Listeria monocytogenes loss of cultivability on carrot is associated with the formation of mesosome-like structures

Bolten, Samantha; Mowery, Joseph; Gu, Ganyu; Redding, Marina; Kroft, Brenda; Luo, Yaguang; Nou, Xiangwu

doi:10.1016/j.ijfoodmicro.2023.110121

Listeria monocytogenes loss of cultivability on carrot is associated with the formation of mesosome-like structures

Journal Article · Wed Feb 08 00:00:00 EST 2023 · International Journal of Food Microbiology

DOI:https://doi.org/10.1016/j.ijfoodmicro.2023.110121· OSTI ID:2425559

Bolten, Samantha ^[1]; Mowery, Joseph ^[2]; Gu, Ganyu ^[2]; Redding, Marina ^[2]; Kroft, Brenda ^[3]; Luo, Yaguang ^[2]; Nou, Xiangwu ^[2]

USDA-ARS Beltsville Agricultural Research Center, Beltsville, MD (United States); Cornell University, Ithaca, NY (United States)
USDA-ARS Beltsville Agricultural Research Center, Beltsville, MD (United States)
University of Maryland, College Park, MD (United States); University of Georgia, Athens, GA (United States)

Raw carrot is known to have antimicrobial activity against Listeria monocytogenes, but the mechanism of action has not been fully elucidated. In this study, we examined carrot antilisterial activity against several strains of Listeria species (including L. grayi, L. innocua, L. seeligeri, and L. welshimeri) and L. monocytogenes. A representative strain of L. monocytogenes was subsequently used for further characterizing carrot antilisterial activity. Exposure to fresh-cut carrot for 15 min resulted in a similar loss of cultivability, ranging from 2.5 to 4.7 log units, across all Listeria strains evaluated. L. monocytogenes recovered from the fresh-cut surface of different raw carrots was 1.6 to 4.1 log lower than levels obtained from paired boiled carrot samples with abolished antilisterial activity. L. monocytogenes levels recovered from fresh-cut carrot were 2.8 to 3.1 log lower when enumerated by culture-dependent methods than by the culture-independent method of PMAxx-qPCR, a qPCR assay that is performed using DNA pre-treated to selectively sequester DNA from cells with injured membranes. These results suggested that L. monocytogenes loss of cultivability on fresh-cut carrot was not associated with a loss of L. monocytogenes cell membrane integrity and putative cell viability. Transmission electron microscopy imaging revealed that L. monocytogenes rapidly formed mesosome-like structures upon exposure to carrot fresh-cut surface but not upon exposure to boiled carrot surface, suggesting there may be an association between the formation of these mesosome-like structures and a loss of cultivability in L. monocytogenes. As a result, further research is necessary to conclude the causality of this association.

View Accepted Manuscript (DOE)

Research Organization:: Oak Ridge Institute for Science and Education (ORISE), Oak Ridge, TN (United States)

Sponsoring Organization:: USDOE Office of Science (SC)

Grant/Contract Number:: SC0014664

OSTI ID:: 2425559

Journal Information:: International Journal of Food Microbiology, Journal Name: International Journal of Food Microbiology Journal Issue: C Vol. 390; ISSN 0168-1605

Publisher:: ElsevierCopyright Statement

Country of Publication:: United States

Language:: English

References (46)

