Ammonia oxidation coupled to CO ₂ fixation by archaea and bacteria in an agricultural soil

Abstract

Ammonia oxidation is an essential part of the global nitrogen cycling and was long thought to be driven only by bacteria. Recent findings expanded this pathway also to the archaea. However, most questions concerning the metabolism of ammonia-oxidizing archaea, such as ammonia oxidation and potential CO 2 fixation, remain open, especially for terrestrial environments. Here, we investigated the activity of ammonia-oxidizing archaea and bacteria in an agricultural soil by comparison of RNA-and DNA-stable isotope probing (SIP). RNA-SIP demonstrated a highly dynamic and diverse community involved in CO 2 fixation and carbon assimilation coupled to ammonia oxidation. DNA-SIP showed growth of the ammonia-oxidizing bacteria but not of archaea. Furthermore, the analysis of labeled RNA found transcripts of the archaeal acetyl-CoA/propionyl-CoA carboxylase (accA/pccB) to be expressed and labeled. These findings strongly suggest that ammoniaoxidizing archaeal groups in soil autotrophically fix CO 2 using the 3-hydroxypropionate-4-hydroxybutyrate cycle, one of the two pathways recently identified for CO 2 fixation in Crenarchaeota. Catalyzed reporter deposition (CARD)-FISH targeting the gene encoding subunit A of ammonia monooxygenase (amoA) mRNA and 16S rRNA of archaea also revealed ammonia-oxidizing archaea to be numerically relevant among the archaea in this soil. Our results demonstrate a diverse and dynamic contribution of ammonia-oxidizing archaea in soil to nitrification and CO 2 assimilation and that their importance to the overall archaeal community might be larger than previously thought.

Ammonia-oxidizing archaea have more important role than ammonia-oxidizing bacteria in ammonia oxidation of strongly acidic soils

“…Because of the development of new technologies like DNA-stable isotope probing (SIP), we could now be able to gain a deep insight into the autotrophic nitrification activity in complex soil environments. 13 CO 2 -DNA-SIP has shown its powerful potential to directly link CO 2 -incorporating ammonia oxidizers with nitrification activity in several neutral or alkaline soils (Jia and Conrad, 2009;Zhang et al, 2010;Pratscher et al, 2011;Xia et al, 2011) and provided evidence for autotrophic growth of N. devanaterra in acidic soil, whereas to the best of our knowledge, no study has been able to clearly identify the dominating ammonia oxidizers in the autotrophic nitrification of acidic soils.…”

Crenarchaeal heterotrophy in salt marsh sediments

“…Most of these studies have focused on autotrophy and ammonia oxidation in various environments such as rice paddies (Lu and Conrad, 2005), soils (Adair and Schwartz, 2011;Pratscher et al, 2011;Lu and Jia, 2013) and in freshwater sediment (Wu et al, 2013). However, there are also reports of heterotrophic activity from an acidic fen (Hamberger et al, 2008) and an estuarine setting in the UK (Webster et al, 2010).…”

Significance of archaeal nitrification in hypoxic waters of the Baltic Sea

“…Phylogenetically affiliated with the novel phylum Thaumarchaeota (Brochier-Armanet et al, 2008;Spang et al, 2010), AOA occur in high abundances in both terrestrial (Zhang et al, 2010;Pratscher et al, 2011) and aquatic (Yakimov et al, 2011;Biller et al, 2012;Amano-Sato et al, 2013) ecosystems, often outnumbering bacterial ammonia oxidizers (Schleper, 2010). As a consequence, questions arise regarding the ecological niche of AOA, their roles in nitrification and primary production and the environmental factors that regulate their contribution to these processes.…”