While most bacterial and archaeal taxa living in surface soils remain undescribed, this problem is exacerbated in deeper soils, owing to the unique oligotrophic conditions found in the subsurface. Additionally, previous studies of soil microbiomes have focused almost exclusively on surface soils, even though the microbes living in deeper soils also play critical roles in a wide range of biogeochemical processes. We examined soils collected from 20 distinct profiles across the United States to characterize the bacterial and archaeal communities that live in subsurface soils and to determine whether there are consistent changes in soil microbial communities with depth across a wide range of soil and environmental conditions. We found that bacterial and archaeal diversity generally decreased with depth, as did the degree of similarity of microbial communities to those found in surface horizons. We observed five phyla that consistently increased in relative abundance with depth across our soil profiles: Chloroflexi, Nitrospirae, Euryarchaeota, and candidate phyla GAL15 and Dormibacteraeota (formerly AD3). Leveraging the unusually high abundance of Dormibacteraeota at depth, we assembled genomes representative of this candidate phylum and identified traits that are likely to be beneficial in low-nutrient environments, including the synthesis and storage of carbohydrates, the potential to use carbon monoxide (CO) as a supplemental energy source, and the ability to form spores. Together these attributes likely allow members of the candidate phylum Dormibacteraeota to flourish in deeper soils and provide insight into the survival and growth strategies employed by the microbes that thrive in oligotrophic soil environments. IMPORTANCE Soil profiles are rarely homogeneous. Resource availability and microbial abundances typically decrease with soil depth, but microbes found in deeper horizons are still important components of terrestrial ecosystems. By studying 20 soil profiles across the United States, we documented consistent changes in soil bacterial and archaeal communities with depth. Deeper soils harbored communities distinct from those of the more commonly studied surface horizons. Most notably, we found that the candidate phylum Dormibacteraeota (formerly AD3) was often dominant in subsurface soils, and we used genomes from uncultivated members of this group to identify why these taxa are able to thrive in such resource-limited environments. Simply digging deeper into soil can reveal a surprising number of novel microbes with unique adaptations to oligotrophic subsurface conditions.
The efficiency with which microbes use substrate (Carbon Use Efficiency or CUE) to make new microbial biomass is an important variable in soil and ecosystem C cycling models. It is generally assumed that CUE of microbial activity in soils is low, however measured values vary widely. It is hypothesized that high values of CUE observed in especially short-term incubations reflect the build-up of storage compounds in response to a sudden increase in substrate availability and are therefore not representative of CUE of microbial activity in unamended soil. To test this hypothesis, we measured the 13 CO 2 release from six position-specific 13 C-labeled glucose isotopomers in ponderosa pine and piñon-juniper soil. We compared this position-specific CO 2 production pattern with patterns expected for 1) balanced microbial growth (synthesis of all compounds needed to build new microbial cells) at a low, medium, or high CUE, and 2) synthesis of storage compounds (glycogen, tri-palmitoyl-glycerol, and polyhydroxybutyrate). Results of this study show that synthesis of storage compounds is not responsible for the observed high CUE. Instead, it is the position-specific CO 2 production expected for balanced growth and high CUE that best matches the observed CO 2 production pattern in these two soils. Comparison with published studies suggests that the amount of glucose added in this study is too low and the duration of the experiment too short to affect microbial metabolism. We conclude that the hypothesis of high CUE in undisturbed soil remains viable and worthy of further testing.
Chemical stabilization of microbial-derived products such as extracellular enzymes (EE) onto mineral surfaces has gained attention as a possibly important mechanism leading to the persistence of soil organic carbon (SOC). While the controls on EE activities and their stabilization in the surface soil are reasonably well-understood, how these activities change with soil depth and possibly diverge from those at the soil surface due to distinct physical, chemical, and biotic conditions remains unclear. We assessed EE activity to a depth of 1 m (10 cm increments) in 19 soil profiles across the Critical Zone Observatory Network, which represents a wide range of climates, soil orders, and vegetation types. For all EEs, activities per mass of soil correlated positively with microbial biomass (MB) and SOC, and all three of these variables decreased logarithmically with depth (p < 0.05). Across all sites, over half of the potential EE activities per mass soil consistently occurred below 20 cm for all measured EEs. Activities per unit MB or SOC were substantially higher at depth (soils below 20 cm accounted for 80% of whole-profile EE activity), suggesting an accumulation of stabilized (i.e. mineral sorbed) EEs in subsoil horizons. The pronounced enzyme stabilization in subsurface horizons was corroborated by mixed-effects models that showed a significant, positive relationship between clay concentration and MB-normalized EE activities in the subsoil. Furthermore, the negative relationships between soil C, N, and P and C-, N-, and P-acquiring EEs found in the surface soil decoupled below 20 cm, which could have also been caused by EE stabilization. This finding suggests that EEs may not reflect soil nutrient availabilities deeper in the soil profile. Taken together, our results suggest that deeper soil horizons hold a significant reservoir of EEs, and that the controls of subsoil EEs differ from their surface soil counterparts.
While most bacterial and archaeal taxa living in surface soils remain undescribed, 5this problem is exacerbated in deeper soils owing to the unique oligotrophic conditions found in the subsurface.
Harnessing the NEON data revolution to advance open environmental science with a diverse and data-capable community. Ecosphere 12(12):e03833.
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