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

Abstract

Ammonium/ammonia is the sole energy substrate of ammonia oxidizers, and is also an essential nitrogen source for other microorganisms. Ammonia oxidizers therefore must compete with other soil microorganisms such as methane-oxidizing bacteria (MOB) in terrestrial ecosystems when ammonium concentrations are limiting. Here we report on the interactions between nitrifying communities dominated by ammonia-oxidizing archaea (AOA) and Nitrospira-like nitrite-oxidizing bacteria (NOB), and communities of MOB in controlled microcosm experiments with two levels of ammonium and methane availability. We observed strong stimulatory effects of elevated ammonium concentration on the processes of nitrification and methane oxidation as well as on the abundances of autotrophically growing nitrifiers. However, the key players in nitrification and methane oxidation, identified by stable-isotope labeling using 13 CO 2 and 13 CH 4 , were the same under both ammonium levels, namely type 1.1a AOA, sublineage I and II Nitrospira-like NOB and Methylomicrobium-/ Methylosarcina-like MOB, respectively. Ammonia-oxidizing bacteria were nearly absent, and ammonia oxidation could almost exclusively be attributed to AOA. Interestingly, although AOA functional gene abundance increased 10-fold during incubation, there was very limited evidence of autotrophic growth, suggesting a partly mixotrophic lifestyle. Furthermore, autotrophic growth of AOA and NOB was inhibited by active MOB at both ammonium levels. Our results suggest the existence of a previously overlooked competition for nitrogen between nitrifiers and methane oxidizers in soil, thus linking two of the most important biogeochemical cycles in nature.

Ammonia-limited conditions cause of Thaumarchaeal dominance in volcanic grassland soil

“…It is therefore plausible to attribute the ammonia oxidation indirectly observed via net nitrification in the NA microcosms to the activity of AOA well in line with a previous DNA-SIP study attributing ammonia-oxidation exclusively to Thaumarchaea in the same soil (Daebeler et al 2014). This is in contrast to many other soils where AOB are suggested to have a more important role in nitrification than AOA (e.g.…”

Proteomics and comparative genomics of Nitrososphaera viennensis reveal the core genome and adaptations of archaeal ammonia oxidizers

“…Studying these features in an environmental context will be important to identify microbial interaction partners of AOA (for example, specific associations with nitrite oxidizers or other groups that could participate in the process of nitrogen species interconversions connected through the substrate-product chain) (90). It will be equally interesting to elucidate those adaptations that are the basis for the enormous ecological success of AOA in terrestrial environments.…”

Expanded metabolic versatility of ubiquitous nitrite-oxidizing bacteria from the genus Nitrospira

“…Analyses of Nitrobacter genome sequences provided first insights into the genomic makeup of NOB and revealed a greater metabolic flexibility than anticipated earlier, which included the mixotrophic utilization of various organic substrates (8,9). However, Nitrobacter require high nitrite concentrations (10,11), and molecular surveys indicated that Nitrobacter are not the primary NOB in ecosystems with low ambient nitrite levels such as unfertilized soils (12), freshwater habitats (13), and most WWTPs (14).…”