The impact of combinatorial stress on the growth dynamics and metabolome of Burkholderia mesoacidophila demonstrates the complexity of tolerance mechanisms

Aims The recently sequenced Burkholderia mesoacidophila (previously Pseudomonas mesoacidophila) is a soil organism and as such will be exposed to multiple concurrent stresses in the natural environment. The combinatorial stress potentially experienced by microbes in soil has not been investigated in...

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Published inJournal of applied microbiology Vol. 127; no. 5; pp. 1521 - 1531
Main Authors Moody, S.C., Bull, J.C., Dudley, E., Loveridge, E.J.
Format Journal Article
LanguageEnglish
Published England Oxford University Press 01.11.2019
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ISSN1364-5072
1365-2672
1365-2672
DOI10.1111/jam.14404

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Abstract Aims The recently sequenced Burkholderia mesoacidophila (previously Pseudomonas mesoacidophila) is a soil organism and as such will be exposed to multiple concurrent stresses in the natural environment. The combinatorial stress potentially experienced by microbes in soil has not been investigated in detail. Methods and Results The impact of combinatorial stress on growth was investigated using tripartite variables—temperature, nutritional environment and either osmotic or oxidative stress. In nutritionally stringent conditions, increasing diamide concentration had no effect on growth while increasing H2O2 concentration reduced both growth rate and maximum density. Metabolomic studies with oxidative stress revealed specific (unidentified) metabolites associated with diamide tolerance, and an overwhelming dominance of sugars and sugar alcohols in nutritionally stringent conditions with and without the additional stressor. Conclusions Combinatorial stress tolerance is complex. Temperature had the greatest independent impact on growth, while the impact of the nutritional environment played a key role in oxidative stress tolerance. In nutritionally stringent conditions, the metabolome suggested different tolerance mechanisms for different types of oxidative stress. Significance and Impact of the Study This work demonstrates the specificity of the stress response, and the need to consider multiple environmental factors to meaningfully investigate tolerance. Both environmental and clinical settings subject bacteria to combinatorial stress and this should be considered in the design of further studies.
AbstractList The recently sequenced Burkholderia mesoacidophila (previously Pseudomonas mesoacidophila) is a soil organism and as such will be exposed to multiple concurrent stresses in the natural environment. The combinatorial stress potentially experienced by microbes in soil has not been investigated in detail. The impact of combinatorial stress on growth was investigated using tripartite variables-temperature, nutritional environment and either osmotic or oxidative stress. In nutritionally stringent conditions, increasing diamide concentration had no effect on growth while increasing H O concentration reduced both growth rate and maximum density. Metabolomic studies with oxidative stress revealed specific (unidentified) metabolites associated with diamide tolerance, and an overwhelming dominance of sugars and sugar alcohols in nutritionally stringent conditions with and without the additional stressor. Combinatorial stress tolerance is complex. Temperature had the greatest independent impact on growth, while the impact of the nutritional environment played a key role in oxidative stress tolerance. In nutritionally stringent conditions, the metabolome suggested different tolerance mechanisms for different types of oxidative stress. This work demonstrates the specificity of the stress response, and the need to consider multiple environmental factors to meaningfully investigate tolerance. Both environmental and clinical settings subject bacteria to combinatorial stress and this should be considered in the design of further studies.
Aims The recently sequenced Burkholderia mesoacidophila (previously Pseudomonas mesoacidophila) is a soil organism and as such will be exposed to multiple concurrent stresses in the natural environment. The combinatorial stress potentially experienced by microbes in soil has not been investigated in detail. Methods and Results The impact of combinatorial stress on growth was investigated using tripartite variables—temperature, nutritional environment and either osmotic or oxidative stress. In nutritionally stringent conditions, increasing diamide concentration had no effect on growth while increasing H2O2 concentration reduced both growth rate and maximum density. Metabolomic studies with oxidative stress revealed specific (unidentified) metabolites associated with diamide tolerance, and an overwhelming dominance of sugars and sugar alcohols in nutritionally stringent conditions with and without the additional stressor. Conclusions Combinatorial stress tolerance is complex. Temperature had the greatest independent impact on growth, while the impact of the nutritional environment played a key role in oxidative stress tolerance. In nutritionally stringent conditions, the metabolome suggested different tolerance mechanisms for different types of oxidative stress. Significance and Impact of the Study This work demonstrates the specificity of the stress response, and the need to consider multiple environmental factors to meaningfully investigate tolerance. Both environmental and clinical settings subject bacteria to combinatorial stress and this should be considered in the design of further studies.