Transmission electron microscopic observations of membrane effects of antibiotic cecropin B on Escherichia coli Chen, Hueih Min; Chan, Shiu‐Chiu; Lee, Jao‐Chang Microscopy Research and Technique, Vol. 62, Issue 5 https://doi.org/10.1002/jemt.10406	journal	October 2003
Quality of carrots as affected by pre‐ and postharvest factors and processing Seljåsen, Randi; Kristensen, Hanne L.; Lauridsen, Charlotte Journal of the Science of Food and Agriculture, Vol. 93, Issue 11 https://doi.org/10.1002/jsfa.6189	journal	June 2013
Isolation and antimicrobial activity of the phytoalexin 6-methoxymellein from cultured carrot cells Kurosaki, Fumiya; Nishi, Arasuke Phytochemistry, Vol. 22, Issue 3 https://doi.org/10.1016/S0031-9422(00)86959-9	journal	January 1983
The global burden of listeriosis: a systematic review and meta-analysis de Noordhout, Charline Maertens; Devleesschauwer, Brecht; Angulo, Frederick J. The Lancet Infectious Diseases, Vol. 14, Issue 11 https://doi.org/10.1016/S1473-3099(14)70870-9	journal	November 2014
Selective antibacterial activity of a novel lactotransferrin-derived antimicrobial peptide LF-1 against Streptococcus mutans Feng, Zening; Luo, Junyuan; Lyu, Xiaohui Archives of Oral Biology, Vol. 139 https://doi.org/10.1016/j.archoralbio.2022.105446	journal	July 2022
Riccardin C derivatives cause cell leakage in Staphylococcus aureus Morita, Daichi; Sawada, Hiromi; Ogawa, Wakano Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1848, Issue 10 https://doi.org/10.1016/j.bbamem.2015.05.008	journal	October 2015
A review of microbial injury and recovery methods in food Wu, V. Food Microbiology, Vol. 25, Issue 6 https://doi.org/10.1016/j.fm.2008.04.011	journal	September 2008
Peroxyacetic acid and chlorine dioxide unlike chlorine induce viable but non-culturable (VBNC) stage of Listeria monocytogenes and Escherichia coli O157:H7 in wash water Truchado, Pilar; Gil, Maria I.; Allende, Ana Food Microbiology, Vol. 100 https://doi.org/10.1016/j.fm.2021.103866	journal	December 2021
Growth capacity of Listeria monocytogenes in ingredients of ready-to-eat salads Lokerse, R. F. A.; Maslowska-Corker, K. A.; van de Wardt, L. C. Food Control, Vol. 60 https://doi.org/10.1016/j.foodcont.2015.07.041	journal	February 2016
Ralstonia insidiosa induces cell aggregation of Listeria monocytogenes Guo, Ailing; Xu, Yunfeng; Mowery, Joseph Food Control, Vol. 67 https://doi.org/10.1016/j.foodcont.2016.03.006	journal	September 2016
Susceptibility of foodborne pathogens to sanitizers in produce rinse water and potential induction of viable but non-culturable state Gu, Ganyu; Bolten, Samantha; Mowery, Joseph Food Control, Vol. 112 https://doi.org/10.1016/j.foodcont.2020.107138	journal	June 2020
Effects of temperature abuse on the growth and survival of Listeria monocytogenes on a wide variety of whole and fresh-cut fruits and vegetables during storage Kroft, Brenda; Gu, Ganyu; Bolten, Samantha Food Control, Vol. 137 https://doi.org/10.1016/j.foodcont.2022.108919	journal	July 2022
Survival and growth behaviour of Listeria monocytogenes in ready-to-eat vegetable salads Alegbeleye, Oluwadara; Sant’Ana, Anderson S. Food Control, Vol. 138 https://doi.org/10.1016/j.foodcont.2022.109023	journal	August 2022
Survival and distribution of Escherichia coli on diverse fresh-cut baby leafy greens under preharvest through postharvest conditions Tomás-Callejas, Alejandro; López-Velasco, Gabriela; Camacho, Alex B. International Journal of Food Microbiology, Vol. 151, Issue 2 https://doi.org/10.1016/j.ijfoodmicro.2011.08.027	journal	December 2011
Growth potential of Salmonella spp. and Listeria monocytogenes in nine types of ready-to-eat vegetables stored at variable temperature conditions during shelf-life Sant'Ana, Anderson S.; Barbosa, Matheus S.; Destro, Maria Teresa International Journal of Food Microbiology, Vol. 157, Issue 1 https://doi.org/10.1016/j.ijfoodmicro.2012.04.011	journal	June 2012
