Archaeal ammonia oxidation in volcanic grassland soils of Iceland. Effects of elevated temperature and N availability on processes and organisms

Abstract

Thaumarchaea are recognized today as the most abundant and ubiquitously dis­tributed archaeal organisms, especially in the oceans and soil. Their phylogenetic placement as a phylum, the capability of all cultivated Thaumarchaea to oxidize ammonia for energy conservation as well as many further aspects concerning their ecology, physiology and evolution are discoveries of the last decade only. Still, conceptual knowledge on the role of Thaumarchaea in soil ammonia oxida­tion is lacking and their ecological significance in soils is poorly understood. The work presented in this thesis is concerned with archaeal ammonia-oxidizing communities in volcanic grassland soil in Grændalur, Iceland. The study site was chosen as it is remote enough from continental Europe to experience very little atmospheric N deposi­tion and because it contains grassland soils with different in situ temperatures as a result of geothermal heating. Several lines of evidence were gathered that Thaumarchaea are most likely of primary importance for ammonia oxidation in Grændalur, while ammonia-oxidizing bacteria (AOB) are present in numbers below the detection limit of conventional PCR (chapter 2, 4 and 5). Supposedly, this finding resembles a high ecological importance of AOA in terrestrial environments with low ammonia availability (chapter 4). Thaumarchaea could be stimulated in growth and activ­ity by N deposition in the form of ammonium, but only in low and medium concentrations of ~ 45 - 150 μg NH4+ - N per ∙ g dry soil-1. AOB however, were only responsive to medium and higher applications of ammonium (chapter 4). Through microcosm incubations it was identified that gross nitrification (i.e. the two step process by which ammonia is converted to nitrate with nitrite as intermedi­ary product) is functionally coupled to gross N mineralization in soils of Grændalur (chapter 3). By exposing the soils to short-term temperature changes however, this coupling of gross nitrification and gross N mineralization was lost and nitrifiers performed less well. This finding led to the conclusion that the nitrifying communities in Grændalur’s soils are adapted to function best at the temperature they experience in situ (chapter 3). In a stable-isotope labeling experiment with soil from Grændalur evidence for autotrophic growth of Nitrosopumilus-like Thaumarchaea, likely coupled to am­monia oxidation, was collected (chapter 5). Additionally, the results strongly sug­gested a syntrophic association between the autotrophically growing Thaumar­chaea and nitrite-oxidizing bacteria (NOB) of the Nitrospira sublineages I and II. The work of chapter 5 furthermore showed that the autotrophically active nitrifiers in this soil (i.e. Thaumarchaea and Nitrospira-like NOB) are stimulated by application of inorganic N in form of ammonium, but suppressed by the pres­ence of active methane-oxidizing bacteria (MOB). Likely, this negative interac­tion is a result of competition for common resources like inorganic N and oxygen. Intriguingly, growth of the total Thaumarchaeal community did not seize under conditions of suppressed net nitrification and autotrophic growth. In addition, the Thaumarchaeal community structure did not change. The data collected in this thesis therefore sug­gests that at least some Thaumarchaea possess the metabolic plasticity to choose for an energetically more advantageous mode of growth than lithoautotrophy by growing mixotrophically, possibly in association with mineralizers (chapters 3 and 5)