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 gamma-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 beta-proteobacterial AOB was significantly elevated in this latter zone. Nitrification in the suboxic zone, most likely microaerobic in nature, was verified by (15)NO(2)(-) and (15)N(15)N production in (15)NH(4)(+) incubations with no measurable oxygen. It provided a direct local source of nitrite for anammox in the suboxic zone. Both ammonia-oxidizing crenarchaea and gamma-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 (15)N-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.