Journal Article

Kinetic analysis of a complete nitrifier reveals an oligotrophic lifestyle

Bulaev, Alexandr, Albertsen, Mads, Sedlacek, Christopher J., Daims, Holger, Stein, Lisa Y., Pjevac, Petra, Han, Ping, Daebeler, Anne, Wagner, Michael, Romano, Stefano, Kits, K. Dimitri, Lebedeva, Elena V.

2017

Overview

A pure culture of the complete nitrifier Nitrospira inopinata shows a high affinity for ammonia, low maximum rate of ammonia oxidation, high growth yield compared to canonical nitrifiers and genomic potential for alternative metabolisms, probably reflecting an important role in nitrification in oligotrophic environments. Nutrient-starved nitrification Nitrospira inopinata was the first bacterium identified that is capable of catalysing complete ammonia oxidization (referred to as comammox). Holger Daims and colleagues now report a pure culture of this organism, which enabled a characterization of its physiology. The authors find that N. inopinata has a high affinity for ammonia, a low maximum rate of ammonia oxidation, a high growth yield compared to canonical nitrifiers, and the genomic potential for alternative metabolisms. The team compare the nitrification kinetics of N. inopinata to that of four ammonia-oxidizing archaea. The results suggest that N. inopinata is likely to have an important role in nitrification, especially in oligotrophic environments. Nitrification, the oxidation of ammonia (NH 3 ) via nitrite (NO 2 − ) to nitrate (NO 3 − ), is a key process of the biogeochemical nitrogen cycle. For decades, ammonia and nitrite oxidation were thought to be separately catalysed by ammonia-oxidizing bacteria (AOB) and archaea (AOA), and by nitrite-oxidizing bacteria (NOB). The recent discovery of complete ammonia oxidizers (comammox) in the NOB genus Nitrospira 1 , 2 , which alone convert ammonia to nitrate, raised questions about the ecological niches in which comammox Nitrospira successfully compete with canonical nitrifiers. Here we isolate a pure culture of a comammox bacterium, Nitrospira inopinata , and show that it is adapted to slow growth in oligotrophic and dynamic habitats on the basis of a high affinity for ammonia, low maximum rate of ammonia oxidation, high growth yield compared to canonical nitrifiers, and genomic potential for alternative metabolisms. The nitrification kinetics of four AOA from soil and hot springs were determined for comparison. Their surprisingly poor substrate affinities and lower growth yields reveal that, in contrast to earlier assumptions, AOA are not necessarily the most competitive ammonia oxidizers present in strongly oligotrophic environments and that N. inopinata has the highest substrate affinity of all analysed ammonia oxidizer isolates except the marine AOA Nitrosopumilus maritimus SCM1 (ref. 3 ). These results suggest a role for comammox organisms in nitrification under oligotrophic and dynamic conditions.

• Publisher: Nature Publishing Group UK,Nature Publishing Group
• Subject: 14/32 / 45 / 45/23 / 45/77 / 631/158/855 / 631/326/171 / Ammonia / Ammonia - metabolism / Ammonia-oxidizing bacteria / Archaea - metabolism / Bacteria / Bacteria - genetics / Bacteria - growth & development / Bacteria - isolation & purification / Bacteria - metabolism / Biogeochemical cycles / Ecological niches / Ecosystem / Hot springs / Hot Springs - microbiology / Humanities and Social Sciences / Kinetics / letter / Microorganisms / multidisciplinary / Niches / Nitrates / Nitrates - metabolism / Nitrification / Nitrites / Nitrites - metabolism / Nitrogen cycle / Nitrogen dioxide / Nitrogen-fixing microorganisms / Observations / Oligotrophic environments / Oligotrophs / Oxidation / Oxidation-Reduction / Oxidizing agents / Pure culture / Reaction kinetics / Science / Seawater / Soil Microbiology