Amino acid consumption and secretion patterns of Staphylococcus aureus following growth in sub-optimal environmental conditions

Mousa M Alreshidi

Abstract


Background: Staphylococcus aureus is highly associated with nosocomial infections due to its ability to adapt to wide range of environmental parameters. The aim of this study was to evaluate amino acids consumption and secretion by S. aureus at mid-exponential and stationary phases under growth in sub-optimal conditions, including changes in pH, temperature and osmolality.

Methods: The consumption and secretion of amino acids were determined by subtracting the original concentrations of the free amino acids in the media from those estimated at both mid-exponential and stationary phases of growth.

Results: The analysis revealed that the consumption and secretion profiles were substantially different between cells grown under optimal control conditions, when compared with those exposed to sub-optimal conditions. The analyses of the supernatants harvested at mid-exponential phase revealed that the total consumption of amino acids was increased by 1.2 and 1.7 times by cells grown at either pH 6 or 8 and 35°C with additional of 5 % NaCl, respectively. However, the final levels of amino acids consumed at stationary phase were significantly reduced in the cells grown in sub-optimal conditions compared with bacteria cells grown under optimal conditions.

Conclusion: It was evident that various environmental conditions led to differential profiles of amino acid consumption and secretion.

Keywords: Staphylococcus aureus; Amino acid metabolism; Stress responses


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References


Alreshidi MM, Dunstan RH, Onyango LA, Roberts TK (2013) Staphylococcal phenomics: metabolomic and proteomic responses to environmental stessors. In: Mendez-Vilas A, editor. Microbial pathogens and strategies for combating them: science, technology and education: Spain Formatex Research Center. pp. 690-701.

Alreshidi MM, Dunstan RH, Macdonald MM, Smith ND, Gottfries J, et al. Amino acids and proteomic acclimation of Staphylococcus aureus when incubated in a defined minimal medium supplemented with 5% sodium chloride. Microbiologyopen, (2019); 8(6): e00772.

Alreshidi MM, Dunstan RH, Gottfries J, Macdonald MM, Crompton MJ, et al. Changes in the Cytoplasmic Composition of Amino Acids and Proteins Observed in Staphylococcus aureus during Growth under Variable Growth Conditions Representative of the Human Wound Site. PLoS One, (2016); 11(7): e0159662.

Onyango LA, Alreshidi MM. Adaptive Metabolism in Staphylococci: Survival and Persistence in Environmental and Clinical Settings. Journal of Pathogens, (2018); 1092632.

Thompson KM, Jefferson KK (2009) Adaption ot Stress: Biofilms and Small-Colony Variants. In: 2, editor. Staphylococci in Human Diseases. pp. 109-110.

Alreshidi MM, Dunstan RH, Macdonald MM, Smith ND, Gottfries J, et al. Metabolomic and proteomic responses of Staphylococcus aureus to prolonged cold stress. Journal of Proteomics, (2015); 12: 144-55.

Tsai M, Ohniwa RL, Kato Y, Takeshita SL, Ohta T, et al. Staphylococcus aureus requires cardiolipin for survival under conditions of high salinity. BMC Microbiology, (2011); 11: 13.

Rode TM, Moretro T, Langsrud S, Langsrud O, Vogt G, et al. Responses of Staphylococcus aureus exposed to HCl and organic acid stress. Canadian journal of microbiology, (2010); 56(9): 777-792.

Onyango LA, Hugh Dunstan R, Roberts TK, Macdonald MM, Gottfries J. Phenotypic variants of staphylococci and their underlying population distributions following exposure to stress. PLoS One, (2013); 8(10): e77614.

Onyango LA, Dunstan RH, Gottfries J, von Eiff C, Roberts TK. Effect of Low Temperature on Growth and Ultra-Structure of Staphylococcus spp. PloS One, (2012); 7(1): e29031.

