Ammonia-oxidizing archaea and bacteria are structured by geography in biological soil crusts across North American arid lands

Ian Anderson,Yevgeniy Marusenko,Shannon L Johnson,Ferran Garcia-Pichel,Scott T Bates,Tanya Soule

doi:10.1186/2192-1709-2-9

Abstract

Abstract Introduction Biological soil crusts (BSCs) can dominate surface cover in dry lands worldwide, playing an integral role in arid land biogeochemistry, particularly in N fertilization through fixation and cycling. Nitrification is a characteristic and universal N transformation in BSCs that becomes important for the export of N beyond the microscopic bounds of the crust itself. The contribution of ammonia-oxidizing bacteria (AOB) in BSCs has been shown, but the role and extent of the recently discovered ammonia-oxidizing archaea (AOA) have not. Methods We sampled various types of crusts in four desert regions across the western United States and characterized the composition and size of ammonia-oxidizing communities using clone libraries and quantitative PCR targeting the amoA gene, which codes for the ammonia monooxygenase enzyme, universally present in ammonia-oxidizing microbes. Results All archaeal amoA sequences retrieved from BSCs belonged to the Thaumarchaeota (Nitrososphaera associated Group I.1b). Sequences from the Sonoran Desert, Colorado Plateau, and Great Basin were indistinguishable from each other but distinct from those of the Chihuahuan Desert. Based on amoA gene abundances, archaeal and bacterial ammonia oxidizers were ubiquitous in our survey, but the ratios of archaeal to bacterial ammonia oxidizers shifted from bacterially dominated in northern, cooler deserts to archaeally dominated in southern, warmer deserts. Conclusions Archaea are shown to be potentially important biogeochemical agents of biological soil crust N cycling. Conditions associated with different types of BSCs and biogeographical factors reveal a niche differentiation between AOA and AOB, possibly driven by temperature.

Highlights

Biological soil crusts (BSCs) can dominate surface cover in dry lands worldwide, playing an integral role in arid land biogeochemistry, in N fertilization through fixation and cycling
With more than 40 clones in each desert, revealed that monophyletic amoA gene populations corresponding to each desert region exist in arid land BSCs: only a single archaeal amoA phylotype was recovered from each desert (98.5–100% nucleotide similarity)
Phylogeny (Figure 2) of the four representative sequences revealed that phylotypes from three of the deserts (Great Basin, Sonoran, and Colorado Plateau) were indistinguishable, grouping in a well-defined clade (>95% similarity, 76% bootstrap support), while a lone sequence type was distinct

Summary

Introduction

Biological soil crusts (BSCs) can dominate surface cover in dry lands worldwide, playing an integral role in arid land biogeochemistry, in N fertilization through fixation and cycling. Nitrification (with ammonia oxidation as its ratelimiting step) mediated by BSC microbes is another important component of arid land nutrient cycling that directly impacts soil fertility and rivals N-fixation in its magnitude (Johnson et al 2005). Nitrifiers, such as Nitrosospira, have been recovered from BSCs in molecular surveys, and most probable number assessments suggest ammonia-oxidizing bacteria (AOB) are numerically abundant in BSCs (Gundlapally and Garcia-Pichel 2006; Johnson et al 2005). Archaea are likely important soil ammonia oxidizers (Leininger et al 2006; Zhang et al 2010; Bates et al 2011; Stahl and de la Torre 2012) and sizable archaeal populations have been reported from BSCs (Soule et al 2009), little is known about the role of archaea in the arid land N-cycle

Methods

Results

Conclusion