AIMS: The recently sequenced Burkholderia mesoacidophila (previously Pseudomonas mesoacidophila) is a soil organism and as such will be exposed to multiple concurrent stresses in the natural environment. The combinatorial stress potentially experienced by microbes in soil has not been investigated in detail. METHODS AND RESULTS: The impact of combinatorial stress on growth was investigated using tripartite variables—temperature, nutritional environment and either osmotic or oxidative stress. In nutritionally stringent conditions, increasing diamide concentration had no effect on growth while increasing H₂O₂ concentration reduced both growth rate and maximum density. Metabolomic studies with oxidative stress revealed specific (unidentified) metabolites associated with diamide tolerance, and an overwhelming dominance of sugars and sugar alcohols in nutritionally stringent conditions with and without the additional stressor. CONCLUSIONS: Combinatorial stress tolerance is complex. Temperature had the greatest independent impact on growth, while the impact of the nutritional environment played a key role in oxidative stress tolerance. In nutritionally stringent conditions, the metabolome suggested different tolerance mechanisms for different types of oxidative stress. SIGNIFICANCE AND IMPACT OF THE STUDY: This work demonstrates the specificity of the stress response, and the need to consider multiple environmental factors to meaningfully investigate tolerance. Both environmental and clinical settings subject bacteria to combinatorial stress and this should be considered in the design of further studies.
AimsThe recently sequenced Burkholderia mesoacidophila (previously Pseudomonas mesoacidophila) is a soil organism and as such will be exposed to multiple concurrent stresses in the natural environment. The combinatorial stress potentially experienced by microbes in soil has not been investigated in detail.Methods and ResultsThe impact of combinatorial stress on growth was investigated using tripartite variables—temperature, nutritional environment and either osmotic or oxidative stress. In nutritionally stringent conditions, increasing diamide concentration had no effect on growth while increasing H2O2 concentration reduced both growth rate and maximum density. Metabolomic studies with oxidative stress revealed specific (unidentified) metabolites associated with diamide tolerance, and an overwhelming dominance of sugars and sugar alcohols in nutritionally stringent conditions with and without the additional stressor.ConclusionsCombinatorial stress tolerance is complex. Temperature had the greatest independent impact on growth, while the impact of the nutritional environment played a key role in oxidative stress tolerance. In nutritionally stringent conditions, the metabolome suggested different tolerance mechanisms for different types of oxidative stress.Significance and Impact of the StudyThis work demonstrates the specificity of the stress response, and the need to consider multiple environmental factors to meaningfully investigate tolerance. Both environmental and clinical settings subject bacteria to combinatorial stress and this should be considered in the design of further studies.
