Menaquinone-mediated regulation of membrane fluidity is relevant for fitness of Listeria monocytogenes.
Bacterial cell fitness
Cold adaptation
Fatty acids
Listeria monocytogenes
Membrane fluidity
Menaquinone
Journal
Archives of microbiology
ISSN: 1432-072X
Titre abrégé: Arch Microbiol
Pays: Germany
ID NLM: 0410427
Informations de publication
Date de publication:
Aug 2021
Aug 2021
Historique:
received:
22
12
2020
accepted:
05
04
2021
revised:
02
04
2021
pubmed:
20
4
2021
medline:
18
8
2021
entrez:
19
4
2021
Statut:
ppublish
Résumé
Listeria monocytogenes is a food-borne pathogen with the ability to grow at low temperatures down to - 0.4 °C. Maintaining cytoplasmic membrane fluidity by changing the lipid membrane composition is important during growth at low temperatures. In Listeria monocytogenes, the dominant adaptation effect is the fluidization of the membrane by shortening of fatty acid chain length. In some strains, however, an additional response is the increase in menaquinone content during growth at low temperatures. The increase of this neutral lipid leads to fluidization of the membrane and thus represents a mechanism that is complementary to the fatty acid-mediated modification of membrane fluidity. This study demonstrated that the reduction of menaquinone content for Listeria monocytogenes strains resulted in significantly lower resistance to temperature stress and lower growth rates compared to unaffected control cultures after growth at 6 °C. Menaquinone content was reduced by supplementation with aromatic amino acids, which led to a feedback inhibition of the menaquinone synthesis. Menaquinone-reduced Listeria monocytogenes strains showed reduced bacterial cell fitness. This confirmed the adaptive function of menaquinones for growth at low temperatures of this pathogen.
Identifiants
pubmed: 33871675
doi: 10.1007/s00203-021-02322-6
pii: 10.1007/s00203-021-02322-6
pmc: PMC8289781
doi:
Substances chimiques
Amino Acids, Aromatic
0
Vitamin K 2
11032-49-8
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
3353-3360Informations de copyright
© 2021. The Author(s).
Références
Annous BA, Becker La, Bayles DO, Labeda DP, Wilkinson BJ (1997) Critical role of anteiso-C
doi: 10.1128/aem.63.10.3887-3894.1997
Asai Y (2000) The interaction of vitamin K
doi: 10.1016/S0927-7757(99)00317-9
Asai Y, Watanabe S (1999) The interaction of ubiquinone-3 with phospholipid membranes. FEBS Lett 446:169–172. https://doi.org/10.1016/S0014-5793(99)00203-3
doi: 10.1016/S0014-5793(99)00203-3
pubmed: 10100636
Carlquist M, Fernandes RL, Helmark S, Heins A-L, Lundin L, Sørensen SJ, Gernaey KV, Lantz AE (2012) Physiological heterogeneities in microbial populations and implications for physical stress tolerance. Microb Cell Fact 11:94. https://doi.org/10.1186/1475-2859-11-94
doi: 10.1186/1475-2859-11-94
pubmed: 22799461
pmcid: 3443036
Chihib N-E, Ribeiro da Silva M, Delattre G, Laroche M, Federighi M (2003) Different cellular fatty acid pattern behaviours of two strains of Listeria monocytogenes Scott A and CNL 895807 under different temperature and salinity conditions. FEMS Microbiol Lett 218:155–160. https://doi.org/10.1111/j.1574-6968.2003.tb11512.x
doi: 10.1111/j.1574-6968.2003.tb11512.x
pubmed: 12583912
Collins MD, Jones D, Goodfellow M, Minnikin DE (1979) Isoprenoid quinone composition as a guide to the classification of Listeria, Brochothrix, Erysipelothrix and Caryophanon. J Gen Microbiol 111:453–457. https://doi.org/10.1099/00221287-111-2-453
doi: 10.1099/00221287-111-2-453
pubmed: 479832
de Mendoza D, Cronan JE (1983) Thermal regulation of membrane lipid fluidity in bacteria. Trends Biochem Sci 8:49–52. https://doi.org/10.1016/0968-0004(83)90388-2
doi: 10.1016/0968-0004(83)90388-2
de Buyser M-L, Dufour B, Maire M, Lafarge V (2001) Implication of milk and milk products in food-borne diseases in France and in different industrialised countries. Int J Food Microbiol 67:1–17. https://doi.org/10.1016/S0168-1605(01)00443-3
