TY - JOUR
T1 - Mediterranean grassland soil C–N compound turnover is dependent on rainfall and depth, and is mediated by genomically divergent microorganisms
AU - Diamond, Spencer
AU - Andeer, Peter F.
AU - Li, Zhou
AU - Crits-Christoph, Alexander
AU - Burstein, David
AU - Anantharaman, Karthik
AU - Lane, Katherine R.
AU - Thomas, Brian C.
AU - Pan, Chongle
AU - Northen, Trent R.
AU - Banfield, Jillian F.
N1 - Funding Information:
The authors thank S. Spaulding for assistance with fieldwork and E. Starr for helpful discussions on data analysis and figure production. Sequencing was carried out under a Community Sequencing Project at the Joint Genome Institute. Funding was provided by the Office of Science, Office of Biological and Environmental Research, of the US Department of Energy (grant DOE-SC10010566).
Publisher Copyright:
© 2019, The Author(s), under exclusive licence to Springer Nature Limited.
PY - 2019/8
Y1 - 2019/8
N2 - Soil microbial activity drives the carbon and nitrogen cycles and is an important determinant of atmospheric trace gas turnover, yet most soils are dominated by microorganisms with unknown metabolic capacities. Even Acidobacteria, among the most abundant bacteria in soil, remain poorly characterized, and functions across groups such as Verrucomicrobia, Gemmatimonadetes, Chloroflexi and Rokubacteria are understudied. Here, we have resolved 60 metagenomic and 20 proteomic data sets from a Mediterranean grassland soil ecosystem and recovered 793 near-complete microbial genomes from 18 phyla, representing around one-third of all microorganisms detected. Importantly, this enabled extensive genomics-based metabolic predictions for these communities. Acidobacteria from multiple previously unstudied classes have genomes that encode large enzyme complements for complex carbohydrate degradation. Alternatively, most microorganisms encode carbohydrate esterases that strip readily accessible methyl and acetyl groups from polymers like pectin and xylan, forming methanol and acetate, the availability of which could explain the high prevalence of C1 metabolism and acetate utilization in genomes. Microorganism abundances among samples collected at three soil depths and under natural and amended rainfall regimes indicate statistically higher associations of inorganic nitrogen metabolism and carbon degradation in deep and shallow soils, respectively. This partitioning decreased in samples under extended spring rainfall, indicating that long-term climate alteration can affect both carbon and nitrogen cycling. Overall, by leveraging natural and experimental gradients with genome-resolved metabolic profiles, we link microorganisms lacking prior genomic characterization to specific roles in complex carbon, C1, nitrate and ammonia transformations, and constrain factors that impact their distributions in soil.
AB - Soil microbial activity drives the carbon and nitrogen cycles and is an important determinant of atmospheric trace gas turnover, yet most soils are dominated by microorganisms with unknown metabolic capacities. Even Acidobacteria, among the most abundant bacteria in soil, remain poorly characterized, and functions across groups such as Verrucomicrobia, Gemmatimonadetes, Chloroflexi and Rokubacteria are understudied. Here, we have resolved 60 metagenomic and 20 proteomic data sets from a Mediterranean grassland soil ecosystem and recovered 793 near-complete microbial genomes from 18 phyla, representing around one-third of all microorganisms detected. Importantly, this enabled extensive genomics-based metabolic predictions for these communities. Acidobacteria from multiple previously unstudied classes have genomes that encode large enzyme complements for complex carbohydrate degradation. Alternatively, most microorganisms encode carbohydrate esterases that strip readily accessible methyl and acetyl groups from polymers like pectin and xylan, forming methanol and acetate, the availability of which could explain the high prevalence of C1 metabolism and acetate utilization in genomes. Microorganism abundances among samples collected at three soil depths and under natural and amended rainfall regimes indicate statistically higher associations of inorganic nitrogen metabolism and carbon degradation in deep and shallow soils, respectively. This partitioning decreased in samples under extended spring rainfall, indicating that long-term climate alteration can affect both carbon and nitrogen cycling. Overall, by leveraging natural and experimental gradients with genome-resolved metabolic profiles, we link microorganisms lacking prior genomic characterization to specific roles in complex carbon, C1, nitrate and ammonia transformations, and constrain factors that impact their distributions in soil.
UR - http://www.scopus.com/inward/record.url?scp=85066065413&partnerID=8YFLogxK
U2 - 10.1038/s41564-019-0449-y
DO - 10.1038/s41564-019-0449-y
M3 - Article
C2 - 31110364
AN - SCOPUS:85066065413
SN - 2058-5276
VL - 4
SP - 1356
EP - 1367
JO - Nature Microbiology
JF - Nature Microbiology
IS - 8
ER -