Diversification, niche adaptation, and evolution of a candidate phylum thriving in the deep Critical Zone
Abstract
The deep subsurface soil microbiome encompasses a vast amount of understudied phylogenetic diversity and metabolic novelty, and the metabolic capabilities and ecological roles of these communities remain largely unknown. We observed a widespread and relatively abundant bacterial phylum (CSP1-3) in deep soils and evaluated its phylogeny, ecology, metabolism, and evolutionary history. Genome analysis indicated that members of CSP1-3 were actively replicating in situ and were widely involved in the carbon, nitrogen, and sulfur cycles. We identified potential adaptive traits of CSP1-3 members for the oligotrophic deep soil environments, including a mixotrophic lifestyle, flexible energy metabolisms, and conservation pathways. The ancestor of CSP1-3 likely originated in an aquatic environment, subsequently colonizing topsoil and, later, deep soil environments, with major CSP1-3 clades adapted to each of these distinct niches. The transition into the terrestrial environment was associated with genome expansion, including the horizontal acquisition of a range of genes for carbohydrate and energy metabolism and, in one lineage, high-affinity terminal oxidases to support a microaerophilic lifestyle. Our results highlight the ecology and genome evolution of microbes in the deep Critical Zone.
Article Details
Journal Info
Proceedings of the National Academy of Sciences
National Academy of Sciences
Authors (14)
Wenlu Feng
Interdisciplinary Research Center for Soil Microbial Ecology and Land Sustainable Productivity in Dry Areas, Northwest A&F University
Xiaonan Wan
Interdisciplinary Research Center for Soil Microbial Ecology and Land Sustainable Productivity in Dry Areas, Northwest A&F University
Yiran Zhang
John Quensen
Center for Microbial Ecology, Michigan State University
Tom A. Williams
Michael Thompson
Department of Population and Public Health Sciences, Keck School of Medicine, University of Southern California, Los Angeles, CA, USA.
Matthew Streeter
Iowa Geological Survey, The University of Iowa
Yang Zhang
Shuo Jiao
Department of Environmental Science, College of Natural Resources and Environment, Northwest A&F University
Gehong Wei
Department of Microbiology, College of Life Sciences, Northwest A&F University
Yuanjun Zhu
Interdisciplinary Research Center for Soil Microbial Ecology and Land Sustainable Productivity in Dry Areas, Northwest A&F University
Jie Gu
State Key Laboratory of Multiphase Complex Systems, Institute of Process Engineering
James M. Tiedje
Interdisciplinary Research Center for Soil Microbial Ecology and Land Sustainable Productivity in Dry Areas, Northwest A&F University
Xun Qian
Interdisciplinary Research Center for Soil Microbial Ecology and Land Sustainable Productivity in Dry Areas, Northwest A&F University