Dataset Information

Soil microorganisms can overcome respiration inhibition by coupling intra- and extracellular metabolism: ¹³C metabolic tracing reveals the mechanisms.

ABSTRACT: CO₂ release from soil is commonly used to estimate toxicity of various substances on microorganisms. However, the mechanisms underlying persistent CO₂ release from soil exposed to toxicants inhibiting microbial respiration, for example, sodium azide (NaN₃) or heavy metals (Cd, Hg, Cu), remain unclear. To unravel these mechanisms, NaN₃-amended soil was incubated with position-specifically ¹³C-labeled glucose and ¹³C was quantified in CO₂, bulk soil, microbial biomass and phospholipid fatty acids (PLFAs). High ¹³C recovery from C-1 in CO₂ indicates that glucose was predominantly metabolized via the pentose phosphate pathway irrespective of inhibition. Although NaN₃ prevented ¹³C incorporation into PLFA and decreased total CO₂ release, ¹³C in CO₂ increased by 12% compared with control soils due to an increased use of glucose for energy production. The allocation of glucose-derived carbon towards extracellular compounds, demonstrated by a fivefold higher ¹³C recovery in bulk soil than in microbial biomass, suggests the synthesis of redox active substances for extracellular disposal of electrons to bypass inhibited electron transport chains within the cells. PLFA content doubled within 10 days of inhibition, demonstrating recovery of the microbial community. This growth was largely based on recycling of cost-intensive biomass compounds, for example, alkyl chains, from microbial necromass. The bypass of intracellular toxicity by extracellular electron transport permits the fast recovery of the microbial community. Such efficient strategies to overcome exposure to respiration-inhibiting toxicants may be exclusive to habitats containing redox-sensitive substances. Therefore, the toxic effects of respiration inhibitors on microorganisms are much less intensive in soils than in pure cultures.

SUBMITTER: K Bore E

PROVIDER: S-EPMC5437355 | biostudies-literature | 2017 Jun

REPOSITORIES: biostudies-literature

ACCESS DATA

Publications

Soil microorganisms can overcome respiration inhibition by coupling intra- and extracellular metabolism: 13C metabolic tracing reveals the mechanisms.

K Bore Ezekiel E Apostel Carolin C Halicki Sara S Kuzyakov Yakov Y Dippold Michaela A MA

The ISME journal 20170203 6

CO2 release from soil is commonly used to estimate toxicity of various substances on microorganisms. However, the mechanisms underlying persistent CO2 release from soil exposed to toxicants inhibiting microbial respiration, for example, sodium azide (NaN3) or heavy metals (Cd, Hg, Cu), remain unclear. To unravel these mechanisms, NaN3-amended soil was incubated with position-specifically 13C-labeled glucose and 13C was quantified ...[more]

PMID: 28157187

Similar Datasets

Project description:Because of severe abiotic limitations, Antarctic soils represent simplified ecosystems, where microorganisms are the principle drivers of nutrient cycling. This relative simplicity makes these ecosystems particularly vulnerable to perturbations, like global warming, and the Antarctic Peninsula is among the most rapidly warming regions on the planet. However, the consequences of the ongoing warming of Antarctica on microorganisms and the processes they mediate are unknown. Here, using 16S rRNA gene pyrosequencing and qPCR, we report a number of highly consistent changes in microbial community structure and abundance across very disparate sub-Antarctic and Antarctic environments following three years of experimental field warming (+ 0.5-2°C). Specifically, we found significant increases in the abundance of fungi and bacteria and in the Alphaproteobacteria-to-Acidobacteria ratio. These alterations were linked to a significant increase in soil respiration. Furthermore, the shifts toward generalist or opportunistic bacterial communities following warming weakened the linkage between bacterial diversity and functional diversity. Warming also increased the abundance of some organisms related to the N-cycle, detected as an increase in the relative abundance of nitrogenase genes via GeoChip microarray analyses. Our results demonstrate that soil microorganisms across a range of sub-Antarctic and Antarctic environments can respond consistently and rapidly to increasing temperatures, thereby potentially disrupting soil functioning. We conducted in situ warming experiments for three years using open-top chambers (OTCs) at one sub-Antarctic (Falkland Islands, 52ºS) and two Antarctic locations (Signy and Anchorage Islands, 60ºS and 67ºS respectively) (see Supplementary Fig. 1 for a map). OTCs increased annual soil temperature by an average of 0.8°C (at a depth of 5 cm), resulting in 8-43% increase in positive-degree days annually and a decrease in freeze-thaw cycle frequency by an average of 15 cycles per year (8). At each location, we included densely vegetated and bare fell-field soils in the experimental design for a total of six environments. Densely vegetated and bare environments represent two contrasting environments for Antarctic soil microorganisms, with large differences in terms of C and N inputs to soils. Massively parallel pyrosequencing (Roche 454 GS FLX Titanium) of 16S rRNA gene amplicons was used to follow bacterial diversity and community composition [GenBank Accession Numbers: HM641909-HM744649], and functional gene microarrays (GeoChip 2.0)(11) were used to assess changes in functional gene distribution. Bacterial and fungal communities were also quantified using real-time PCR.

