Thermodynamic characterization of proton‐ionizable functional groups on the cell surfaces of ammonia‐oxidizing bacteria and archaea

Abstract

The ammonia-oxidizing archaeon Nitrosopumilus maritimus strain SCM1 (strain SCM1), a representative of the Thaumarchaeota archaeal phylum, can sustain high specific rates of ammonia oxidation at ammonia concentrations too low to sustain metabolism by ammonia-oxidizing bacteria (AOB). One structural and biochemical difference between N. maritimus and AOB that might be related to the oligotrophic adaptation of strain SCM1 is the cell surface. A proteinaceous surface layer (S-layer) comprises the outermost boundary of the strain SCM1 cell envelope, as opposed to the lipopolysaccharide coat of Gram-negative AOB. In this work, we compared the surface reactivities of two archaea having an S-layer (strain SCM1 and Sulfolobus acidocaldarius) with those of four representative AOB (Nitrosospira briensis, Nitrosomonas europaea, Nitrosolobus multiformis, and Nitrosococcus oceani) using potentiometric and calorimetric titrations to evaluate differences in proton-ionizable surface sites. Strain SCM1 and S. acidocaldarius have a wider range of proton buffering (approximately pH 10-3.5) than the AOB (approximately pH 10-4), under the conditions investigated. Thermodynamic parameters describing proton-ionizable sites (acidity constants, enthalpies, and entropies of protonation) are consistent with these archaea having proton-ionizable amino acid side chains containing carboxyl, imidazole, thiol, hydroxyl, and amine functional groups. Phosphorous-bearing acidic functional groups, which might also be present, could be masked by imidazole and thiol functional groups. Parameters for the AOB are consistent with surface structures containing anionic oxygen ligands (carboxyl- and phosphorous-bearing acidic functional groups), thiols, and amines. In addition, our results showed that strain SCM1 has more reactive surface sites than the AOB and a high concentration of sites consistent with aspartic and/or glutamic acid. Because these alternative boundary layers mediate interaction with the local external environment, these data provide the basis for further comparisons of the thermodynamic behavior of surface reactivity toward essential nutrients.

Interactions between Thaumarchaea, Nitrospira and methanotrophs modulate autotrophic nitrification in volcanic grassland soil

“…AOA of the 1.1a and the Nitrosotalea lineages, which comprise the vast majority of the AOA community detected in our incubations, are often found under oligotrophic conditions and may be adapted to low ammonium environments (MartensHabbena et al, 2009;Martens-Habbena and Stahl, 2011;French et al, 2012;Nakagawa and Stahl, 2013;Gorman-Lewis et al, 2014). Nitrosotalea-like AOA have been demonstrated to be adapted to low pH environments, but are also abundant among ammonia oxidizers in many other terrestrial ecosystems and not exclusively found in low pH soils (Leininger et al, 2006;Gubry-Rangin et al, 2011;Lehtovirta-Morley et al, 2011;Pester et al, 2011).…”

Genomes of Two New Ammonia-Oxidizing Archaea Enriched from Deep Marine Sediments

“…This is in partial contrast to the COG classes found in the GIs of other archaeal genomes, which are predominantly M or Q (secondary metabolite biosynthesis, transport, and catabolism) [32]. The proteinaceous surface layers of AOA have an abundance of reactive surface sites that are conceivably related to their oligotrophic adaptations [33]. The frequent observation of COG class M genes in the GIs of the AR1 and AR2 genomes could contribute to variations in cell surface structure, which might be important factors for niche specialization in AOA ecotypes.…”

Ammonia-oxidizing archaea have better adaptability in oxygenated/hypoxic alternant conditions compared to ammonia-oxidizing bacteria

“…Nitrification, a two-step process in the oxidation of ammonia to nitrate, begins with the aerobic oxidation of ammonia to nitrite (Gorman-Lewis et al 2014). Betaproteobacteria and Gammaproteobacteria were long thought to be the only two clades to perform ammonia oxidation (Prosser and Nicol 2008).…”