Ecological and Genomic Attributes of Novel Bacterial Taxa That Thrive in Subsurface Soil Horizons
Tess E. Brewer,
Emma L. Aronson,
Keshav Arogyaswamy,
Sharon A. Billings,
Jon K. Botthoff,
Ashley N. Campbell,
Nicholas C. Dove,
Dawson Fairbanks,
Rachel E. Gallery,
Stephen C. Hart,
Jason Kaye,
Gary King,
Geoffrey Logan,
Kathleen A. Lohse,
Mia R. Maltz,
Emilio Mayorga,
Caitlin O’Neill,
Sarah M. Owens,
Aaron Packman,
Jennifer Pett-Ridge,
Alain F. Plante,
Daniel D. Richter,
Whendee L. Silver,
Wendy H. Yang,
Noah Fierer
Affiliations
Tess E. Brewer
Cooperative Institute for Research in Environmental Sciences and Department of Molecular, Cellular, and Developmental Biology, University of Colorado, Boulder, Colorado, USA
Emma L. Aronson
Department of Microbiology and Plant Pathology, University of California, Riverside, California, USA
Keshav Arogyaswamy
Department of Microbiology and Plant Pathology, University of California, Riverside, California, USA
Sharon A. Billings
Department of Ecology and Evolutionary Biology, Kansas Biological Survey, University of Kansas, Lawrence, Kansas, USA
Jon K. Botthoff
Center for Conservation Biology, University of California, Riverside, California, USA
Ashley N. Campbell
Physical and Life Sciences Directorate, Lawrence Livermore National Laboratory, Livermore, California, USA
Nicholas C. Dove
Environmental Systems Graduate Group, University of California, Merced, California, USA
Dawson Fairbanks
Department of Soil, Water and Environmental Science, University of Arizona, Tucson, Arizona, USA
Rachel E. Gallery
School of Natural Resources and the Environment, Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, Arizona, USA
Stephen C. Hart
Department of Life & Environmental Sciences, Sierra Nevada Research Institute, University of California, Merced, California, USA
Jason Kaye
Department of Ecosystem Science and Management, Pennsylvania State University, University Park, Pennsylvania, USA
Gary King
Department of Biological Sciences, Louisiana State University, Baton Rouge, Louisiana, USA
Geoffrey Logan
Department of Microbiology and Plant Pathology, University of California, Riverside, California, USA
Kathleen A. Lohse
Department of Biological Sciences, Idaho State University, Pocatello, Idaho, USA
Mia R. Maltz
Center for Conservation Biology, University of California, Riverside, California, USA
Emilio Mayorga
Applied Physics Laboratory, University of Washington, Seattle, Washington, USA
Caitlin O’Neill
Department of Plant Biology, University of Illinois at Urbana Champaign, Urbana, Illinois, USA
Sarah M. Owens
Biosciences Division, Argonne National Laboratory, Argonne, Illinois, USA
Aaron Packman
Civil and Environmental Engineering, Northwestern University, Evanston, Illinois, USA
Jennifer Pett-Ridge
Physical and Life Sciences Directorate, Lawrence Livermore National Laboratory, Livermore, California, USA
Alain F. Plante
Department of Earth & Environmental Science, University of Pennsylvania, Philadelphia, Pennsylvania, USA
Daniel D. Richter
Nicholas School of the Environment, Duke University, Durham, North Carolina, USA
Whendee L. Silver
Department of Environmental Science, Policy, and Management, University of California, Berkeley, California, USA
Wendy H. Yang
Departments of Plant Biology and Geology, University of Illinois at Urbana-Champaign, Urbana, Illinois, USA
Noah Fierer
Department of Ecology and Evolutionary Biology, Cooperative Institute for Research in Environmental Sciences, University of Colorado, Boulder, Colorado, USA
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.