Crompton MJ, Dunstan RH, Macdonald MM, Gottfries J, von Eiff C, et al. Small changes in environmental parameters lead to alterations in antibiotic resistance, cell morphology and membrane fatty acid composition in Staphylococcus lugdunensis. PLoS One, (2014); 9(4):

e92296.

Zhu Y, Weiss EC, Otto M, Fey PD, Smeltzer MS, et al. Staphylococcus aureus biofilm metabolism and the influence of arginine on polysaccharide intercellular adhesin synthesis, biofilm formation, and pathogenesis. Infection and Immunity, (2007); 75(9): 4219-4226.

Valle J, Da Re S, Schmid S, Skurnik D, D'Ari R, et al. The amino acid valine is secreted in continuous-flow bacterial biofilms. Journal of Bacteriology, (2008); 190(1): 264-274.

Sendi P, Proctor RA. Staphylococcus aureus as an intracellular pathogen: the role of small colony variants. Trends in Microbiology, (2009); 17(2): 54-58.

Schmitz FJ, von Eiff C, Gondolf M, Fluit AC, Verhoef J, et al. Staphylococcus aureus small colony variants: rate of selection and MIC values compared to wild-type strains, using ciprofloxacin, ofloxacin, levofloxacin, sparfloxacin and moxifloxacin. Clinical Microbiology and Infection, (1999); 5(6): 376-378.

Proctor RA, von Eiff C, Kahl BC, Becker K, McNamara P, et al. Small colony variants: a pathogenic form of bacteria that facilitates persistent and recurrent infections. Nature Reviews Microbiology, (2006); 4(4): 295-305.

von Eiff C, Proctor RA, Peters G. Small colony variants of Staphylococci: a link to persistent infections. Berliner und Münchener tierärztliche Wochenschrift, (2000); 113(9): 321-325.

Lee S, Choi KH, Yoon Y. Effect of NaCl on Biofilm Formation of the Isolate from Staphylococcus aureus Outbreak Linked to Ham. Korean Journal for Food Science of Animal Resources, (2014); 34(2): 257-261.

Jaishankar J, Srivastava P. Molecular Basis of Stationary Phase Survival and Applications. Frontiers in Microbiology, (2017); 82000.

Jones EM, Cochrane CA, Percival SL. The Effect of pH on the Extracellular Matrix and Biofilms. Advances in Wound Care (New Rochelle), (2015); 4(7): 431-439.

Li W, Li Y, Wu Y, Cui Y, Liu Y, et al. Phenotypic and genetic changes in the life cycle of small colony variants of Salmonella enterica serotype Typhimurium induced by streptomycin. Annals of Clinical Microbiology and Antimicrobials, (2016); 15(1): 37.

Yao YF, Sturdevant DE, Otto M. Genomewide analysis of gene expression in Staphylococcus epidermidis biofilms: Insights into the pathophysiology of S-epidermidis biofilms and the role of phenol-soluble modulins in formation of biofilms. Journal of Infectious Diseases, (2005); 191(2): 289-298.

Noumi E, Merghni A, M MA, Haddad O, Akmadar G, et al. Chromobacterium violaceum and Pseudomonas aeruginosa PAO1: Models for Evaluating Anti-Quorum Sensing Activity of Melaleuca alternifolia Essential Oil and Its Main Component Terpinen-4-ol. Molecules, (2018); 23(10).

Noumi E, Snoussi M, Alreshidi MM, Rekha PD, Saptami K, et al. Chemical and Biological Evaluation of Essential Oils from Cardamom Species. Molecules, (2018); 23(11).

Ammons MC, Tripet BP, Carlson RP, Kirker KR, Gross MA, et al. Quantitative NMR metabolite profiling of methicillin-resistant and methicillin-susceptible Staphylococcus aureus discriminates between biofilm and planktonic phenotypes. Journal of Proteome Research, (2014); 13(6): 2973-2985.