doi: 10.1016/S0168-1605(01)00443-3
pubmed: 11482557
Doumith M, Buchrieser C, Glaser P, Jacquet C, Martin P (2004) Differentiation of the major Listeria monocytogenes serovars by multiplex PCR. J Clin Microbiol 42:3819–3822. https://doi.org/10.1128/JCM.42.8.3819-3822.2004
doi: 10.1128/JCM.42.8.3819-3822.2004
pubmed: 15297538
pmcid: 497638
EFSA-ECDC, (2019) The European Union One Health 2018 Zoonoses Report. EFSA J 17:e05926. https://doi.org/10.2903/j.efsa.2019.5926
doi: 10.2903/j.efsa.2019.5926
Farber JM, Peterkin PI (1991) Listeria monocytogenes, a food-borne pathogen. Microbiol Rev 55:476–511
doi: 10.1128/mr.55.3.476-511.1991
Fleming DW, Cochi SL, MacDonald KL, Brondum J, Hayes PS, Plikaytis BD, Holmes MB, Audurier A, Broome CV, Reingold AL (1985) Pasteurized milk as a vehicle of infection in an outbreak of listeriosis. N Engl J Med 312:404–407. https://doi.org/10.1056/NEJM198502143120704
doi: 10.1056/NEJM198502143120704
pubmed: 3918263
Gounot AM, Russell NJ (1999) Physiology of cold-adapted microorganisms. In: Margesin R, Schinner F (eds) Cold-adapted organisms. Springer, Berlin, pp 33–55
doi: 10.1007/978-3-662-06285-2_3
Grubbs FE (1950) Sample criteria for testing outlying observations. Ann Math Statist 21:27–58. https://doi.org/10.1214/aoms/1177729885
doi: 10.1214/aoms/1177729885
Harris FM, Best KB, Bell JD (2002) Use of laurdan fluorescence intensity and polarization to distinguish between changes in membrane fluidity and phospholipid order. Biochim Biophys Acta Biomembr 1565:123–128. https://doi.org/10.1016/S0005-2736(02)00514-X
doi: 10.1016/S0005-2736(02)00514-X
Hu H-Y, Fujie K, Urano K (1999) Development of a novel solid phase extraction method for the analysis of bacterial quinones in activated sludge with a higher reliability. J Biosci Bioeng 87:378–382. https://doi.org/10.1016/S1389-1723(99)80049-8
doi: 10.1016/S1389-1723(99)80049-8
pubmed: 16232485
Jones SL, Drouin P, Wilkinson BJ, Morse PD II (2002) Correlation of long-range membrane order with temperature-dependent growth characteristics of parent and a cold-sensitive, branched-chain-fatty-acid-deficient mutant of Listeria monocytogenes. Arch Microbiol 177:217–222. https://doi.org/10.1007/s00203-001-0380-4
doi: 10.1007/s00203-001-0380-4
pubmed: 11907677
Knothe G, Dunn RO (2009) A comprehensive evaluation of the melting points of fatty acids and esters determined by differential scanning calorimetry. J Am Oil Chem Soc 86:843–856. https://doi.org/10.1007/s11746-009-1423-2
doi: 10.1007/s11746-009-1423-2
Lipski A, Altendorf K (1997) Identification of heterotrophic bacteria isolated from ammonia-supplied experimental biofilters. Syst Appl Microbiol 20:448–457. https://doi.org/10.1016/S0723-2020(97)80014-8
doi: 10.1016/S0723-2020(97)80014-8
López S, Prieto M, Dijkstra J, Dhanoa MS, France J (2004) Statistical evaluation of mathematical models for microbial growth. Int J Food Microbiol 96:289–300. https://doi.org/10.1016/j.ijfoodmicro.2004.03.026
doi: 10.1016/j.ijfoodmicro.2004.03.026
pubmed: 15454319
Lopez-Valladares G, Danielsson-Tham M-L, Tham W (2018) Implicated food products for listeriosis and changes in serovars of Listeria monocytogenes affecting humans in recent decades. Foodborne Pathog Dis 15:387–397. https://doi.org/10.1089/fpd.2017.2419
doi: 10.1089/fpd.2017.2419
pubmed: 29958028
Mastronicolis SK, German JB, Megoulas N, Petrou E, Foka P, Smith GM (1998) Influence of cold shock on the fatty-acid composition of different lipid classes of the food-borne pathogen Listeria monocytogenes. Food Microbiol 15:299–306. https://doi.org/10.1006/fmic.1997.0170
doi: 10.1006/fmic.1997.0170
