Ecological and Genomic Attributes of Novel Bacterial Taxa That Thrive in Subsurface Soil Horizons

Abstract

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.

Identifying Mechanisms for Successful Ecological Restoration with Salvaged Topsoil in Coastal Sage Scrub Communities

“…Although soil profiles are rarely homogenous, soil thickness or depth in the soil profile has been an important gradient structuring root distribution and bacterial community composition and functioning [85]. A recent study by Brewer et al (2019) illustrated that bacterial attributes associated with microbial survival in oligotrophic conditions may promote their survival and capacity to thrive in subsurface soil horizons. Furthermore, microbial communities at depth were more dissimilar to surface microbial communities, along with greater distance from the surface within a soil profile [86].…”

“…A recent study by Brewer et al (2019) illustrated that bacterial attributes associated with microbial survival in oligotrophic conditions may promote their survival and capacity to thrive in subsurface soil horizons. Furthermore, microbial communities at depth were more dissimilar to surface microbial communities, along with greater distance from the surface within a soil profile [86]. Our study examined how microbial (AMF) communities and bacterial abundance shifts with topsoil thickness in recipient sites receiving topsoil from a reference coastal sage scrub ecosystem.…”

Influence of Substrate Concentration on the Culturability of Heterotrophic Soil Microbes Isolated by High-Throughput Dilution-to-Extinction Cultivation

“…The temperature and soil moisture of subsurface soils are also less variable than those of shallower soils that are exposed to seasonal changes in temperature and precipitation (10). These relatively stable and low-nutrient conditions found at depth constrain both the amount of microbial biomass present in the subsurface and the structure of these microbial communities (11)(12)(13)(14). Many of the microbial taxa that are abundant in these subsurface environments are underrepresented in microbial culture and genome databases (11).…”

Microbial Life Deep Underfoot

“…While some of these genes can be lost through relaxed selection, it appears that ϳ30 sporulation genes are required to produce a viable spore (4). Brewer et al (1) recovered only 15 and 19 sporulation genes in their two draft genomes (ϳ70% assembly), and some of the critical transcription factors that coordinate the complex developmental process were not found. Nevertheless, in a cultivation-independent assay, the authors demonstrated that Dormibacteraeota tolerated ethanol exposure, which was hypothesized to kill off vegetative cells but not spores.…”

“…The study by Brewer et al (1) showcases a novel dimension of soil microbial biodiversity. While bacteria in deep soils are less abundant and active than assemblages found in surface soils, they nevertheless conduct unique biogeochemical processes that contribute to further development of the soil environment.…”