Beenken KE, Dunman PM, McAleese F, Macapagal D, Murphy E, et al. Global gene expression in Staphylococcus aureus biofilms. Journal of Bacteriology, (2004); 186(14): 4665-4684.

Schwan WR, Wetzel KJ, Gomez TS, Stiles MA, Beitlich BD, et al. Low-proline environments impair growth, proline transport and in vivo survival of Staphylococcus aureus strain-specific putP mutants. Microbiology, (2004); 150(Pt 4): 1055-1061.

Murphy GR, Dunstan RH, Macdonald MM, Gottfries J, Roberts TK. Alterations in amino acid metabolism during growth by Staphylococcus aureus following exposure to H2O2 – A multifactorial approach. Heliyon, (2018); 4(5): e00620.

Dorries K, Lalk M. Metabolic footprint analysis uncovers strain specific overflow metabolism and D-isoleucine production of Staphylococcus aureus COL and HG001. PLoS One, (2013); 8(12): e81500.

Liebeke M, Dorries K, Zuhlke D, Bernhardt J, Fuchs S, et al. A metabolomics and proteomics study of the adaptation of Staphylococcus aureus to glucose starvation. Molecular Biosystems, (2011); 7(4): 1241-1253.

Stipetic LH, Dalby MJ, Davies RL, Morton FR, Ramage G, et al. A novel metabolomic approach used for the comparison of Staphylococcus aureus planktonic cells and biofilm samples. Metabolomics, (2016); 1275.

Wehrli PM, Lindberg E, Svensson O, Sparén A, Josefson M, et al. Exploring bacterial phenotypic diversity using factorial design and FTIR multivariate fingerprinting. Chemometrics, (2014); 30283-289.

Butt HL, Dunstan RH, McGregor NR, Roberts TK, Zerbes M, et al. An association of membrane-damaging toxins from coagulase-negative staphylococci and chronic orofacial muscle pain. Journal of Medical Microbiology, (1998); 47(7): 577-584.

Brown GK, Martin AR, Roberts TK, Aitken RJ. Detection of Ehrlichia platys in dogs in Australia. Australian Veterinary Journal, (2001); 79(8): 554-558.

Zhu Y, Xiong YQ, Sadykov MR, Fey PD, Lei MG, et al. Tricarboxylic acid cycle-dependent attenuation of Staphylococcus aureus in vivo virulence by selective inhibition of amino acid transport. Infection and Immunity, (2009); 77(10): 4256-4264.

Turner GW, Cuthbertson DJ, Voo SS, Settles ML, Grimes HD, et al. Experimental sink removal induces stress responses, including shifts in amino acid and phenylpropanoid metabolism, in soybean leaves. Planta, (2012); 235(5): 939-954.

Tremaroli V, Workentine ML, Weljie AM, Vogel HJ, Ceri H, et al. Metabolomic investigation of the bacterial response to a metal challenge. Applied and environmental microbiology, (2009); 75(3): 719-728.

Dickgiesser N, Eppli P. Amino acid requirements of Staphylococcus aureus strains from Germany and Austria that produce toxic shock syndrome toxin-1 (TSST-1). Zentralbl Bakteriol Mikrobiol Hyg A, (1988); 268(1): 1-7.

Liebeke M, Lalk M. Staphylococcus aureus metabolic response to changing environmental conditions – a metabolomics perspective. International Journal of Medical Microbiology, (2014); 304(3-4): 222-229.

Richardson AR, Dunman PM, Fang FC. The nitrosative stress response of Staphylococcus aureus is required for resistance to innate immunity. Molecular microbiology, (2006); 61(4): 927-939.

Booth IR. Regulation of cytoplasmic pH in bacteria. Microbiological reviews, (1985); 49(4): 359-378.

Nystrom T. Stationary-phase physiology. Annual Review of Microbiology, (2004); 58161-181.