Growth potential of Listeria monocytogenes in twelve different types of RTE salads: Impact of food matrix, storage temperature and storage time Ziegler, Matthias; Kent, David; Stephan, Roger International Journal of Food Microbiology, Vol. 296 https://doi.org/10.1016/j.ijfoodmicro.2019.01.016	journal	May 2019
Dynamics of Listeria monocytogenes and the microbiome on fresh-cut cantaloupe and romaine lettuce during storage at refrigerated and abusive temperatures Gu, Ganyu; Kroft, Brenda; Lichtenwald, Marina International Journal of Food Microbiology, Vol. 364 https://doi.org/10.1016/j.ijfoodmicro.2022.109531	journal	March 2022
A new class of synthetic retinoid antibiotics effective against bacterial persisters Kim, Wooseong; Zhu, Wenpeng; Hendricks, Gabriel Lambert Nature, Vol. 556, Issue 7699 https://doi.org/10.1038/nature26157	journal	March 2018
Multistate Outbreak of Listeriosis Associated with Cantaloupe McCollum, Jeffrey T.; Cronquist, Alicia B.; Silk, Benjamin J. New England Journal of Medicine, Vol. 369, Issue 10 https://doi.org/10.1056/NEJMoa1215837	journal	September 2013
Hospital-Acquired Listeriosis Outbreak Caused by Contaminated Diced Celery—Texas, 2010 Gaul, Linda Knudson; Farag, Noha H.; Shim, Trudi Clinical Infectious Diseases, Vol. 56, Issue 1 https://doi.org/10.1093/cid/cis817	journal	September 2012
Induction, detection, formation, and resuscitation of viable but non‐culturable state microorganisms Dong, Kai; Pan, Hanxu; Yang, Dong Comprehensive Reviews in Food Science and Food Safety, Vol. 19, Issue 1 https://doi.org/10.1111/1541-4337.12513	journal	December 2019
Practical in‐storage interventions to control foodborne pathogens on fresh produce Sheng, Lina; Zhu, Mei‐Jun Comprehensive Reviews in Food Science and Food Safety, Vol. 20, Issue 5 https://doi.org/10.1111/1541-4337.12786	journal	June 2021
Water Activity of Fresh Foods Chirife, Jorge; Fontan, Constantino Ferro Journal of Food Science, Vol. 47, Issue 2 https://doi.org/10.1111/j.1365-2621.1982.tb10145.x	journal	March 1982
The lethal effect of carrot onListeriaspecies Nguyen-the, C.; Lund, Barbara M. Journal of Applied Bacteriology, Vol. 70, Issue 6 https://doi.org/10.1111/j.1365-2672.1991.tb02744.x	journal	June 1991
An investigation of the antibacterial effect of carrot on Listeria monocytogenes Nguyen-the, C.; Lund, Barbara M. Journal of Applied Bacteriology, Vol. 73, Issue 1 https://doi.org/10.1111/j.1365-2672.1992.tb04964.x	journal	July 1992
Antimicrobial activity of shredded carrot extracts on food‐borne bacteria and yeast Babic, I.; Nguyen‐the, C.; Amiot, M. J. Journal of Applied Bacteriology, Vol. 76, Issue 2 https://doi.org/10.1111/j.1365-2672.1994.tb01608.x	journal	February 1994
Activity and mechanism of the action of zeylasterone against Bacillus subtilis de León, L.; Moujir, L. Journal of Applied Microbiology, Vol. 104, Issue 5 https://doi.org/10.1111/j.1365-2672.2007.03663.x	journal	May 2008
Induction of 6‐Methoxymellein and Resistance to Storage Pathogens in Carrot Slices by UV‐C Mercier, J.; Arul, J.; Ponnampalam, R. Journal of Phytopathology, Vol. 137, Issue 1 https://doi.org/10.1111/j.1439-0434.1993.tb01324.x	journal	January 1993
Inhibition of Foodborne Pathogens by Native Microflora Recovered from Fresh Peeled Baby Carrot and Propagated in Cultures Liao, C. ‐H. Journal of Food Science, Vol. 72, Issue 4 https://doi.org/10.1111/j.1750-3841.2007.00333.x	journal	April 2007
Inhibitory effects of raw carrots on Listeria monocytogenes Beuchat, L. R.; Brackett, R. E. Applied and Environmental Microbiology, Vol. 56, Issue 6 https://doi.org/10.1128/aem.56.6.1734-1742.1990	journal	June 1990
