Diversity of archaea and niche preferences among putative ammonia-oxidizing Nitrososphaeria dominating across European arable soils

Abstract

Background: Archaeal communities in arable soils are dominated by Nitrososphaeria, a class within Thaumarchaeota comprising all known ammonia-oxidizing archaea (AOA). AOA are key players in the nitrogen cycle and defining their niche specialization can help predicting effects of environmental change on these communities. However, hierarchical effects of environmental filters on AOA and the delineation of niche preferences of nitrososphaerial lineages remain poorly understood. Here we combined multiple environmental gradients with fine-scale phylogenetic analyses and machine learning for new insights into ecological preferences within Nitrososphaeria. With this approach, we could identify climatic, edaphic and geomorphological drivers of Nitrososphaeria and other archaea in arable soils along a 3 000 km European gradient. Results: Mean annual temperature, C:N ratio and pH were the best predictors of diversity, evenness and distribution of Nitrososphaeria and thresholds in the predictions could be defined for C:N ratio and cation exchange capacity. Recent adaptations to soil pH were indicated in the Nitrososphaeria phylogeny. Our analyses further suggest the coexistence of widespread ecophysiological differences between closely related soil Nitrososphaeria. Only limited insights into the ecology of the low-abundant, but highly diverse classes Thermoplasmata and Woesearchaeia could be inferred. However, for explaining the overall archaeal community composition at the continental scale the contribution of distance (reflecting stochastic assembly processes) and environmental factors (reflecting deterministic processes) were comparable. Conclusions: Our findings underline the multifactorial nature of niche differentiation in soil Nitrososphaeria and the ecophysiological differences between closely related members observed suggest that the phylogeny does not reflect their ecology. Our results also imply multiple, independent specializations to low pH. The study highlights that the ecology of Nitrososphaeria is best studied at fine phylogenetic scale. Finally, the identification of thresholds in the responses show that simple correlations are not sufficient when determining environmental drivers of archaeal diversity.