occurrence but low diversity. Environ. Microbiol9: 1476-1484.
Darwin Center authors: op den Camp H. J. M., Jetten M. S. M.

Schmid, M.C., Hooper, A.B., Klotz, M.G., Woebken, D. Lam, P., Kuypers, M.M.M., Pommering-Roeser, A., Op den Camp, H.J.M. & Jetten, M.S.M. (2008). Environmental detection of the octaheme cyctochrome c hydroxylamine/hydrazine oxidoreductase genes of aerobic and anaerobic ammonium-oxidizing bacteria. Environmental Microbiology10: 3140-3149.
Darwin Center authors: op den Camp H. J. M., Jetten M. S. M.

Klotz, M.G., Schmid, M.C., Strous, M., Op den Camp, H.J.M., Jetten, M.S.M. & Hooper, A.B. (2008). Evolution of an octaheme cytochrome c protein family that is key to aerobic and anaerobic ammonia oxidation by bacteria. Environmental Microbiology10: 3150-3163.
Darwin Center authors: op den Camp H. J. M., Jetten M. S. M.

Kartal B, van Niftrik L, Rattray J, van de Vossenberg JL, Schmid MC, Sinninghe Damsté JS, Jetten MSM, Strous M. (2008). Candidatus 'Brocadia fulgida': an autofluorescent anaerobic ammonium oxidizing bacterium. FEMS Microbiol Ecol63: 46-55.
Darwin Center authors: Jetten M. S. M., van Niftrik L.A.M.P., Sinninghe Damsté J. S.

Lam, P., Lavik, G., Jensen, M.M., van de Vossenberg, J., Schmid, M., Woebken, D., Gutiérrez, D., Amann, R., Jetten, M.S.M. & Kuypers, M.M.M. (2009). Revising the nitrogen cycle in the Peruvian oxygen minimum zone. PNAS106: 4752-4757.
Darwin Center authors: Jetten M. S. M.

Pavlekovic, M., Schmid, M.C., Schmider-Poignee, N., Spring, S., Pilhofer, M., Gaul, T., Fiandaca, M., Löffler, F.E., Jetten, M.S.M., Schleifer, K.H. & Lee, N.M. (2009). Optimization of three FISH procedures for in situ detection of anaerobic ammonium oxidizing bacteria in biological wastewater treatment. J Microbiol Methods78: 119-126.
Darwin Center authors: Jetten M. S. M.

Piña-Ochoa E., Koho K.A., Geslin E., Risgaard-Petersen N. (2010). Survival and life strategy of the foraminiferan Globobulimina turgida through nitrate storage and denitrification. Marine Ecology Progress Series417: 39-49.
Darwin Center authors: Koho K. A.

Gooday A.J., Da Silva A.A., Koho K.A., Lecroq B., Pearce R.B. (2010). The 'mica sandwich'; a remarkable new genus of foraminifera (Protista, Rhizaria) from the Nazaré Canyon (Portuguese margin, NE Atlantic). Micropaleontology56: 345-357.
Darwin Center authors: Koho K. A.

Koho K.A., Piña-Ochoa E., Geslin E. and Risgaard-Petersen N. (2011). Vertical migration, nitrate uptake and denitrification: survival mechanisms of foraminifers (Globobulimina turgida) in low oxygen conditions. FEMS Microbiol Ecol75: 273-283.
Darwin Center authors: Koho K. A.

Nardy Kip Wenjing Ouyang Julia van Winden Ashna Raghoebarsing Laura van Niftrik Arjan Pol Yao Pan Levente Bodrossy Elly G. van Donselaar Gert-Jan Reichart Mike S. M. Jetten Jaap S. Sinninghe Damsté and Huub J. M. Op den Camp (2011). Detection, Isolation, and Characterization of Acidophilic Methanotrophs from Sphagnum Mosses. applied and environmental microbiology77: 5643-5654.
Darwin Center authors: op den Camp H. J. M., Jetten M. S. M., Kip D. J., van Niftrik L.A.M.P., Reichart G. J., Sinninghe Damsté J. S., van Winden J. F.