Project description:Abstract Litter inputs can influence soil respiration directly through labile C availability and, indirectly, through the activity of soil microorganisms and modifications in soil microclimate; however, their relative contributions and the magnitude of any effect remain poorly understood. We synthesized 66 recently published papers on forest ecosystems using a meta?analysis approach to investigate the effect of litter inputs on soil respiration and the underlying mechanisms involved. Our results showed that litter inputs had a strong positive impact on soil respiration, labile C availability, and the abundance of soil microorganisms, with less of an impact related to soil moisture and temperature. Overall, soil respiration was increased by 36% and 55%, respectively, in response to natural and doubled litter inputs. The increase in soil respiration induced by litter inputs showed a tendency for coniferous forests (50.7%)> broad?leaved forests (41.3%)> mixed forests (31.9%). This stimulation effect also depended on stand age with 30? to 100?year?old forests (53.3%) and ?100?year?old forests (50.2%) both 1.5 times larger than ?30?year?old forests (34.5%). Soil microbial biomass carbon and soil dissolved organic carbon increased by 21.0%?33.6% and 60.3%?87.7%, respectively, in response to natural and doubled litter inputs, while soil respiration increased linearly with corresponding increases in soil microbial biomass carbon and soil dissolved organic carbon. Natural and doubled litter inputs increased the total phospholipid fatty acid (PLFA) content by 6.6% and 19.7%, respectively, but decreased the fungal/bacterial PLFA ratio by 26.9% and 18.7%, respectively. Soil respiration also increased linearly with increases in total PLFA and decreased linearly with decreases in the fungal/bacterial PLFA ratio. The contribution of litter inputs to an increase in soil respiration showed a trend of total PLFA > fungal/bacterial PLFA ratio > soil dissolved organic carbon > soil microbial biomass carbon. Therefore, in addition to forest type and stand age, labile C availability and soil microorganisms are also important factors that influence soil respiration in response to litter inputs, with soil microorganisms being more important than labile C availability. Soil respiration, labile C availability, and soil microorganisms (e.g., microbial quantity and community structure) were significantly influenced by litter inputs. The increase in soil respiration in response to litter inputs was closely related to labile C availability and soil microorganisms. Soil microorganisms had a greater effect than labile C availability influence soil respiration in response to litter inputs.

Project description:Phenanthrene-metabolizing soil microbial communities were characterized by examining mineralization of [(14)C]phenanthrene, by most-probable-number (MPN) counting, by 16S-23S spacer DNA analysis of the numerically dominant, culturable phenanthrene-degrading isolates, and by examining incorporation of [(13)C]phenanthrene-derived carbon into sterols and polar lipid fatty acids (PLFAs). An unpolluted agricultural soil, a roadside soil diffusely polluted with polycyclic aromatic hydrocarbons (PAHs), and two highly PAH-polluted soils from industrial sites were analyzed. Microbial phenanthrene degraders were not detected by MPN counting in the agricultural soil and the roadside soil. In the industrial soils, phenanthrene degraders constituted 0.04 and 3.6% of the total number of CFU. 16S-23S spacer DNA analysis followed by partial 16S DNA sequencing of representative isolates from one of the industrial soils showed that one-half of the isolates belonged to the genus Sphingomonas and the other half were closely related to an unclassified beta-proteobacterium. The (13)C-PLFA profiles of the two industrial soils were relatively similar and resembled the profiles of phenanthrene-degrading Sphingomonas reference strains and unclassified beta-proteobacterium isolates but did not match the profiles of Pseudomonas, Mycobacterium, or Nocardia reference strains. The (13)C-PLFA profiles of phenanthrene degraders in the agricultural soil and the roadside soil were different from each other and different from the profiles of the highly polluted industrial soils. Only in the roadside soil were 10me/12me18:0 PLFAs enriched in (13)C, suggesting that actinomycetes metabolized phenanthrene in this soil. The (13)C-PLFA profiles of the unpolluted agricultural soil did not resemble the profiles of any of the reference strains. In all of the soils investigated, no excess (13)C was recovered in the 18:2omega6,9 PLFA, suggesting that fungi did not contribute significantly to assimilation of [(13)C]phenanthrene.

Project description:Grazing exclusion is an effective management practice to restore grassland ecosystem functioning. However, little is known about the role of soil microbial communities in regulating grassland ecosystem functioning during long-term ecosystem restorations. We evaluated the recovery of a degraded semiarid grassland ecosystem in northern China by investigating plant and soil characteristics and the role of soil microbial communities in ecosystem functioning after 22 years of grazing exclusion. Grazing exclusion significantly increased the alpha diversity and changed the community structure of bacteria, but did not significantly affect the alpha diversity or community structure of fungi. The higher abundance of copiotrophic Proteobacteria and Bacteroidetes with grazing exclusion was due to the higher carbon and nutrient concentrations in the soil, whereas the high abundance of Acidobacteria in overgrazed soils was likely an adaptation to the poor environmental conditions. Bacteria of the Sphingomonadaceae family were associated with C cycling under grazing exclusion. Bacteria of the Nitrospiraceae family, and especially of the Nitrospira genus, played an important role in changes to the N cycle under long-term exclusion of grazing. Quantitative PCR further revealed that grazing exclusion significantly increased the abundance of nitrogen fixing bacteria (nifH), ammonia oxidizers (AOA and AOB), and denitrifying bacteria (nirK and nosZ1). Denitrifying enzyme activity (DEA) was positively correlated with abundance of denitrifying bacteria. The increase in DEA under grazing exclusion suggests that the dependence of DEA on the availability of NO3 - produced is due to the combined activity of ammonia oxidizers and denitrifiers. Our findings indicate that decades-long grazing exclusion can trigger changes in the soil bacterial diversity and composition, thus modulating the restoration of grassland ecosystem functions, carbon sequestration and soil fertility.

Dataset Information

Soil microorganisms can overcome respiration inhibition by coupling intra- and extracellular metabolism: ¹³C metabolic tracing reveals the mechanisms.

Publications

Soil microorganisms can overcome respiration inhibition by coupling intra- and extracellular metabolism: <sup>13</sup>C metabolic tracing reveals the mechanisms.

Similar Datasets

OmicsDI is part of the ELIXIR infrastructure

Tweets