Organization of biogeochemical nitrogen pathways with switch-like adjustment in fluctuating soil redox conditions

Abstract

Nitrogen is cycled throughout ecosystems by a suite of biogeochemical processes. The high complexity of the nitrogen cycle resides in an intricate interplay between reversible biochemical pathways alternatively and specifically activated in response to diverse environmental cues. Despite aggressive research, how the fundamental nitrogen biochemical processes are assembled and maintained in fluctuating soil redox conditions remains elusive. Here, we address this question using a kinetic modelling approach coupled with dynamical systems theory and microbial genomics. We show that alternative biochemical pathways play a key role in keeping nitrogen conversion and conservation properties invariant in fluctuating environments. Our results indicate that the biochemical network holds inherent adaptive capacity to stabilize ammonium and nitrate availability, and that the bistability in the formation of ammonium is linked to the transient upregulation of the amo-hao mediated nitrification pathway. The bistability is maintained by a pair of complementary subsystems acting as either source or sink type systems in response to soil redox fluctuations. It is further shown how elevated anthropogenic pressure has the potential to break down the stability of the system, altering substantially ammonium and nitrate availability in the soil, with dramatic effects on biodiversity.

Functional properties of bacterial communities in water and sediment of the eutrophic river-lake system of Poyang Lake, China

“…Poyang Lake has been facing serious threat of eutrophication (Wang et al, 2015; Zhang et al, 2015; Liu, Fang & Sun, 2016) because of the aggravated nutrient loading from agriculture and urbanization of the catchment in recent decades (Wang & Liang, 2015; Liu, Fang & Sun, 2016). Nitrogen has many different chemical forms from the oxidation state of nitrate (+5) to the reduction state of ammonia (−3) and is cycled by a suite of biogeochemical processes (Ollivier et al, 2011), including four reduction pathways (denitrification, nitrogen fixation, ANRA, and DNRA) and two oxidation pathway (anammox and nitrification) (Lamba et al, 2017). In aquatic ecosystems, denitrification is the main biological process turning nitrate to dinitrogen and nitrous oxide (Tiedje et al, 1983; Seitzinger, 1988) and anammox is another important pathway turning nitrite and ammonia to dinitrogen (Dalsgaard et al, 2003; Kuypers et al, 2003).…”

“…In nitrogen metabolism pathways, both ANRA and DNRA had a higher relative abundance in water than in sediment, suggesting strong potentials of nitrate reduction to ammonia for bacterial communities in water column. ANRA and DNRA serve distinct cellular functions (Lamba et al, 2017): ANRA consumes energy and provides ammonium for cell to synthesize amino acids and nucleotides, while NDRA generates ATP in absence of oxygen and retains the nitrogen in the form of NH 4 + for further biological processes (Zumft, 1997).…”

Microbial functional genes elucidate environmental drivers of biofilm metabolism in glacier-fed streams

“…In ecosystems, nitrogen metabolic pathways are particularly susceptible to environmental redox fluctuations because of the large difference between the oxidation state of nitrate (+5) in nitrate and that of ammonia (−3) 80 , 81 . Moreover, some other environmental factors also strongly impact nitrogen cycling.…”

Microbial community structure and functional properties in permanently and seasonally flooded areas in Poyang Lake

“…In general, ANR processes are much more prevalent than DNR processes in natural ecosystems 3,71 , and high concentrations of NH 4 + could stimulate assimilatory pathways 67,71,72 . The reduction processes of NO 3 − to NO 2 − and then to NH 4 + are part of the ANR processes, which usually occur in anaerobic environments such as sediment and soil 73 . In the wet season, a large amount of mineralized nitrogen (especially NH 4 + ) could be easily dissolved in pore water and be rapidly released into lake water, and these mineralized nitrogen types could be used by bacterial communities as an energy source 3,71,74 .…”