Adaptive Mechanisms of Listeria monocytogenes to Stressors: An Overview

Main Article Content

B. A. Haruna
A. S. Kumurya
A. H. Musa

Abstract

Listeria monocytogenes is a food borne pathogen which usually infects individuals with impaired cellular immunity and the healthy. Gastrointestinal tract (GIT) of the humans has lots of defensive mechanisms placed to prevent pathogens from establishing themselves and cause infectious diseases. Survival depends on the pathogen’s ability to overcome such preventive mechanism of the host. Listeria monocytogenes exhibits array of mechanisms that ensure its survival against these stressor. These stressors include gastric acid, bile salt, low oxygen tension, antimicrobial peptides e.t.c. Acid tolerance system (ATR), glutamate decarboxylase system (GAD), BilE system, MVs, oxygen sensors are used by Listeria monocytogenes to enhance its chances of survival within host. Our interest here is to look at such adaptive mesures with respect to the stressors encountered.  

Keywords:
Glutamate decarboxylase system (GAD), Bile Expulsion (BilE), Membrane Vesicles (MVs), Acid Tolerance System (ATR), Listeria monocytogenes, stressors, Bile Salt Hydrolase (BSH).

Article Details

How to Cite
Haruna, B. A., Kumurya, A. S., & Musa, A. H. (2019). Adaptive Mechanisms of Listeria monocytogenes to Stressors: An Overview. South Asian Journal of Research in Microbiology, 4(4), 1-8. https://doi.org/10.9734/sajrm/2019/v4i430111
Section
Review Article

References

Schlech WF. Foodborne Listeriosis. Clin. Infect. Dis. 2000;31:770–775.

Begley M, Gahan CG, Hill C. The interaction between bacteria and bile. FEMS Microbiol. Rev. 2005;29:625–651.

Dalton CB, Austin CC, Sobel J, Hayes PS, Bibb WF, Graves LM, et al. An outbreak of gastroenteritis and fever due to Listeria monocytogenes in milk, N. Engl. J. Med. 1997;336: 100–105.

Mook P, Grant KA, Little CL, Kafatos G, Gillespie IA. Emergence of pregnancy-related listeriosis amongst ethnic minorities in England and Wales. Euro Surveill. 2010;15:19610.

Moorhead SM, Dykes GA. The role of the sig B gene in the general stress response of Listeria monocytogenes varies between a strain of serotype 1/2a and a strain of serotype 4c. Curr Microbiol. 2003;46: 0461–0466.

Begley M, Kerr C, Hill C. Exposure to bile influences biofilm formation by Listeria monocytogenes. Gut Pathog. 2009;1:11.
DOI: 10.1186/1757-4749-1-11

Jeroen Koomena, Heidy MW, den Bestena, Karin I. Metselaara 1, Marcel H. Tempelaarsa, Lucas M. Wijnandsb, Marcel H. Zwieteringa, Tjakko Abee. Gene profiling-based phenotyping for identification of cellular parameters that contribute to fitness, stress-tolerance and virulence of Listeria monocytogenes variants. International Journal of Food Microbiology. 2018;283:14–21

Higuchi T, Hayashi H, Abe K. Exchange of glutamate and aminobutyrate in a Lactobacillus strain. Appl. Environ. Microbiol. 1997;179:3362–3364.

Paul D. Cotter, Sheila Ryan, Cormac G. M. Gahan, Colin hill presence of GadD1 glutamate decarboxylase in selected Listeria monocytogenes strains Is associated with an ability to grow at low pH. Applied and Environmental Microbiology. 2005;71:2832–2839.

Karatzas KA, Brennan O, Heavin S, Morrissey J, O'Byrne CP. Intracellular accumulation of high levels of gamma-aminobutyrate by Listeria monocytogenes 10403S in response to low pH: uncoupling of gamma-aminobutyrate synthesis from efflux in a chemically defined medium. Appl. Environ. Microbiol. 2010;76:3529–3537.
DOI: 10.1128/AEM.03063-09

Wemekamp-Kamphuis HH, Wouters JA, de Leeuw PPLA, Hain T, Chakraborty T, Abee T. Identification of sigma factor B-controlled genes and their impact on acid stress, high hydrostatic pressure, and freeze survival in Listeria monocytogenes EGD-e. Appl. Environ. Microbiol. 2004;70:3457–3466.

Ma´ire Begley, Colin Hill and Cormac G. M. Gahan. Bile Salt Hydrolase Activity in Probiotics Applied and Environmental Microbiology. 2006;72:1729–1738.

Bonnet M, Rafi MM, Chikindas ML, Montville TJ. Bioenergetic mechanism for nisin resistance, induced by the acid tolerance response of Listeria monocytogenes. Appl. Environ. Microbiol. 2006;72:2556–2563.

McEntire JC, Carman GM, Montville TJ. Increased ATPase activity is responsible for acid sensitivity of nisin-resistant Listeria monocytogenes ATCC 700302. Appl. Environ. Microbiol. 2004;70:2717–2721.

Van Schaik W, Gahan CG, Hill C. Acid-adapted Listeria monocytogenes displays enhanced tolerance against the lantibiotics nisin and lacticin. J. Food Prot. 1999; 62:536–539.

