Linking crenarchaeal and bacterial nitrification to anammox in the Black Sea
- Phyllis Lam*,†,
- Marlene M. Jensen‡,
- Gaute Lavik*,
- Daniel F. McGinnis§,
- Beat Müller§,
- Carsten J. Schubert§,
- Rudolf Amann*,
- Bo Thamdrup‡, and
- Marcel M. M. Kuypers*
- *Max Planck Institute for Marine Microbiology, Celsiusstrasse 1, 28359 Bremen, Germany;
- ‡Nordic Center for Earth Evolution, Institute of Biology, University of Southern Denmark, Campusvej 55, 5230 Odense M, Denmark; and
- §Surface Waters-Research and Management, Swiss Federal Institute of Aquatic Science and Technology (EAWAG), Seestrasse 79, CH-6047 Kastanienbaum, Switzerland
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Edited by David M. Karl, University of Hawaii, Honolulu, HI, and approved March 1, 2007 (received for review December 15, 2006)
Abstract
Active expression of putative ammonia monooxygenase gene subunit A (amoA) of marine group I Crenarchaeota has been detected in the Black Sea water column. It reached its maximum, as quantified by reverse-transcription quantitative PCR, exactly at the nitrate maximum or the nitrification zone modeled in the lower oxic zone. Crenarchaeal amoA expression could explain 74.5% of the nitrite variations in the lower oxic zone. In comparison, amoA expression by γ-proteobacterial ammonia-oxidizing bacteria (AOB) showed two distinct maxima, one in the modeled nitrification zone and one in the suboxic zone. Neither the amoA expression by crenarchaea nor that by β-proteobacterial AOB was significantly elevated in this latter zone. Nitrification in the suboxic zone, most likely microaerobic in nature, was verified by 15NO2 − and 15N15N production in 15NH4 + incubations with no measurable oxygen. It provided a direct local source of nitrite for anammox in the suboxic zone. Both ammonia-oxidizing crenarchaea and γ-proteobacterial AOB were important nitrifiers in the Black Sea and were likely coupled to anammox in indirect and direct manners respectively. Each process supplied about half of the nitrite required by anammox, based on 15N-incubation experiments and modeled calculations. Because anammox is a major nitrogen loss in marine suboxic waters, such nitrification–anammox coupling potentially occurring also in oceanic oxygen minimum zones would act as a short circuit connecting regenerated ammonium to direct nitrogen loss, thus reducing the presumed direct contribution from deep-sea nitrate.
Footnotes
- †To whom correspondence should be addressed. E-mail: plam{at}mpi-bremen.de
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Author contributions: P.L., M.M.J., B.T., and M.M.M.K. designed research; P.L., M.M.J., G.L., D.F.M., B.T., and M.M.M.K. performed research; D.F.M., B.M., C.J.S., and R.A. contributed new reagents/analytical tools; P.L., M.M.J., G.L., B.T., and M.M.M.K. analyzed data; and P.L. and M.M.M.K. wrote the paper.
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The authors declare no conflict of interest.
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This article is a PNAS direct submission.
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Data deposition: The sequences reported in this paper have been deposited in the GenBank database (accession nos. EF414229–EF414283).
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See Commentary on page 6881.
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This article contains supporting information online at www.pnas.org/cgi/content/full/0611081104/DC1.
- Abbreviations:
- AOB,
- ammonia-oxidizing bacteria;
- βAOB,
- β-proteobacterial AOB;
- γAOB,
- γ-proteobacterial AOB;
- MGI,
- marine group I;
- amoA,
- ammonia monooxygenase gene subunit A;
- OMZ,
- oxygen minimum zone;
- AMO,
- ammonia monooxygenase;
- CARD,
- catalyzed reporter deposition;
- qPCR,
- quantitative PCR;
- OTU,
- operational taxonomic unit.
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Freely available online through the PNAS open access option.
- © 2007 by The National Academy of Sciences of the USA