Aertsen A, Michiels CW. Stress and how bacteria cope with death and survival. Critical Reviews in Microbiology, (2004); 30(4): 263-273.

Kussell E, Kishony R, Balaban NQ, Leibler S. Bacterial persistence: a model of survival in changing environments. Genetics, (2005); 169(4): 1807-1814.

Balaban NQ, Merrin J, Chait R, Kowalik L, Leibler S. Bacterial persistence as a phenotypic switch. Science, (2004); 305(5690): 1622-1625.

De Kievit TR, Gillis R, Marx S, Brown C, Iglewski BH. Quorum-sensing genes in Pseudomonas aeruginosa biofilms: their role and expression patterns. Applied and Environmental Microbiology, (2001);

(4): 1865-1873.

Aliashkevich A, Alvarez L, Cava F. New Insights Into the Mechanisms and Biological Roles of D-Amino Acids in Complex Eco-Systems. Frontiers in Microbiology, (2018); 9683.

Lam H, Oh DC, Cava F, Takacs CN, Clardy J, et al. D-amino acids govern stationary phase cell wall remodeling in bacteria. Science, (2009); 325(5947): 1552-1555.

Martin MF, Liras P. Organization and expression of genes involved in the biosynthesis of antibiotics and other secondary metabolites. Annual Review of Microbiology, (1989); 43173-206.

Lopez D, Vlamakis H, Kolter R. Biofilms. Cold Spring Harbor Perspectives in Biology, (2010); 2(7): a000398.

Lopez D, Kolter R. Extracellular signals that define distinct and coexisting cell fates in Bacillus subtilis. FEMS Microbiology Reviews, (2010); 34(2): 134-149.

Resch A, Leicht S, Saric M, Pasztor L, Jakob A, et al. Comparative proteome analysis of Staphylococcus aureus biofilm and planktonic cells and correlation with transcriptome profiling. Proteomics, (2006); 6(6): 1867-1877.

Vuong C, Kidder JB, Jacobson ER, Otto M, Proctor RA, et al. Staphylococcus epidermidis polysaccharide intercellular adhesin production significantly increases during tricarboxylic acid cycle stress. Journal of Bacteriology, (2005); 187(9): 2967-2973.

Sadykov MR, Zhang B, Halouska S, Nelson JL, Kreimer LW, et al. Using NMR metabolomics to investigate tricarboxylic acid cycle-dependent signal transduction in Staphylococcus epidermidis. The Journal of Biological Chemistry, (2010); 285(47): 36616-36624.

Sadykov MR, Olson ME, Halouska S, Zhu Y, Fey PD, et al. Tricarboxylic acid cycle-dependent regulation of Staphylococcus epidermidis polysaccharide intercellular adhesin synthesis. Journal of Bacteriology, (2008); 190(23): 7621-7632.

Somerville GA, Proctor RA. At the crossroads of bacterial metabolism and virulence factor synthesis in Staphylococci. Microbiology and Molecular Biology Reviews, (2009); 73(2): 233-248.

Fleury B, Kelley WL, Lew D, Gotz F, Proctor RA, et al. Transcriptomic and metabolic responses of Staphylococcus aureus exposed to supra-physiological temperatures. BMC Microbiology, (2009); 976.

Chatterjee I, Somerville GA, Heilmann C, Sahl HG, Maurer HH, et al. Very low ethanol concentrations affect the viability and growth recovery in post-stationary-phase Staphylococcus aureus populations. Applied Environmental Microbiology, (2006); 72(4): 2627-2636.

Casadevall A. Evolution of intracellular pathogens. Annual review of microbiology, (2008); 6219-33.

de Jonge BL, Chang YS, Gage D, Tomasz A. Peptidoglycan composition of a highly methicillin-resistant Staphylococcus aureus strain. The role of penicillin binding protein 2A. The Journal of biological chemistry, (1992); 267(16): 11248-11254.




DOI: http://dx.doi.org/10.62940/als.v7i2.912

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