Shabala L, Budde B, Ross T, Siegumfeldt H, McMeekin T. Responses of Listeria monocytogenes to acid stress and glucose availability monitored by measurements of intracellular pH and viable counts. Int. J. Food Microbiol. 2002;75(1–2): 89–97.

Phan-Thanh L, Mahouin F. A proteomic approach to study the acid response in Listeria monocytogenes. Electrophoresis. 1999;20(11):2214–2224.

Gahan CG, O'Driscoll B, Hill C. Acid adaptation of Listeria monocytogenes can enhance survival in acidic foods and during milk fermentation. Applied and Environmental Microbiology. 1996;62(9): 3128–3132.

Ferreira A, Sue D, O’Byrne CP, Boor KJ. Role of Listeria monocytogenes sigma (B) in survival of lethal acidic conditions and in the acquired acid tolerance response. Appl. Environ. Microbiol. 2003;69(5):2692–2698.

Kazmierczak MJ, Mithoe SC, Boor KJ, Wiedmann M. Listeria monocytogenes σB regulates stress response and virulence functions. J. Bacteriol. 2003;185:5722–5734.

Cotter PD, Gahan CGM, Hill C. Analysis of the role of the Listeria monocytogenes F0F1-ATPase operon in the acid tolerance response. Int. J. Food Microbiol. 2000;60:137–146.

Meenakshi Thakur, Rajesh Kumar Asrani, Vikram Patial. Listeria monocytogenes: A food-borne pathogen. Copyright ©. Elsevier Inc. All rights reserved. Chapter 6. 2006;157.

Neuhaus K, Satorhelyi P, Schauer K, Scherer S, Fuchs T. Acid shock of Listeria monocytogenes at low environmental temperatures induces prfA, epithelial cell invasion and lethality towards Caenorhabditis elegans. BMC Genom. 2013;14:285.

Li T, Chiang JY. Bile acids as metabolic regulators. Current opinion in Lucas M. Wijnandsb, Marcel H. Zwieteringa, Tjakko Abee. Gene profiling-based phenotyping for identification of cellular parameters that contribute to fitness, stress-tolerance and virulence of Listeria monocytogenes variants. International Journal of Food Microbiology. 2015;283:14-21.

Chand D, Avinash VS, Yadav Y, Pundle AV, Suresh CG, Ramasamy S. Molecular features of bile salt hydrolases and relevance in human health. Biochimica et Biophysica Acta. 2017; 1861(1 Pt A):2981-2991.
DOI: 10.1016/j.bbagen.2016.09.024

Barrett Kim E. Ganong's review of medical physiology 24th ed. New York: McGraw-Hill medical. 2012;512.
ISBN: 978-0-07-178003-2

Guyton and Hall. Textbook of medical physiology. U.S. Saunders Elsevier. 2011;784.
ISBN: 978-1-4160-4574-8.

Bernstein C, Bernstein H, Payne CM, Beard SE, Schneider J. Bile Salt Activation of Stress Response Promoters in Escherichia coli. Curr. Microbiol. 1999; 39:68–72.

Begley M, Gahan CG, Hill C. The interaction between bacteria and bile. FEMS Microbiol. Rev. 2005;29:625–651.

Dussurget O, Cabanes D, Dehoux P, Lecuit M, Buchrieser C, Glaser P, Cossart P. Listeria monocytogenes bile salt hydrolase is a PrfA-regulated virulence factor involved in the intestinal and hepatic phases of listeriosis. Mol. Microbiol. 2002; 45:1095–1106.

Dowd GC, Joyce SA, Hill C, Gahan CG. Investigation of the mechanisms by which Listeria monocytogenes grows in porcine gallbladder bile. Infect. Immun. 2011;79:369–379.

Sleator RD, Wemekamp-Kamphuis HH, Gahan CG, Abee T, Hill C. A PrfA-regulated bile exclusion system (BilE) is a novel virulence factor in Listeria monocytogenes. Mol. Microbiol. 2005;55:1183–1195.

Begley M, Hill C, Ross RP. Tolerance of Listeria monocytogenes to cell envelope-acting antimicrobial agents is dependent on SigB. Appl. Environ. Microbiol. 2006; 72:2231–2234.

Grill JP, Cayuela C, Antoine JM, Schneider F. Isolation and characterization of a Lactobacillus amylovorus mutant depleted in conjugated bile salt hydrolase activity: Relation between activity and bile salt resistance. J. Appl. Microbiol. 2000;89: 553–563.

Ruiz L, Hidalgo C, Blanco-Míguez A, Lourenço A, Sánchez B, Margolles A. Tackling probiotic and gut microbiota functionality through proteomics. Journal of Proteomics. 2016;147:28-39.

Siciliano RA, Mazzeo MF. Molecular mechanisms of probiotic action: A proteomic perspective. Current Opinion in Microbiology. 2012;15(3):390-396.

Sue D, Fink D, Wiedmann M, Boor KJ. B-dependent gene induction and expression in Listeria monocytogenes during osmotic and acid stress conditions simulating the intestinal environment. Microbiology. 2004;150:3843–3855.

