Anaerobic ammonium‐oxidizing bacteria in marine environments: widespread occurrence but low diversity

Abstract

Laboratory and field studies have indicated that anaerobic ammonium oxidation (anammox) is an important process in the marine nitrogen cycle. In this study 11 additional anoxic marine sediment and water column samples were studied to substantiate this claim. In a combined approach using the molecular methods, polymerase chain reaction (PCR), qualitative and quantitative fluorescence in situ hybridization (FISH), as well as (15)N stable isotope activity measurements, it was shown that anammox bacteria were present and active in all samples investigated. The anammox activity measured in the sediment samples ranged from 0.08 fmol cell(-1) day(-1) N(2) in the Golfo Dulce (Pacific Ocean, Costa Rica) sediment to 0.98 fmol cell(-1) day(-1) N(2) in the Gullmarsfjorden (North Sea, Sweden) sediment. The percentage of anammox cell of the total population (stained with DAPI) as assessed by quantitative FISH was highest in the Barents Sea (9% +/- 4%) and in most of the samples well over 2%. Fluorescence in situ hybridization and phylogenetic analysis of the PCR products derived from the marine samples indicated the exclusive presence of members of the Candidatus'Scalindua' genus. This study showed the ubiquitous presence of anammox bacteria in anoxic marine ecosystems, supporting previous observations on the importance of anammox for N cycling in marine environments.

Nitrogen removal through different pathways in an aged refuse bioreactor treating mature landfill leachate

“…We were not sure whether some of the unidentified Planctomycetes (2.36 % of total bacteria) were anammox bacteria. Our current results also showed that anammox bacteria were present not only in the freshwater and marine environments (Schmid et al 2007;Wang and Gu 2012;Woebken et al 2008), but also in the complicated landfill system. This expands our knowledge on the biogeography of anammox bacteria.…”

“…Candidatus Kuenenia stuttgartiensis is a salt-and alkaline-resistant bacterium Strous et al 2006), and it was detected mostly in wastewater treatment system (Egli et al 2001;Schmid et al 2000). Previous research showed that anammox diversity was usually low in an ecosystem (Schmid et al 2007;Kartal et al 2007). In our bioreactor, anammox bacteria detected by qPCR accounted for 0.27 % of total bacteria, and the value was higher than that from the pyrosequencing method.…”

Potential roles of anaerobic ammonium and methane oxidation in the nitrogen cycle of wetland ecosystems

“…Various anoxic marine ecosystems have been monitored for anammox activity and the presence of anammox cells (Kuypers et al 2003Rysgaard et al 2004;Risgaard-Petersen et al 2004;Schmid et al 2007). The anammox bacteria in marine environments seem to be restricted to the Scalindua branch with relatively little biodiversity as reflected in very similar 16S rRNA gene sequences (Fig.…”

“…4. In various ecosystems, anammox and NC10 bacteria will be dependent on the activity of aerobic ammonia-oxidizing bacteria under oxygen-limited conditions, e.g., at the oxic/anoxic interface (Dalsgaard et al 2003;Schmid et al 2007;Lam et al , 2009). Oxic/anoxic interfaces are abundant in nature, for example in the rhizosphere of helophytes, biofilms, and marine sediments (Murray et al 1989).…”

Presence and activity of anaerobic ammonium-oxidizing bacteria at deep-sea hydrothermal vents

“…Nutrient profiles, activity measurements, ladderane lipids analysis, 16S rRNA gene sequences and fluorescent in situ hybridization showed that Candidatus 'Scalindua sorokinii' was present and active in the anoxic basin of the Black Sea (Kuypers et al, 2003). In the meantime, many studies have shown that the anammox bacteria and the annamox process are ubiquitous and constitute a substantial sink of fixed nitrogen in the oceans (Dalsgaard et al, 2003;Kuypers et al, 2003;Penton et al, 2006;Schmid et al, 2007). The process is also significant in minimum oxygen zones (Kuypers et al, 2005;Hamersley et al, 2007;Jaeschke et al, 2007), sediments (Engstrom et al, 2005;Penton et al, 2006) and estuaries (Trimmer et al, 2003;Tal et al, 2005).…”