Dependence of the Staphylococcal Volatilome Composition on Microbial Nutrition

Jenkins, Carrie L.; Bean, Heather D.

doi:10.3390/metabo10090347

Cited by 19 publications

(26 citation statements)

References 84 publications

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“…Metformin was isolated utilising an adapted version of the liquid–liquid extraction previously described 69 . Briefly, the tissues were weighed (between ~ 2 to 20 mg) or biological fluids pipetted (~ 10 µL) into 2 mL screw cap Eppendorf plastic tube (Eppendorf, Stevenage, UK) along with a single 5 mm stainless steel ball bearing.…”

Section: Methodsmentioning

confidence: 99%

Inhibition of mitochondrial function by metformin increases glucose uptake, glycolysis and GDF-15 release from intestinal cells

Yang

Darwish

Larraufie

et al. 2021

Sci Rep

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Even though metformin is widely used to treat type2 diabetes, reducing glycaemia and body weight, the mechanisms of action are still elusive. Recent studies have identified the gastrointestinal tract as an important site of action. Here we used intestinal organoids to explore the effects of metformin on intestinal cell physiology. Bulk RNA-sequencing analysis identified changes in hexose metabolism pathways, particularly glycolytic genes. Metformin increased expression of Slc2a1 (GLUT1), decreased expression of Slc2a2 (GLUT2) and Slc5a1 (SGLT1) whilst increasing GLUT-dependent glucose uptake and glycolytic rate as observed by live cell imaging of genetically encoded metabolite sensors and measurement of oxygen consumption and extracellular acidification rates. Metformin caused mitochondrial dysfunction and metformin’s effects on 2D-cultures were phenocopied by treatment with rotenone and antimycin-A, including upregulation of GDF15 expression, previously linked to metformin dependent weight loss. Gene expression changes elicited by metformin were replicated in 3D apical-out organoids and distal small intestines of metformin treated mice. We conclude that metformin affects glucose uptake, glycolysis and GDF-15 secretion, likely downstream of the observed mitochondrial dysfunction. This may explain the effects of metformin on intestinal glucose utilisation and food balance.

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Section: Methodsmentioning

confidence: 99%

Inhibition of mitochondrial function by metformin increases glucose uptake, glycolysis and GDF-15 release from intestinal cells

Yang

Darwish

Larraufie

et al. 2021

Sci Rep

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“…Second, our data show that the growth phase of the organism has a strong influence on the volatilome, and therefore, using in vitro culture conditions that can most closely replicate the in vivo environment and microbial growth phases may increase the likelihood of putative biomarker translation from bench to bedside. In addition to controlling the growth phase of dimorphic organisms, macronutrient, micronutrient, and oxygen availability should all be considered in the development of in vitro model systems that replicate the in vivo physiology of the pathogen (14,17,(36)(37)(38)(39)(40)(41). In this study, we observed 35 VOCs present in at least 67% of all spherule strains (Fig.…”

Section: Downloaded Frommentioning

confidence: 58%

Life Cycle Dominates the Volatilome Character of Dimorphic Fungus Coccidioides spp.

Keppler

Mead

Barker

et al. 2021

mSphere

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Valley fever (coccidioidomycosis) is an endemic fungal pneumonia of the North and South American deserts. The causative agents of Valley fever are the dimorphic fungi Coccidioides immitis and C. posadasii, which grow as mycelia in the environment and as spherules within the lungs of vulnerable hosts. Current diagnostics for Valley fever are severely lacking due to poor sensitivity and invasiveness, contributing to a 23-day median time to diagnosis, and therefore, new diagnostic tools are needed. We are working toward the development of a breath-based diagnostic for coccidioidomycosis, and in this initial study, we characterized the volatile metabolomes (or volatilomes) of in vitro cultures of Coccidioides. Using solid-phase microextraction (SPME) and comprehensive two-dimensional gas chromatography coupled to time of flight mass spectrometry (GC×GC-TOFMS), we characterized the volatile organic compounds (VOCs) produced by six strains of each species during mycelial or spherule growth. We detected a total of 353 VOCs that were at least 2-fold more abundant in a Coccidioides culture than in medium controls and found that the volatile metabolome of Coccidioides is more dependent on the growth phase (spherules versus mycelia) than on the species. The volatile profiles of C. immitis and C. posadasii have strong similarities, indicating that a single suite of Valley fever breath biomarkers can be developed to detect both species. IMPORTANCE Coccidioidomycosis, or Valley fever, causes up to 30% of community-acquired pneumonias in highly populated areas of the U.S. desert southwest where the disease is endemic. The infection is difficult to diagnose by standard serological and histopathological methods, which delays appropriate treatment. Therefore, we are working toward the development of breath-based diagnostics for Valley fever. In this study, we characterized the volatile metabolomes (or volatilomes) of six strains each of Coccidioides immitis and C. posadasii, the dimorphic fungal species that cause Valley fever. By analyzing the volatilomes during the two modes of growth of the fungus—mycelia and spherules—we observed that the life cycle plays a significant role in the volatiles produced by Coccidioides. In contrast, we observed no significant differences in the C. immitis versus C. posadasii volatilomes. These data suggest that life cycle, rather than species, should guide the selection of putative biomarkers for a Valley fever breath test.

