scholarly journals Ecophysiological Study of Paraburkholderia sp. Strain 1N under Soil Solution Conditions: Dynamic Substrate Preferences and Characterization of Carbon Use Efficiency

2020 ◽  
Vol 86 (24) ◽  
Author(s):  
K. Taylor Cyle ◽  
Annaleise R. Klein ◽  
Ludmilla Aristilde ◽  
Carmen Enid Martínez
Keyword(s):  
Molecular Weight ◽  
Soil Solution ◽  
Growth Curve ◽  
Microbial Growth ◽  
Low Molecular Weight ◽  
Time Resolved ◽  
Carbon Use Efficiency ◽  
Substrate Preferences ◽  
Soil Isolate ◽  
Use Efficiency

ABSTRACT 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, Paraburkholderia sp. strain 1N. The growth of Paraburkholderia 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 Paraburkholderia 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 Paraburkholderia sp. 1N induced multiauxic substrate depletion patterns that could not be explained by the traditional paradigm of catabolite repression. IMPORTANCE 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, Paraburkholderia 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 Paraburkholderia 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.

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

2021 ◽  
Author(s):  
K. Taylor Cyle ◽  
Annaleise R. Klein ◽  
Ludmilla Aristilde ◽  
Carmen Enid Martínez
Keyword(s):  
Molecular Weight ◽  
Growth Rate ◽  
Soil Solution ◽  
Oxidation State ◽  
Fungal Isolate ◽  
Chemical Characteristics ◽  
Low Molecular Weight ◽  
Bacterial Isolates ◽  
Ralstonia Pickettii ◽  
Use Efficiency

AbstractConstantly in flux, low-molecular-weight organic substances (LMWOSs) are at the nexus between microorganisms, plant roots, detritus, and the soil mineral matrix. Nominal oxidation state of carbon (NOSC) has been put forward as one way to parameterize microbial uptake rates of LMWOSs and efficiency of carbon incorporation into new biomass. In this study, we employed an ecophysiological approach to test these proposed relationships using targeted exometabolomics (1H-NMR, HR-LCMS) coupled with stable isotope (13C) probing. 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 microorganisms (Penicillium spinulosum, Paraburkholderia solitsugae, and Ralstonia pickettii) in media containing 34 common LMWOSs. Microbial isolates were chosen to span a gradient in growth rate (0.046-0.316 hr−1) and differ phylogenetically (a fungal isolate and two bacterial isolates). Clustered, co-utilization of LMWOSs occured for all three organisms, but temporal cluster separation was most apparent for P. solitsugae. 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 are not useful relationships for prediction. The SUEs ranged from 0.16-0.99 and the hypothesized inverse relationship between NOSC and SUE was not observed. Thus, our results do not provide compelling support for NOSC as a predictive tool, implying that metabolic strategies of organisms may be more important than chemical identity in determining LMWOS cycling in soils.ImportanceCommunity-level observations from soils indicate that low-molecular-weight compounds of higher oxidation state tend to be depleted from soil solution faster and incorporated less efficiently into microbial biomass under oxic conditions. Here, we tested hypothetical relationships between substrate chemical characteristics and the order of substrate utilization by aerobic heterotrophs at the population-level in culture, using two bacterial isolates (Ralstonia pickettii and Paraburkholderia solitsugae) and one fungal isolate from soil (Penicillium spinulosum). We found weak relationships indicating earlier uptake of more oxidized substrates by the two bacterial isolates but no relationship for the fungal isolate. We found no relationship between substrate identity and substrate use efficiency. Our findings indicate that substrate chemical characteristics have limited utility for modeling the depletion of low-molecular-weight organics from soil solution and incorporation into biomass over broader phylogenetic gradients.

Detection of low molecular weight cysteine proteinase inhibitors by time-resolved fluoroimmunoassay

1986 ◽  
Vol 86 (2) ◽  
pp. 243-247 ◽  
Author(s):  
I. Joronen ◽  
V.K. Hopsu-Havu ◽  
M. Manninen ◽  
A. Rinne ◽  
M. Järvinen ◽  
...  
Keyword(s):  
Molecular Weight ◽  
Proteinase Inhibitors ◽  
Cysteine Proteinase ◽  
Low Molecular Weight ◽  
Time Resolved ◽  
Cysteine Proteinase Inhibitors

Rapid turnover of organic acids in a Dystric Brunisol under a spruce–lichen forest in northern Saskatchewan, Canada

2013 ◽  
Vol 93 (3) ◽  
pp. 295-304 ◽  
Author(s):  
Kazumichi Fujii ◽  
Kokoro Morioka ◽  
Ryan Hangs ◽  
Shinya Funakawa ◽  
Takashi Kosaki ◽  
...  
Keyword(s):  
Molecular Weight ◽  
Organic Acids ◽  
Soil Solution ◽  
Surface Soil ◽  
Microbial Respiration ◽  
Mineral Weathering ◽  
Low Molecular Weight ◽  
Rapid Turnover ◽  
C Cycle ◽  
Northern Saskatchewan

