Dataset Information

Dynamic utilization of low-molecular-weight organic substrates across a microbial growth rate gradient

ABSTRACT:

AIM: Low-molecular-weight organic substances (LMWOSs) are at the nexus between micro-organisms, plant roots, detritus and the soil mineral matrix. The nominal oxidation state of carbon (NOSC) has been suggested as a potential parameter for modelling microbial uptake rates of LMWOSs and the efficiency of carbon incorporation into new biomass.

METHODS AND RESULTS: In this study, we assessed the role of compound class and oxidation state on uptake kinetics and substrate-specific carbon use efficiency (SUE) during the growth of three model soil micro-organisms, a fungal isolate (Penicillium spinulosum) and two bacterial isolates (Paraburkholderia solitsugae, and Ralstonia pickettii). Isolates were chosen that spanned a growth rate gradient (0.046-0.316 h-1) in media containing 34 common LMWOSs at realistically low initial concentrations (25 μM each). Clustered, co-utilization of LMWOSs occurred for all three organisms. Potential trends (p < 0.05) for early utilization of more oxidized substrates were present for the two bacterial isolates (P. solitsugae and R. pickettii), but high variability (R2 < 0.15) and a small effect of NOSC indicate these relationships are not useful for prediction. The SUEs of selected substrates ranged from 0.16 to 0.99 and there was no observed relationship between NOSC and SUE.

CONCLUSION: Our results do not provide compelling population-level support for NOSC as a predictive tool for either uptake kinetics or the efficiency of use of LMWOS in soil solution.

SIGNIFICANCE AND IMPACT OF THE STUDY: Metabolic strategies of organisms are likely more important than chemical identity in determining LMWOS cycling in soils. Previous community-level observations may be biased towards fast-responding bacterial community members.

INSTRUMENT(S): Liquid Chromatography MS - negative - reverse phase, Liquid Chromatography MS - alternating - hilic, Nuclear Magnetic Resonance (NMR) -

SUBMITTER: Taylor Cyle

PROVIDER: MTBLS3558 | MetaboLights | 2023-08-14

REPOSITORIES: MetaboLights

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Dynamic utilization of low-molecular-weight organic substrates across a microbial growth rate gradient.

Cyle K Taylor KT Klein Annaleise R AR Aristilde Ludmilla L Martínez Carmen Enid CE

Journal of applied microbiology 20220622 3

<h4>Aim</h4>Low-molecular-weight organic substances (LMWOSs) are at the nexus between micro-organisms, plant roots, detritus, and the soil mineral matrix. The nominal oxidation state of carbon (NOSC) has been suggested as a potential parameter for modelling microbial uptake rates of LMWOSs and the efficiency of carbon incorporation into new biomass.<h4>Methods and results</h4>In this study, we assessed the role of compound class and oxidation state on uptake kinetics and substrate-specific carbo ...[more]

PMID: 35665577

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Project description:<p>We used time-resolved metabolic footprinting, an important technical approach used to monitor changes in extracellular compound concentrations during microbial growth, to study the order of substrate utilization (i.e., substrate preferences) and kinetics of a fast-growing soil isolate, <em>Paraburkholderia</em> sp. strain 1N. The growth of <em>Paraburkholderia</em> sp. 1N was monitored under aerobic conditions in a soil-extracted solubilized organic matter medium, representing a realistic diversity of available substrates and gradient of initial concentrations. We combined multiple analytical approaches to track over 150 compounds in the medium and complemented this with bulk carbon and nitrogen measurements, allowing estimates of carbon use efficiency throughout the growth curve. Targeted methods allowed the quantification of common low-molecular-weight substrates: glucose, 20 amino acids, and 9 organic acids. All targeted compounds were depleted from the medium, and depletion followed a sigmoidal curve where sufficient data were available. Substrates were utilized in at least three distinct temporal clusters as <em>Paraburkholderia</em> sp. 1N produced biomass at a cumulative carbon use efficiency of 0.43. The two substrates with highest initial concentrations, glucose and valine, exhibited longer usage windows, at higher biomass-normalized rates, and later in the growth curve. Contrary to hypotheses based on previous studies, we found no clear relationship between substrate nominal oxidation state of carbon (NOSC) or maximal growth rate and the order of substrate depletion. Under soil solution conditions, the growth of <em>Paraburkholderia</em> sp. 1N induced multiauxic substrate depletion patterns that could not be explained by the traditional paradigm of catabolite repression.</p><p><strong>IMPORTANCE:</strong> Exometabolomic footprinting methods have the capability to provide time-resolved observations of the uptake and release of hundreds of compounds during microbial growth. Of particular interest is microbial phenotyping under environmentally relevant soil conditions, consisting of relatively low concentrations and modeling pulse input events. Here, we show that growth of a bacterial soil isolate, <em>Paraburkholderia</em> sp. 1N, on a dilute soil extract resulted in a multiauxic metabolic response, characterized by discrete temporal clusters of substrate depletion and metabolite production. Our data did not support the hypothesis that compounds with lower energy content are used preferentially, as each cluster contained compounds with a range of nominal oxidation states of carbon. These new findings with <em>Paraburkholderia</em> sp. 1N, which belongs to a metabolically diverse genus, provide insights on ecological strategies employed by aerobic heterotrophs competing for low-molecular-weight substrates in soil solution.</p>

Project description:The goal of this project was to screen soil samples for bacteria that may harbor B. anthracis virulence-associated genes (VAGs). There is currently no information about the prevalence of these types of organisms in the environment. Due to increased environmental monitoring of select agents by programs such as BioWatch and biodetection systems in place at the United States Post Offices and Department of State locations, it has become critical that we not only better understand the natural range of B. anthracis but also how widespread B. anthracis virulence genes are in environmental communities. Naturally occurring isolates containing the B. anthracis virulence genes could generate false-positive results in tests that detect the anthrax toxins, capsule or their associated genes. Understanding the true diversity and pathogenic potential of Bacillus spp. and particularly the B. cereus group is crucial not only in terms of understanding data from environmental monitoring but also diagnosing patients with clinical presentations similar to anthrax in the future. Severe and fatal disease caused by strains similar to B. anthracis could unnecessarily initiate emergency responses if anthrax was incorrectly suspected. Conversely, these strains may be used as bioterror agents requiring science-based responses; presently our limited understanding of these organisms does not permit data-driven decision making. We have investigated 700 aerobic sporoform soil isolates obtained from two areas in the Southwest of the US. Soil samples from the first site had been taken from public access land approximately 50 meters across from the work site of a fatal pneumonia case in a welding factory. This took place in year 2003 when B. cereus was isolated from a metal worker. The second site was targeted because of a recent case involving a deceased mule suspected to have died of a B. anthracis infection. Soil samples were initially analyzed at the CDC. Isolates were obtained by heating the soil at 65 degrees Celcius for 30 minutes followed by plating on agar media. All isolates were screened by PCR for the presence of B. anthracis genomic traits such as toxin genes (cya, lef and pag) as well as chromosomal markers. All isolates were also tested for their hemolytic activity as well as phage sensitivity.

Dataset Information

Dynamic utilization of low-molecular-weight organic substrates across a microbial growth rate gradient

Publications

Dynamic utilization of low-molecular-weight organic substrates across a microbial growth rate gradient.

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