Mastronicolis SK, Boura A, Karaliota A, Magiatis P, Arvanitis N, Litos C, Tsakirakis A, Paraskevas P, Moustaka H, Heropoulos G (2006) Effect of cold temperature on the composition of different lipid classes of the foodborne pathogen Listeria monocytogenes: focus on neutral lipids. Food Microbiol 23:184–194. https://doi.org/10.1016/j.fm.2005.03.001
doi: 10.1016/j.fm.2005.03.001
pubmed: 16943003
Mykytczuk NCS, Trevors JT, Leduc LG, Ferroni GD (2007) Fluorescence polarization in studies of bacterial cytoplasmic membrane fluidity under environmental stress. Prog Biophys Mol Biol 95:60–82. https://doi.org/10.1016/j.pbiomolbio.2007.05.001
doi: 10.1016/j.pbiomolbio.2007.05.001
pubmed: 17628643
Neunlist MR, Federighi M, Laroche M, Sohier D, Delattre G, Jacquet C, Chihib N-E (2005) Cellular lipid fatty acid pattern heterogeneity between reference and recent food isolates of Listeria monocytogenes as a response to cold stress. Antonie Van Leeuwenhoek 88:199–206. https://doi.org/10.1007/s10482-005-5412-7
doi: 10.1007/s10482-005-5412-7
pubmed: 16284926
Ortiz A, Aranda FJ (1999) The influence of vitamin K
doi: 10.1016/S0005-2736(99)00034-6
Royston P (1995) Remark AS R94: A remark on algorithm AS 181: the W-test for normality. J Appl Stat 44:547. https://doi.org/10.2307/2986146
doi: 10.2307/2986146
Russel N (1984) Mechanisms of thermal adaptation in bacteria: blueprints for survival. Trends Biochem Sci 9:108–112. https://doi.org/10.1016/0968-0004(84)90106-3
doi: 10.1016/0968-0004(84)90106-3
Ryser ET, Marth EH (2007) Listeria, listeriosis, and food safety. CRC Press, Boca Raton
doi: 10.1201/9781420015188
Sasser M (1990) Identification of bacteria through fatty acid analysis. In: Klement Z, Rudolph K, Sands DC (eds) Methods in phytobacteriology. Akadémiai Kiadó, Budapest, pp 199–204
Seel W, Flegler A, Zunabovic-Pichler M, Lipski A (2018) Increased isoprenoid quinone concentration modulates membrane fluidity in Listeria monocytogenes at low growth temperatures. J Bacteriol 200:e00148-e218. https://doi.org/10.1128/JB.00148-18
doi: 10.1128/JB.00148-18
pubmed: 29661862
pmcid: 5996689
Sleight SC, Wigginton NS, Lenski RE (2006) Increased susceptibility to repeated freeze-thaw cycles in Escherichia coli following long-term evolution in a benign environment. BMC Evol Biol 6:104. https://doi.org/10.1186/1471-2148-6-104
doi: 10.1186/1471-2148-6-104
pubmed: 17147797
pmcid: 1698501
Søballe B, Poole RK (1999) Microbial ubiquinones: multiple roles in respiration, gene regulation and oxidative stress management. Microbiology (Reading, Engl) 145:1817–1830. https://doi.org/10.1099/13500872-145-8-1817
doi: 10.1099/13500872-145-8-1817
Suutari M, Laakso S (1994) Microbial fatty acids and thermal adaptation. Crit Rev Microbiol 20:285–328. https://doi.org/10.3109/10408419409113560
doi: 10.3109/10408419409113560
pubmed: 7857519
Tasara T, Stephan R (2006) Cold stress tolerance of Listeria monocytogenes: a review of molecular adaptive mechanisms and food safety implications. J Food Prot 69:1473–1484. https://doi.org/10.4315/0362-028X-69.6.1473
doi: 10.4315/0362-028X-69.6.1473
pubmed: 16786878
Tatituri RVV, Wolf BJ, Brenner MB, Turk J, Hsu F-F (2015) Characterization of polar lipids of Listeria monocytogenes by HCD and low-energy CAD linear ion-trap mass spectrometry with electrospray ionization. Anal Bioanal Chem 407:2519–2528. https://doi.org/10.1007/s00216-015-8480-1
doi: 10.1007/s00216-015-8480-1
pubmed: 25656850
pmcid: 4368491
Tsukamoto Y, Kasai M, Kakuda H (2001) Construction of a Bacillus subtilis (natto) with high productivity of vitamin K
doi: 10.1271/bbb.65.2007
pubmed: 11676013
Walker SJ, Archer P, Banks JG (1990) Growth of Listeria monocytogenes at refrigeration temperatures. J Appl Bacteriol 68:157–162. https://doi.org/10.1111/j.1365-2672.1990.tb02561.x
doi: 10.1111/j.1365-2672.1990.tb02561.x
pubmed: 2108109
Zhang Y-M, Rock CO (2008) Membrane lipid homeostasis in bacteria. Nat Rev Microbiol 6:222–233. https://doi.org/10.1038/nrmicro1839
doi: 10.1038/nrmicro1839
pubmed: 18264115