Our results show that archaeal amoA genes are conspicuously and widely represented in BSCs from several arid regions of North America, suggesting that archaea are potentially involved in the process of ammonia oxidation of these soil communities. In general, average AOA abundance in BSCs was 10- to 20-fold lower than in most other types of soils, with some overlap in range (He et al.
2007; Leininger et al.
2006), and less than 10-fold smaller as reported in few other environments (Chen et al.
2008; Gleeson et al.
2010; Zeglin et al.
2011). Judged by the counts of amoA gene copies, AOA in fact outnumbered AOB when averaged over all sites.
The populations of amoA-bearing archaea are, however, of low diversity based on initial surveying in these systems using clone libraries, which mirrors the findings that archaeal diversity is also generally restricted in both bulk soils (Auguet et al.
2010; Fernandez-Guerra and Casamayor
2012) and in BSCs (Nagy et al.
2005; Soule et al.
2009). We note that most publicly available sequences that had high similarity (>97% at the nucleotide level) to those of BSCs from this study originated from terrestrial environments with source soils of relatively alkaline character (Leininger et al.
2006; Shen et al.
2008; Zhang et al.
2011; Liu et al.
2010; Glaser et al.
2010; Fan et al.
2011). Because the number of samples analyzed is not exhaustive, we cannot assert with confidence that the two main amoA phylotypes found in BSCs in this study represent crust-specific lineages, although this remains a possibility to be explored further. Other studies have shown that certain AOA lineages have adapted to specific levels of pH (Gubry-Rangin et al.
2011). Arid lands are characteristically extreme environments exposed to intense UV radiation, limited availability of nutrients, alkaline soils, as well as distinct seasonal changes of long desiccation periods punctuated by pulsed precipitation events (Schlesinger
1997; Safriel et al.
2005), all of which may help carve separate niches for soil organisms (Wall and Virginia
1999). AOA dynamics may be distinct and depend on the range of a certain environmental variable (e.g., temperature gradient in only alkaline soils) in different types of BSCs and other local conditions that affect crusts (Garcia-Pichel et al.
2003; Pointing and Belnap
2012). What seems clear is that crust-dwelling AOA are part of a broader consortium of archaea more related to the group I.1b Nitrososphaera cluster than to any other Thaumarchaeota group. All BSC amoA archaeal phylotypes were nested within a larger group that holds the sequence from the only pure culture isolate from soil capable of chemolithoautotrophic ammonia oxidation, Nitrososphaera viennensis (Tourna et al.
Unexpected patterns of distribution emerged when AOA and AOB population size was related to geography. Variables that are associated with latitude become important predictors of amoA abundance. Since an AOA/AOB ratio of >10 (accounting for cell sizes, specific growth rates; Prosser and Nicol
2012) suggests archaea outcompete bacteria in ammonia-oxidizing activities, such latitudinal factors likely structure communities and soil function across the dry lands surveyed here. Temperature was positively associated with AOA abundance and with the ratio of AOA/AOB, in support of other studies showing that AOA respond preferentially to elevated temperature in enrichment cultures (Kim et al.
2012) and in soil microcosms (Tourna et al.
2008), and correlate well with environmental temperature gradients (Bates et al.
2011; Cao et al.
2011), while some studies show negative or no response to temperature (Adair and Schwartz
2008; Jung et al.
2011). Together with our results, these findings suggest that temperature may be an important driver of niche separation for AOA, potentially leading to diverse ecosystem function responses that will depend on the magnitude of temperature change in the environment.
Based on previously reported qPCR determinations of 16S rRNA gene copy numbers for archaea from the same sample set (Soule et al.
2009), AOA can account but for a small proportion of the extant total population of BSC archaea. Assuming the number of copies per cell for amoA (1 for archaea, 2.5 for bacteria) and 16S rRNA genes (1 for both archaea and bacteria) as can be inferred from known genome studies (Klappenbach et al.
2001; Norton et al.
2002; Hallam et al.
2006; Blainey et al.
2011), putative AOA represent only about ~5% of the archaeal populations present in BSCs across all deserts and as little as 0.03% on average for the Great Basin samples. Even when considering possible uncertainties in these estimates stemming from primer bias (Baker et al.
2003; Agoguè et al.
2008), our results are consistent with other soil environments globally (Lehtovirta et al.
2009; Ochsenreiter et al.
2003; Schleper and Nicol
2010). This clearly implies that the bulk of archaeal populations in BSCs (particularly the few dominant crust phylotypes documented by Soule et al.
2009) cannot be identified as AOA, leaving the functional role for the bulk of BSC archaea as undetermined. While archaea are potentially important for nitrification processes in arid lands, AOA must then be found among the rarer, possibly as yet to be detected, members of BSC microbial communities.