Fujii, K., Morioka, K., Hangs, R., Funakawa, S., Kosaki, and Anderson, D. W. 2013. Rapid turnover of organic acids in a Dystric Brunisol under a spruce–lichen forest in northern Saskatchewan, Canada. Can. J. Soil Sci. 93: 295–304. Organic acids released by lichen play an important role in mineral weathering and podzolization in the Boreal–Tundra transition zone of Canada; however, importance of low-molecular-weight organic acids in the soil carbon (C) cycle in the black spruce–lichen forests remains unclear. We examined soil solution composition and mineralization kinetics of 14C-radiolabelled oxalate and citrate to quantify the C fluxes from organic acid mineralization in a Dystric Brunisol under a spruce–lichen forest in northern Saskatchewan. Oxalate concentration in soil solution was greatest in the lichen layer, while the high levels of citrate were observed in the lichen and organic (O) layers to the Ae horizon with the lowest sorption capacity. Oxalate and citrate were rapidly mineralized within the lichen and O layers and had short mean residence times (0.5 to 2.7 h). Substantial C fluxes due to citrate mineralization were observed both within the lichen and O layers, but oxalate mineralization led to C flux in the lichen layer only. The contribution of citrate and oxalate to microbial respiration was large (up to 57%) in the surface soil layers. Citrate was the dominant substrate for microbial respiration of the surface soil; however, it appears that oxalate could also be an important microbial substrate within the lichen layer, at least in summer months. We conclude that the exudation of low-molecular-weight organic acids by lichenous fungi, followed by their rapid mineralization, could play an important role in the C cycles of the sandy soils under spruce–lichen forest.

Determination of low molecular weight organic acids in soil solution by HPLC

Talanta ◽  
1999 ◽  
Vol 48 (1) ◽  
pp. 173-179 ◽  
Author(s):  
P VANHEES ◽  
J DAHLEN ◽  
U LUNDSTROM ◽  
H BOREN ◽  
B ALLARD
Keyword(s):  
Molecular Weight ◽  
Organic Acids ◽  
Soil Solution ◽  
Low Molecular Weight

New insights on carbon use efficiency using calorespirometry – a bioenergetics-based model

2020 ◽  
Author(s):  
Arjun Chakrawal ◽  
Anke M. Herrmann ◽  
Stefano Manzoni
Keyword(s):  
Metabolic Pathways ◽  
Microbial Growth ◽  
Energy Content ◽  
Growth Yields ◽  
Balance Model ◽  
Organic C ◽  
Degree Of Reduction ◽  
Carbon Use Efficiency ◽  
Use Efficiency

&lt;p&gt;Soil organic carbon (SOC) represents both a source of energy (catabolism) and a building material for biosynthesis (anabolism) for microorganisms. Microbial carbon use efficiency (CUE) &amp;#8211; the ratio of C used for biosynthesis over C consumed &amp;#8211; measures the partitioning between anabolic and catabolic processes. While most work on CUE has been based on C mass flows, the role of SOC energy content, microbial energy demand, and general energy flows on CUE have been rarely considered. Thus, a bioenergetics perspective on CUE could provide new insights on how microorganisms utilize C substrates and ultimately allow C to be stabilized in soils.&lt;/p&gt;&lt;p&gt;The microbial growth reactions are generally associated with a negative enthalpy change, which results in heat dissipation from the system. This heat can be measured using an isothermal calorimeter, which is often coupled with respiration measurements. This coupled system allows studying energy and C exchanges, and calculating their ratio referred to as the calorespirometric ratio (CR). Here, we formulate a coupled mass and energy balance model for microbial growth and provide a generalized relationship between CUE and CR. In the model, we consider two types of organic C in soils, the added substrate (i.e., glucose) and the native SOC. Furthermore, we assume that glucose is taken up via aerobic (AE) and two fermentation metabolic pathways &amp;#8211; glucose to ethanol (F1) and glucose to lactic acid (F2); for simplicity, only aerobic growth on the native SOC was adopted. We use this model as a framework to generalize previous formulations and generate hypotheses on the expected variations in CR as a function of substrate type, metabolic pathways, and microbial properties (specifically CUE). In turn, the same equations can be used to estimate CUE from measured CR.&lt;/p&gt;&lt;p&gt;Our results show that in a non-growing system, CR depends only on the rates of different metabolic pathways (AE, F1, and F2). While in growing systems, CR is a function of rates as well as growth yields for these metabolic pathways. Under purely aerobic conditions, our model predicts that CUE increases with increasing CR when the degree of reduction of the substrate is higher than that of the microbial biomass. Similarly, CUE decreases with increasing CR when the degree of reduction of substrate is lower than that of the biomass. In the case of combined metabolism &amp;#8211; aerobic and fermentation simultaneously &amp;#8211; CUE is not only a function of CR and the degree of reduction of substrates but also the rates and growth yields of all metabolic pathways involved. To summarize, in this contribution we illustrate how calorespirometry can become an efficient tool to evaluate CUE and the role of different metabolic pathways in soil systems.&lt;/p&gt;

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