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Proteogenomic analyses indicate bacterial methylotrophy and archaeal heterotrophy are prevalent below the grass root zone.

ABSTRACT: Annually, half of all plant-derived carbon is added to soil where it is microbially respired to CO₂. However, understanding of the microbiology of this process is limited because most culture-independent methods cannot link metabolic processes to the organisms present, and this link to causative agents is necessary to predict the results of perturbations on the system. We collected soil samples at two sub-root depths (10-20 cm and 30-40 cm) before and after a rainfall-driven nutrient perturbation event in a Northern California grassland that experiences a Mediterranean climate. From ten samples, we reconstructed 198 metagenome-assembled genomes that represent all major phylotypes. We also quantified 6,835 proteins and 175 metabolites and showed that after the rain event the concentrations of many sugars and amino acids approach zero at the base of the soil profile. Unexpectedly, the genomes of novel members of the Gemmatimonadetes and Candidate Phylum Rokubacteria phyla encode pathways for methylotrophy. We infer that these abundant organisms contribute substantially to carbon turnover in the soil, given that methylotrophy proteins were among the most abundant proteins in the proteome. Previously undescribed Bathyarchaeota and Thermoplasmatales archaea are abundant in deeper soil horizons and are inferred to contribute appreciably to aromatic amino acid degradation. Many of the other bacteria appear to breakdown other components of plant biomass, as evidenced by the prevalence of various sugar and amino acid transporters and corresponding hydrolyzing machinery in the proteome. Overall, our work provides organism-resolved insight into the spatial distribution of bacteria and archaea whose activities combine to degrade plant-derived organics, limiting the transport of methanol, amino acids and sugars into underlying weathered rock. The new insights into the soil carbon cycle during an intense period of carbon turnover, including biogeochemical roles to previously little known soil microbes, were made possible via the combination of metagenomics, proteomics, and metabolomics.

SUBMITTER: Butterfield CN

PROVIDER: S-EPMC5103831 | biostudies-literature | 2016

REPOSITORIES: biostudies-literature

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Proteogenomic analyses indicate bacterial methylotrophy and archaeal heterotrophy are prevalent below the grass root zone.

Butterfield Cristina N CN Li Zhou Z Andeer Peter F PF Spaulding Susan S Thomas Brian C BC Singh Andrea A Hettich Robert L RL Suttle Kenwyn B KB Probst Alexander J AJ Tringe Susannah G SG Northen Trent T Pan Chongle C Banfield Jillian F JF

PeerJ 20161108

Annually, half of all plant-derived carbon is added to soil where it is microbially respired to CO<sub>2</sub>. However, understanding of the microbiology of this process is limited because most culture-independent methods cannot link metabolic processes to the organisms present, and this link to causative agents is necessary to predict the results of perturbations on the system. We collected soil samples at two sub-root depths (10-20 cm and 30-40 cm) before and after a rainfall-driven nutrient ...[more]

PMID: 27843720

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Project description:BACKGROUND AND AIMS:The perennial C4 grass Urochloa humidicola is widely planted on infertile acidic and waterlogging-prone soils of tropical America. Waterlogging results in soil anoxia, and O2 deficiency can reduce nutrient uptake by roots. Interestingly, both nutrient deficiencies and soil waterlogging can enhance root cortical cell senescence, and the increased gas-filled porosity facilitates internal aeration of roots. We tested the influence of nutrient supply and root-zone O2 on root traits, leaf nutrient concentrations and growth of U. humidicola. METHODS:Plants were grown in pots in a completely randomized design under aerated or stagnant deoxygenated hydroponic conditions and six nutrient regimes, with low to high concentrations of all essential elements, for 28 d in a controlled-temperature greenhouse. The standard acid solution (SAS) used was previously designed based on infertile acidic soils of the tropical America savannas, and step increases in the concentration of SAS were used in aerated or deoxygenated 0.1 % agar solution, which mimics changes in gas composition in waterlogged soils. Measurements included shoot and root growth, root porosity, root anatomy, radial O2 loss, and leaf tissue nutrient concentrations. KEY RESULTS:Shoot dry mass was reduced for plants in stagnant compared with aerated conditions at high, but not at low, levels of mineral nutrition. In low-nutrition stagnant solution, roots were shorter, of greater porosity and had smaller radial thickness of the stele. Suberized lamellae and lignified sclerenchyma, as well as a strong barrier to radial O2 loss, were documented for roots from all treatments. Leaf nutrient concentrations of K, Mg and Ca (but not N, P and S) were higher in aerated than in stagnant conditions. CONCLUSIONS:Under low-nutrient conditions, plant growth in stagnant solution was equal to that in aerated solution, whereas under higher-nutrient regimes growth increased but dry mass in stagnant solution was less than in aerated solution. Slow growth in low-nutrient conditions limited any further response to the low O2 treatment, and greater porosity and smaller stele size in roots would enhance internal O2 movement within roots in the nutrient-limited stagnant conditions. A constitutive barrier to radial O2 loss and aerenchyma facilitates O2 movement to the tips of roots, which presumably contributes to maintaining nutrient uptake and the tolerance of U. humidicola to low O2 in the root-zone.

Dataset Information

Proteogenomic analyses indicate bacterial methylotrophy and archaeal heterotrophy are prevalent below the grass root zone.

Publications

Proteogenomic analyses indicate bacterial methylotrophy and archaeal heterotrophy are prevalent below the grass root zone.

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