The recently sequenced Burkholderia mesoacidophila (previously Pseudomonas mesoacidophila) is a soil organism and as such will be exposed to multiple concurrent stresses in the natural environment. The combinatorial stress potentially experienced by microbes in soil has not been investigated in detail.AIMSThe recently sequenced Burkholderia mesoacidophila (previously Pseudomonas mesoacidophila) is a soil organism and as such will be exposed to multiple concurrent stresses in the natural environment. The combinatorial stress potentially experienced by microbes in soil has not been investigated in detail.The impact of combinatorial stress on growth was investigated using tripartite variables-temperature, nutritional environment and either osmotic or oxidative stress. In nutritionally stringent conditions, increasing diamide concentration had no effect on growth while increasing H2 O2 concentration reduced both growth rate and maximum density. Metabolomic studies with oxidative stress revealed specific (unidentified) metabolites associated with diamide tolerance, and an overwhelming dominance of sugars and sugar alcohols in nutritionally stringent conditions with and without the additional stressor.METHODS AND RESULTSThe impact of combinatorial stress on growth was investigated using tripartite variables-temperature, nutritional environment and either osmotic or oxidative stress. In nutritionally stringent conditions, increasing diamide concentration had no effect on growth while increasing H2 O2 concentration reduced both growth rate and maximum density. Metabolomic studies with oxidative stress revealed specific (unidentified) metabolites associated with diamide tolerance, and an overwhelming dominance of sugars and sugar alcohols in nutritionally stringent conditions with and without the additional stressor.Combinatorial stress tolerance is complex. Temperature had the greatest independent impact on growth, while the impact of the nutritional environment played a key role in oxidative stress tolerance. In nutritionally stringent conditions, the metabolome suggested different tolerance mechanisms for different types of oxidative stress.CONCLUSIONSCombinatorial stress tolerance is complex. Temperature had the greatest independent impact on growth, while the impact of the nutritional environment played a key role in oxidative stress tolerance. In nutritionally stringent conditions, the metabolome suggested different tolerance mechanisms for different types of oxidative stress.This work demonstrates the specificity of the stress response, and the need to consider multiple environmental factors to meaningfully investigate tolerance. Both environmental and clinical settings subject bacteria to combinatorial stress and this should be considered in the design of further studies.SIGNIFICANCE AND IMPACT OF THE STUDYThis work demonstrates the specificity of the stress response, and the need to consider multiple environmental factors to meaningfully investigate tolerance. Both environmental and clinical settings subject bacteria to combinatorial stress and this should be considered in the design of further studies.
Author Moody, S.C.
Loveridge, E.J.
Dudley, E.
Bull, J.C.
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crossref_primary_10_3390_microorganisms12010040
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Issue 5
Keywords stress tolerance
Burkholderia
metabolome
oxidative stress
growth dynamics
diamide
Language English
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Snippet Aims The recently sequenced Burkholderia mesoacidophila (previously Pseudomonas mesoacidophila) is a soil organism and as such will be exposed to multiple...
The recently sequenced Burkholderia mesoacidophila (previously Pseudomonas mesoacidophila) is a soil organism and as such will be exposed to multiple...
AimsThe recently sequenced Burkholderia mesoacidophila (previously Pseudomonas mesoacidophila) is a soil organism and as such will be exposed to multiple...
AIMS: The recently sequenced Burkholderia mesoacidophila (previously Pseudomonas mesoacidophila) is a soil organism and as such will be exposed to multiple...
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SubjectTerms Alcohols
amides
bacteria
Burkholderia
Burkholderia - growth & development
Burkholderia - isolation & purification
Burkholderia - metabolism
Burkholderia cepacia complex
Combinatorial analysis
Complexity
diamide
Environment
Environmental factors
Environmental impact
growth dynamics
Growth rate
Hydrogen peroxide
Hydrogen Peroxide - metabolism
Metabolites
Metabolome
Metabolomics
Natural environment
Oxidative Stress
Pseudomonas
soil biota
Soil investigations
Soil Microbiology
Soil microorganisms
Soils
stress response
stress tolerance
Stress, Physiological
Sugar
sugar alcohols
Temperature
Temperature tolerance
Title The impact of combinatorial stress on the growth dynamics and metabolome of Burkholderia mesoacidophila demonstrates the complexity of tolerance mechanisms
URI https://onlinelibrary.wiley.com/doi/abs/10.1111%2Fjam.14404
https://www.ncbi.nlm.nih.gov/pubmed/31359569
https://www.proquest.com/docview/2304429180
https://www.proquest.com/docview/2267018261
https://www.proquest.com/docview/2352446126
Volume 127
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