Linking crenarchaeal and bacterial nitrification to anammox in the Black Sea

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 ␥-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 ␤-proteobacterial AOB was significantly elevated in this latter zone. Nitrification in the suboxic zone, most likely microaerobic in nature, was verified by 15 ammonia-oxidizing bacteria ͉ amoA gene expression ͉ marine group ͉ Crenarchaeota ͉ marine nitrogen loss N itrification, the stepwise oxidation of ammonium to nitrite and then nitrate, is a key process in marine nitrogen cycling. It is responsible for the formation of the large deep-sea nitrate reservoir. It connects the recycling of organic nitrogen to the ultimate nitrogen loss from the oceans, because its products are substrates for denitrification and anaerobic ammonium oxidation (anammox), the only two presently known nitrogen loss processes. In productive waters such as upwelling regions, high fluxes of organic matter and thus remineralization create strong subsurface oxygen minima, enabling denitrification (1-4) or anammox (5-8) to occur. Nitrogen losses from these oxygen minimum zones (OMZs) are estimated to account for 30-50% of total nitrogen loss from the oceans (9, 10). Because remineralization also releases large amounts of ammonium, high nitrification rates are often associated with these OMZs (11), implying that nitrification may play an important role in promoting marine nitrogen loss.The Black Sea is the largest marine anoxic basin in the world. A 20-to 40-m-thick suboxic transitional zone, characterized by low oxygen (Ͻ5 M) and undetectable sulfide, persists throughout the basin between the surface oxic layer and the sulfidic anoxic deep water (Ն100 m) (12, 13). The exact depth zonation varies according to the location within the basin because of circulation and gyre formation, but similar concentrations of chemical species can be traced along isopycnals or density ( t ) surfaces throughout the basin (12). Therefore, the Black Sea provides an ideal model system to study nitrogen cycling processes along oxygen gradients. Nitrification has been reported in the lower oxic zone (14) and so has nitrogen loss via anammox in the suboxic zone (15). Nevertheless, the identity and abundance of the responsible nitrifiers, or any coupling between nitrification and nitrogen losses, remain poorly documented.The first and rate-limiting step of nitrification is aerobic ammonia oxidation. It is a microbially mediated reaction. For decades, only specific groups of ␤-and ␥-proteobacteria have been found to exh...

Prokaryotic diversity, distribution, and insights into their role in biogeochemical cycling in marine basalts

“…Nitrification could provide the substrate for both denitrification and anaerobic ammonium oxidation (anammox), both of which lead to loss of nitrogen (Lam et al, 2007). In fact, we found numerous genes coding for nitrate and nitrite reduction; therefore, the genetic potential for denitrification is present in this environment.…”

Towards a better understanding of microbial carbon flux in the sea*

“…While our knowledge of the spatial distribution and magnitude of carbon fixation in the oxygenated dark realm, comprising ca. 75% of the global ocean's volume, is rather rudimentary, inorganic carbon fixation in oxygen minimum zones has received far more attention, although it comprises only 0.1% of the ocean's volume (Taylor et al 2001, Hannig et al 2007, Lam et al 2007). …”

“…Pelagic prokaryotic chemoautotrophy increases with decreasing oxygen concentrations in the water column (Taylor et al 2001, Hannig et al 2007, Lam et al 2007). Consequently, highest pelagic prokaryotic carbon fixation rates have been reported for suboxic and anoxic water bodies such as the Black Sea, the Cariaco Basin and the twilight zones of upwelling areas (Taylor et al 2001, Kuypers et al 2005, Hamersley et al 2007.…”

Enrichment and characterization of ammonia-oxidizing archaea from the open ocean: phylogeny, physiology and stable isotope fractionation

“…Mesophilic archaea are ubiquitous and abundant members of diverse marine environments including coastal waters (Mincer et al, 2007;Beman et al, 2010), marine sediments, estuaries (Mosier and Francis, 2008;Bernhard et al, 2010;Urakawa et al, 2010), stratified basins (Coolen et al, 2007;Lam et al, 2007) and open ocean water columns (Beman et al, 2008;Church et al, 2010;Santoro et al, 2010). The recent cultivation of the first mesophilic marine archaeon, Nitrosopumilus maritimus, (Konneke et al, 2005;Martens-Habbena et al, 2009), two thermophilic archaea, Nitrosocaldus yellowstonii and Nitrosophaera gargensis (Hatzenpichler et al, 2008;de la Torre et al, 2008) and a freshwater archaeon, Nitrosoarchaeum limnia (Blainey et al, 2011) established that at least some of these organisms are chemolithoautotrophic ammonia oxidizers.…”