Ammonia-oxidizing archaea possess a wide range of cellular ammonia affinities

Man-Young Jung,Chloe Wright,Christopher J Sedlacek,Craig W Herbold,Linda Hink,Sung-Keun Rhee,Jose R De La Torre,Petra Pjevac,Barbara Bayer,Laura Lehtovirta-Morley,Graeme W Nicol,K Dimitri Kits,Anna J Mueller,Michael Wagner,Holger Daims

doi:10.1038/s41396-021-01064-z

Abstract

Nitrification, the oxidation of ammonia to nitrate, is an essential process in the biogeochemical nitrogen cycle. The first step of nitrification, ammonia oxidation, is performed by three, often co-occurring guilds of chemolithoautotrophs: ammonia-oxidizing bacteria (AOB), archaea (AOA), and complete ammonia oxidizers (comammox). Substrate kinetics are considered to be a major niche-differentiating factor between these guilds, but few AOA strains have been kinetically characterized. Here, the ammonia oxidation kinetic properties of 12 AOA representing all major cultivated phylogenetic lineages were determined using microrespirometry. Members of the genus Nitrosocosmicus have the lowest affinity for both ammonia and total ammonium of any characterized AOA, and these values are similar to previously determined ammonia and total ammonium affinities of AOB. This contrasts previous assumptions that all AOA possess much higher substrate affinities than their comammox or AOB counterparts. The substrate affinity of ammonia oxidizers correlated with their cell surface area to volume ratios. In addition, kinetic measurements across a range of pH values supports the hypothesis that—like for AOB—ammonia and not ammonium is the substrate for the ammonia monooxygenase enzyme of AOA and comammox. Together, these data will facilitate predictions and interpretation of ammonia oxidizer community structures and provide a robust basis for establishing testable hypotheses on competition between AOB, AOA, and comammox.

Highlights

Nitrification, the microbially mediated oxidation of ammonia (NH3) to nitrate (NO3−) via nitrite (NO2−), is a key process of the biogeochemical nitrogen cycle [1, 2] and is mostly driven by autotrophic microorganisms that are capable of growing with NH3 and/or NO2− as sole energy generating substrates
The ammonia-oxidizing archaea (AOA) strains ‘Ca. N. nevadensis’ GerE, ‘Ca. N. oleophilus’ MY3 [68] and ‘Ca. N. franklandus’ C13 [69] were kinetically characterized, and conof habitats and have optimal growth pH and temperatures ranging from 5.3–7.8 to 25–72 °C, respectively (Table S2)
While it should be recognized that in substrate, such as ammonium assimilating heterotrophic bacteria our dataset no ammoniaoxidizing microorganisms (AOM) were included that have a pH optimum or diatoms [29]. While this is useful when evaluating competition between 5.3 and 7.0, the effect of pH and temperature on the for total ammonium in mixed communities or environmental ammonia oxidation kinetics of AOM must be considered in order settings, an a° calculated using the Km(app) value for NH3 may be more useful when directly comparing the interspecies competitiveness of AOM for the following reasons: (i) our data support the hypothesis that the substrate for all AOM is NH3 and not NH4+ and (ii) the Km(app) value for total ammonium is more dependent on the environmental factors it was measured at

Summary

Introduction

Nitrification, the microbially mediated oxidation of ammonia (NH3) to nitrate (NO3−) via nitrite (NO2−), is a key process of the biogeochemical nitrogen cycle [1, 2] and is mostly driven by autotrophic microorganisms that are capable of growing with NH3 and/or NO2− as sole energy generating substrates. The AOA strains ‘Ca. N. nevadensis’ GerE (culture information provided in Supplementary Results and Discussion), ‘Ca. N. oleophilus’ MY3 [68] and ‘Ca. N. franklandus’ C13 [69] were kinetically characterized, and conof habitats (marine, soil, sediment, hot spring) and have optimal growth pH and temperatures ranging from 5.3–7.8 to 25–72 °C, respectively (Table S2).

Results

Conclusion