Microbial Biogeochemical Cycling of Nitrogen in Arid Ecosystems

Abstract

Arid ecosystems cover ∼40% of the Earth's terrestrial surface and store a high proportion of the global nitrogen (N) pool. They are low-productivity, low-biomass, and polyextreme ecosystems, i.e., with (hyper)arid and (hyper)oligotrophic conditions and high surface UV irradiation and evapotranspiration. These polyextreme conditions severely limit the presence of macrofauna and -flora and, particularly, the growth and productivity of plant species. Therefore, it is generally recognized that much of the primary production (including N-input processes) and nutrient biogeochemical cycling (particularly N cycling) in these ecosystems are microbially mediated. Consequently, we present a comprehensive survey of the current state of knowledge of biotic and abiotic N-cycling processes of edaphic (i.e., open soil, biological soil crust, or plant-associated rhizosphere and rhizosheath) and hypo/endolithic refuge niches from drylands in general, including hot, cold, and polar desert ecosystems. We particularly focused on the microbially mediated biological nitrogen fixation, N mineralization, assimilatory and dissimilatory nitrate reduction, and nitrification N-input processes and the denitrification and anaerobic ammonium oxidation (anammox) N-loss processes. We note that the application of modern meta-omics and related methods has generated comprehensive data sets on the abundance, diversity, and ecology of the different N-cycling microbial guilds. However, it is worth mentioning that microbial N-cycling data from important deserts (e.g., Sahara) and quantitative rate data on N transformation processes from various desert niches are lacking or sparse. Filling this knowledge gap is particularly important, as climate change models often lack data on microbial activity and environmental microbial N-cycling communities can be key actors of climate change by producing or consuming nitrous oxide (N₂O), a potent greenhouse gas.

Keywords: biogeochemistry; biological soil crusts; desert; diazotrophy; drylands; lithobiont; nitrogen cycling; soils.

FIG 1

Global aridity index (AI) map and microbial N-cycling gene abundances in various desert niches. The AI map (Esri grid) was obtained from the Food and Agriculture Organization of the United Nations (FAO, 10 arc min; https://data.apps.fao.org/map/catalog/srv/eng/catalog.search#/metadata/221072ae-2090-48a1-be6f-5a88f061431a) and was visually represented with ArcGIS Pro. The AI classification is shown in the key on the figure. Hot, cold, and polar deserts where quantification of microbial cycling genes has been performed are indicated by numbers. Quantitative expression (qPCR) levels of functional genes involved in N cycling were collected from available sources (Table 3), and the average expression per gene (as copies g⁻¹dry/crusted soil) was calculated for each desert. Note that the y axes of the bar plots present different scales. “D” indicates genes detected by metagenomic and/or metatranscriptomic data without available quantitative expressions levels. N.E., not evaluated; BSC, biological soil crusts. References are given in Tables 1, 2, and 3.

FIG 2

Biogeochemical cycle of nitrogen. Denitrification encompasses the nitrate, nitrite, nitric oxide, and nitrous oxide reduction reactions, and nitrification encompasses the aerobic ammonia, hydroxylamine, and nitrite oxidation reactions. Amm., ammonification; AO, ammonia oxidation; BNF, biological nitrogen fixation; DNRA, dissimilatory nitrate reduction to ammonium; HO, hydroxylamine oxidation; NO, nitrate oxidation; anammox, anaerobic ammonium oxidation; comammox, complete ammonia oxidation; Damo, denitrifying anaerobic methane oxidation. Microbial genes relevant to each process are indicated. N-Org, organic nitrogen. The NH₄⁺/NH₃ equilibrium in the environment is controlled by many parameters. Ammonia volatilization has notably been positively correlated to soil pH, CaCO₃, and salt contents and negatively to soil cation exchange capacity, organic matter, and clay contents (323).

FIG 3

Cryptic and productive desert niches colonized by free-living and symbiotic N fixers. (A) Large quartz hypolith from the McMurdo Dry Valleys (East Antarctica). The ventral surface of the quartz rock shows extensive hypolithic biomass. (B) Cryptoendolithic community in Antarctic Beacon sandstone. The green layer is dominated by Cyanobacteria. (C) Antarctic glacial runoff pan with extensive Nostoc species growth. (D) Rhizosheath-root structure of Stipagrostis ciliata (Namib Desert). (E) Namib Desert stratified salt pan microbial mat. Black bars, 3 cm. Black arrows indicate the productive and N-fixing zone.