Van der Veen S, Abee T. Mixed species biofilms of Listeria monocytogenes and Lactobacillus plantarum show enhanced resistance to benzalkonium chloride and peracetic acid. International Journal of Food Microbiology. 2011;144(3):421-431.

Kim SH, Gorski L, Reynolds J, Orozco E, Fielding S, Park YH, et al. Role of uvrA in the growth and survival of Listeria monocytogenes under UV radiation and acid and bile stress. J. Food Prot. 2006;69:3031–3036.

So-Hyun Juna, Taewon Leeb, Je-Chul Leea, Ji-Hyun Shin. Different epithelial cell response to membrane vesicles produced by Listeria monocytogenes cultured with or without salt stress. Microbial Pathogenesis. 2019;131:103554.

Šárka H, Milada P, Kateřina D. Importance of microbial defence systems to bile salts and mechanisms of serum cholesterol reduction. Biotechnology Advances; 2017.

Quillin SJ, Schwartz KT, Leber JH. The novel Listeria monocytogenes bile sensor BrtA controls expression of the cholic acid efflux pump MdrT. Mol. Microbiol. 2011;81:129–142.
DOI: 10.1111/j.1365-2958.2011.07683.x

Davis ML, Ricke SC, Donaldson JR. Establishment of Listeria monocytogenes in the gastrointestinal tract. Microorganisms. 2019;7(3):75.
DOI:10.3390/microorganisms7030075

Crimmins GT, Herskovits AA, Rehder K, Sivick KE, Lauer P, Dubensky TW, et al. Listeria monocytogenes multidrug resistance transporters activate a cytosolic surveillance pathway of innate immunity. Proc. Natl. Acad. Sci. U.S.A. 2008;105:10191–10196.
DOI: 10.1073/pnas.0804170105

Gill CO, Tan KH. Effect of carbon dioxide on growth of meat spoilage bacteria. Appl. Environ. Microbiol. 1980;39: 317–319.

Jydegaard-Axelsen AM, Hoiby PE, Holmstrom K, Russell N, Knochel S. CO2 - and anaerobiosis-induced changes in physiology and gene expression of different Listeria monocytogenes strains. Appl. Environ. Microbiol. 2004;70:4111–4117.

Stock AM, Robinson VL, Goudreau PN. Two-component signal transduction. Annu. Rev. Biochem. 2000;69:183.
DOI: 10.1146/annurev.biochem

Throup JP, Lunsford RD, Lonsdale JT, Bryant AP, McDevitt D, Rosenberg M, Burnham MK. The srhSR gene pair from Staphylococcus aureus: Genomic and proteomic approaches to the identification and characterization of gene function. Biochemistry. 2001,40:10392–10401.

Yarwood JM, McCormick JK, Schlievert PM. Identification of a novel two-component regulatory system that acts in Global regulation of virulence factors of Staphylococcus aureus. J. Bacteriol. 2001;183:1113–1123.
DOI: 10.1128/JB.183.4.1113-1123.2001

Nakano MM, Dailly YP, Zuber P, Clark DP. Characterization of anaerobic fermentative growth of Bacillus subtilis: Identification of fermentation end products and genes required for growth. J. Bacteriol. 1997;179:6749–6755.

Kinkel TL, Roux CM, Dunman PM, Fang FC. The Staphylococcus aureus SrrAB two-component system promotes resistance to Nitrosative Stress and Hypoxia. mBio. 2013;4:696-13.

Morgan L. Davis, Steven C. Ricke, Janet R. Donaldson. Establishment of Listeria monocytogenes in the gastrointestinal tract. Microorganisms. 2019;7(3):75.

Larsen MH, Kallipolitis BH, Christiansen JK, Olsen JE, Ingmer H. The response regulator ResD modulates virulence gene expression in response to carbohydrates in Listeria monocytogenes. Mol. Microbiol. 2006;61:1622–1635.

Chiara M, D’Erchia AM, Manzari C, Minotto A, Montagna C, Addante N, Santagada G, Latorre L, Pesole G, Horner DS. Draft genome sequences of six Listeria monocytogenes strains isolated from dairy products from a processing plant in Southern Italy. Genome Announc. 2014; 2:e00282-14.

Holch A, Webb K, Lukjancenko O, Ussery D, Rosenthal BM, Gram L. Genome sequencing identifies two nearly unchanged strains of persistent Listeria monocytogenes isolated at two different fish processing plants sampled 6 years apart. Appl. Environ. Microbiol. 2013;79:2944–2951.

Wright ML, Pendarvis K, Nanduri B, Edelmann MJ, Jenkins HN, Reddy JS, Wilson JG, Ding X, Broadway PR, Ammari MG. The effect of oxygen on bile resistance in Listeria monocytogenes. J. Proteom. Bioinform. 2016;9: 107–119.

Vázquez-Boland JA, Kuhn M, Berche P, Chakraborty T, Domínguez-Bernal G, Goebel W, Kreft J. Listeria pathogenesis and molecular virulence determinants. Clinical Microbiology Reviews. 2001;14(3): 584–640.
DOI:10.1128/CMR.14.3.584-640