Examining the global distribution of dominant archaeal populations in soil

Abstract

Archaea, primarily Crenarchaeota, are common in soil; however, the structure of soil archaeal communities and the factors regulating their diversity and abundance remain poorly understood. Here, we used barcoded pyrosequencing to comprehensively survey archaeal and bacterial communities in 146 soils, representing a multitude of soil and ecosystem types from across the globe. Relative archaeal abundance, the percentage of all 16S rRNA gene sequences recovered that were archaeal, averaged 2% across all soils and ranged from 0% to >10% in individual soils. Soil C:N ratio was the only factor consistently correlated with archaeal relative abundances, being higher in soils with lower C:N ratios. Soil archaea communities were dominated by just two phylotypes from a constrained clade within the Crenarchaeota, which together accounted for >70% of all archaeal sequences obtained in the survey. As one of these phylotypes was closely related to a previously identified putative ammonia oxidizer, we sampled from two long-term nitrogen (N) addition experiments to determine if this taxon responds to experimental manipulations of N availability. Contrary to expectations, the abundance of this dominant taxon, as well as archaea overall, tended to decline with increasing N. This trend was coupled with a concurrent increase in known N-oxidizing bacteria, suggesting competitive interactions between these groups.

Figure 1

Neighbor-joining tree based on the alignment of 16S rRNA gene sequences (∼250-bp long) showing the relationship between archaeal phylotypes (PT) recovered from samples of 146 soils by pyrosequencing. The dominant soil Crenarchaeota (DSC1 and DSC2) are indicated along with a basic classification for clades within the Archaea. Sequences of representative archaeal isolates (and clone 54d9) have been included and their GenBank accession numbers are given. For simplicity, some well-supported clades have been collapsed at their nodes. The tree is rooted with a bacterial phylotype (PT 01742) recovered in our study and consensus bootstrap confidence levels are indicated if >60%.

Figure 2

Relative archaeal abundances (on the y axis as archaeal % of all 16S rRNA gene sequences in each sample) grouped by general biome for each of the non-experimental soil samples (those excluding experimental N addition sites at CC and KBS; ^*soil samples used for clone libraries). The portions represented by the dominant soil Crenarchaeota (DSC1 and DSC2) as well as for remaining Crenarchaeotal and Euryarchaeotal phylotypes are indicated. More specific biome vegetation/climate classes are given on the x axis, as is the site of origin for each sample. AGF, agricultural field; ACF, arid/semi-arid conifer forest; ABF, arid/semi-arid broadleaf forest; ADL, arid/semi-arid desert land; AGL, arid/semi-arid grassland; ASL, arid/semi-arid shrubland; HCF, humid conifer forest; HBF, humid broadleaf forest; HGL, humid grassland/prairie; PDL, polar desert land; TBF, tropical broadleaf forest; TGL, tropical grassland.

Figure 3

Relative abundances (group % of all 16S rRNA gene sequences in each sample) for archaea and specific groups of bacteria across soils from medium (∼100 kg ha⁻¹ year⁻¹) and high (∼300 kg ha⁻¹ year⁻¹) experimental N addition as well as control plots at CC (a) and KBS (b). The portions represented by the dominant soil crenarchaeota (DSC1 and DSC2) and the remaining Archaea as well as Nitrosomonas/Nitrosospira and Nitrospirae bacterial groups are indicated (actual mean values and s.d. are reported in Supplementary Table S2). Significant difference (P<0.5) in relative abundances between the control and N addition plots is indicated with an asterisk (^*).