Molecular and biogeochemical evidence for ammonia oxidation by marine Crenarchaeota in the Gulf of California.
Nitrification plays an important role in marine biogeochemistry, yet efforts to link this process to the microorganisms that mediate it are surprisingly limited. In particular, ammonia oxidation is the first and rate-limiting step of nitrification, yet ammonia oxidation rates and the abundance of ammonia-oxidizing bacteria (AOB) have rarely been measured in tandem. Ammonia oxidation rates have not been directly quantified in conjunction with ammonia-oxidizing archaea (AOA), although mounting evidence indicates that marine Crenarchaeota are capable of ammonia oxidation, and they are among the most abundant microbial groups in the ocean. Here, we have directly quantified ammonia oxidation rates by 15N labeling, and AOA and AOB abundances by quantitative PCR analysis of ammonia monooxygenase subunit A (amoA) genes, in the Gulf of California. Based on markedly different archaeal amoA sequence types in the upper water column (60 m) and oxygen minimum zone (OMZ; 450 m), novel amoA PCR primers were designed to specifically target and quantify 'shallow' (group A) and 'deep' (group B) clades. These primers recovered extensive variability with depth. Within the OMZ, AOA were most abundant where nitrification may be coupled to denitrification. In the upper water column, group A tracked variations in nitrogen biogeochemistry with depth and between basins, whereas AOB were present in relatively low numbers or undetectable. Overall, 15NH4+ oxidation rates were remarkably well correlated with AOA group A amoA gene copies (r2=0.90, P<0.001), and with 16S rRNA gene copies from marine Crenarchaeota (r2=0.85, P<0.005). These findings represent compelling evidence for an archaeal role in oceanic nitrification.
Beman
J Michael
JM
Department of Geological and Environmental Sciences, Stanford University, Stanford, CA, USA. jmbeman@gmail.com
Popp
Brian N
BN
Francis
Christopher A
CA
D000641:Ammonia / Q000378:metabolism*; D002140:California; D019615:Crenarchaeota / Q000235:genetics* / Q000378:metabolism; D019641:DNA, Archaeal / Q000032:analysis / Q000302:isolation & purification; D008969:Molecular Sequence Data; D009584:Nitrogen / Q000737:chemistry / Q000378:metabolism; D009587:Nitrogen Isotopes / Q000378:metabolism; D010084:Oxidation-Reduction; D010088:Oxidoreductases / Q000235:genetics / Q000378:metabolism; D012623:Seawater / Q000382:microbiology*; D017422:Sequence Analysis, DNA
D019641:DNA, Archaeal; D009587:Nitrogen Isotopes; D000641:Ammonia; D010088:Oxidoreductases; C045582:ammonia monooxygenase; D009584:Nitrogen