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“…Since the emergence of antibiotic-resistant strains of S. aureus that caused epidemics in the 1950s and 1960s there have been large global efforts to develop early detection systems ( Cookson, 2011 ). In the last 15 years, the understanding of the core and accessory components of the S. aureus volatilome has been steadily growing due to a growing number of in vitro volatilomic profiling studies ( Bunge et al, 2008 ; Filipiak et al, 2012b ; Baptista et al, 2019 ; Fitzgerald et al, 2020 ; Jenkins and Bean, 2020 ). The clinical value of in vitro volatilomic profiling has been demonstrated by Filipiak et al (2015) who reported detection of VOCs, known to be emitted by S. aureus , in the breath of patients with S. aureus -positive respiratory infections.…”

Section: Discussionmentioning

confidence: 99%

“…The diversity and mechanisms behind microbial volatilomes have been recently illustrated in several comprehensive review papers ( Schulz and Dickschat, 2007 ; Elmassry and Piechulla, 2020 ; Kai, 2020 ; Weisskopf et al, 2021 ) and books ( Ryu et al, 2020 ). Growth parameters such as growth media ( Jenkins and Bean, 2019 , 2020 ), growth phase ( Filipiak et al, 2012b ; Chen et al, 2016 ), oxygen content ( Insam and Seewald, 2010 ), temperature ( Misztal et al, 2018 ) and pH ( Schulz-Bohm et al, 2017 ), all influence microbial volatilomes. Another less studied factor in the overall variation seen across the volatilomes of microbial species is the occurrence of strain-level specificity in volatilomic emission within a given species ( Schulz et al, 2020 ; Weisskopf et al, 2021 ).…”

Section: Introductionmentioning

confidence: 99%

An Investigation of Stability and Species and Strain-Level Specificity in Bacterial Volatilomes

2021

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Microbial volatilomics is a rapidly growing field of study and has shown great potential for applications in food, farming, and clinical sectors in the future. Due to the varying experimental methods and growth conditions employed in microbial volatilomic studies as well as strain-dependent volatilomic differences, there is limited knowledge regarding the stability of microbial volatilomes. Consequently, cross-study comparisons and validation of results and data can be challenging. In this study, we investigated the stability of the volatilomes of multiple strains of Staphylococcus aureus, Pseudomonas aeruginosa and Escherichia coli across three frequently used nutrient-rich growth media. Volatilomic stability was assessed based on media-, time- and strain-dependent variation across the examined bacterial volatilomes. Strain-level specificity of the observed volatilomes of E. coli and P. aeruginosa strains was further investigated by comparing the emission of selected compounds at varying stages of cell growth. Headspace solid phase microextraction (HS-SPME) sampling coupled with gas chromatography mass spectrometry (GC-MS) was used to analyze the volatilome of each strain. The whole volatilomes of the examined strains demonstrate a high degree of stability across the three examined growth media. At the compound-level, media dependent differences were observed particularly when comparing the volatilomes obtained in glucose-containing brain heart infusion (BHI) and tryptone soy broth (TSB) growth media with the volatilomes obtained in glucose-free Lysogeny broth (LB) media. These glucose-dependent volatilomic differences were primarily seen in the emission of primary metabolites such as alcohols, ketones, and acids. Strain-level differences in the emission of specific compounds in E. coli and P. aeruginosa samples were also observed across the media. These strain-level volatilomic differences were also observed across varying phases of growth of each strain, therefore confirming that these strains had varying core and accessory volatilomes. Our results demonstrate that, at the species-level, the examined bacteria have a core volatilome that exhibits a high-degree of stability across frequently-used growth media. Media-dependent differences in microbial volatilomes offer valuable insights into identifying the cellular origin of individual metabolites. The observed differences in the core and accessory volatilomes of the examined strains illustrate the complexity of microbial volatilomics as a study while also highlighting the need for more strain-level investigations to ultimately elucidate the whole volatilomic capabilities of microbial species in the future.

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Dependence of the Staphylococcal Volatilome Composition on Microbial Nutrition

Cited by 19 publications

References 84 publications

Inhibition of mitochondrial function by metformin increases glucose uptake, glycolysis and GDF-15 release from intestinal cells

Inhibition of mitochondrial function by metformin increases glucose uptake, glycolysis and GDF-15 release from intestinal cells

Life Cycle Dominates the Volatilome Character of Dimorphic Fungus Coccidioides spp.

An Investigation of Stability and Species and Strain-Level Specificity in Bacterial Volatilomes

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