Mesosomes: membranous bacterial organelles Greenawalt, J. W.; Whiteside, T. L. Bacteriological Reviews, Vol. 39, Issue 4 https://doi.org/10.1128/br.39.4.405-463.1975	journal	December 1975
Viable-but-Nonculturable Listeria monocytogenes and Salmonella enterica Serovar Thompson Induced by Chlorine Stress Remain Infectious Highmore, Callum J.; Warner, Jennifer C.; Rothwell, Steve D. mBio, Vol. 9, Issue 2 https://doi.org/10.1128/mBio.00540-18	journal	April 2018
Fitting Linear Mixed-Effects Models Using lme4 Bates, Douglas; Mächler, Martin; Bolker, Ben Journal of Statistical Software, Vol. 67, Issue 1 https://doi.org/10.18637/jss.v067.i01	journal	January 2015
Simplified Agar Plate Method for Quantifying Viable Bacteria Jett, Bradley D.; Hatter, Kenneth L.; Huycke, Mark M. BioTechniques, Vol. 23, Issue 4 https://doi.org/10.2144/97234bm22	journal	October 1997
Multistate Outbreak of Listeriosis Associated with Packaged Leafy Green Salads, United States and Canada, 2015–2016 Self, Julie L.; Conrad, Amanda; Stroika, Steven Emerging Infectious Diseases, Vol. 25, Issue 8 https://doi.org/10.3201/eid2508.180761	journal	August 2019
Advances and Challenges in Viability Detection of Foodborne Pathogens Zeng, Dexin; Chen, Zi; Jiang, Yuan Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.01833	journal	November 2016
Anti-listeria Activities of Linalool and Its Mechanism Revealed by Comparative Transcriptome Analysis Gao, Zhipeng; Van Nostrand, Joy D.; Zhou, Jizhong Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.02947	journal	December 2019
Silver Nanoparticles Combined With Naphthoquinones as an Effective Synergistic Strategy Against Staphylococcus aureus Krychowiak, Marta; Kawiak, Anna; Narajczyk, Magdalena Frontiers in Pharmacology, Vol. 9 https://doi.org/10.3389/fphar.2018.00816	journal	July 2018
Antimicrobial Activity and Mode of Action of Celastrol, a Nortriterpen Quinone Isolated from Natural Sources Padilla-Montaño, Nayely; de León Guerra, Leandro; Moujir, Laila Foods, Vol. 10, Issue 3 https://doi.org/10.3390/foods10030591	journal	March 2021
Changes in the Ultrastructure of Staphylococcus aureus Treated with Cationic Peptides and Chlorhexidine Grigor’eva, Alina; Bardasheva, Alevtina; Tupitsyna, Anastasiya Microorganisms, Vol. 8, Issue 12 https://doi.org/10.3390/microorganisms8121991	journal	December 2020
Detection and Potential Virulence of Viable but Non-Culturable (VBNC) Listeria monocytogenes: A Review Wideman, Nathan E.; Oliver, James D.; Crandall, Philip Glen Microorganisms, Vol. 9, Issue 1 https://doi.org/10.3390/microorganisms9010194	journal	January 2021
Leuconostoc mesenteroides Strains Isolated from Carrots Show Probiotic Features Schifano, Emily; Tomassini, Alberta; Preziosi, Adele Microorganisms, Vol. 9, Issue 11 https://doi.org/10.3390/microorganisms9112290	journal	November 2021
Mesosomes, Unique Membranous Structures in Bacteria Li, Xin; Yang, Li Peng; Zhu, Wen Xue Advanced Materials Research, Vol. 894 https://doi.org/10.4028/www.scientific.net/AMR.894.316	journal	February 2014
Changes in Populations of Listeria monocytogenes Inoculated on Packaged Fresh-Cut Vegetables Farber, J. M.; Wang, S. L.; Cai, Y. Journal of Food Protection, Vol. 61, Issue 2 https://doi.org/10.4315/0362-028X-61.2.192	journal	February 1998
ComBase Models Are Valid for Predicting Fate of Listeria monocytogenes on 10 Whole Intact Raw Fruits and Vegetables Girbal, Marina; Strawn, Laura K.; Murphy, Claire M. Journal of Food Protection, Vol. 84, Issue 4 https://doi.org/10.4315/JFP-20-327	journal	April 2021
Wet versus Dry Inoculation Methods Have a Significant Effect of Listeria monocytogenes Growth on Many Types of Whole Intact Fresh Produce Girbal, Marina; Strawn, Laura K.; Murphy, Claire M. Journal of Food Protection, Vol. 84, Issue 10 https://doi.org/10.4315/JFP-21-187	journal	October 2021