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http://dx.doi.org/10.4014/jmb.2007.07036

Transcriptomic Approach for Understanding the Adaptation of Salmonella enterica to Contaminated Produce  

Park, Sojung (Department of Molecular Science and Technology, Ajou University)
Nam, Eun woo (Department of Molecular Science and Technology, Ajou University)
Kim, Yeeun (Department of Molecular Science and Technology, Ajou University)
Lee, Seohyeon (Department of Applied Chemistry and Biological Engineering, Ajou University)
Kim, Seul I (Department of Molecular Science and Technology, Ajou University)
Yoon, Hyunjin (Department of Molecular Science and Technology, Ajou University)
Publication Information
Journal of Microbiology and Biotechnology / v.30, no.11, 2020 , pp. 1729-1738 More about this Journal
Abstract
Salmonellosis is a form of gastroenteritis caused by Salmonella infection. The main transmission route of salmonellosis has been identified as poorly cooked meat and poultry products contaminated with Salmonella. However, in recent years, the number of outbreaks attributed to contaminated raw produce has increased dramatically. To understand how Salmonella adapts to produce, transcriptomic analysis was conducted on Salmonella enterica serovar Virchow exposed to fresh-cut radish greens. Considering the different Salmonella lifestyles in contact with fresh produce, such as motile and sessile lifestyles, total RNA was extracted from planktonic and epiphytic cells separately. Transcriptomic analysis of S. Virchow cells revealed different transcription profiles between lifestyles. During bacterial adaptation to fresh-cut radish greens, planktonic cells were likely to shift toward anaerobic metabolism, exploiting nitrate as an electron acceptor of anaerobic respiration, and utilizing cobalamin as a cofactor for coupled metabolic pathways. Meanwhile, Salmonella cells adhering to plant surfaces showed coordinated upregulation in genes associated with translation and ribosomal biogenesis, indicating dramatic cellular reprogramming in response to environmental changes. In accordance with the extensive translational response, epiphytic cells showed an increase in the transcription of genes that are important for bacterial motility, nucleotide transporter/metabolism, cell envelope biogenesis, and defense mechanisms. Intriguingly, Salmonella pathogenicity island (SPI)-1 and SPI-2 displayed up- and downregulation, respectively, regardless of lifestyles in contact with the radish greens, suggesting altered Salmonella virulence during adaptation to plant environments. This study provides molecular insights into Salmonella adaptation to plants as an alternative environmental reservoir.
Keywords
Salmonella enterica; produce; planktonic; epiphytic; transcriptomics;
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1 Balzer GJ, McLean RJ. 2002. The stringent response genes relA and spoT are important for Escherichia coil biofilms under slowgrowth conditions. Can. J. Microbiol. 48: 675-680.   DOI
2 Chin KCJ, Taylor TD, Hebrard M, Anbalagan K, Dashti MG, Phua KK. 2017. Transcriptomic study of Salmonella enterica subspecies enterica serovar Typhi biofilm. BMC Genomics 18: 836.   DOI
3 Galan JE. 2001. Salmonella interactions with host cells: type III secretion at work. Annu. Rev. Cell Dev. Biol. 17: 53-86.   DOI
4 McGhie EJ, Brawn LC, Hume PJ, Humphreys D, Koronakis V. 2009. Salmonella takes control: effector-driven manipulation of the host. Curr. Opin. Microbiol. 12: 117-124.   DOI
5 Shirron N, Yaron S. 2011. Active suppression of early immune response in tobacco by the human pathogen Salmonella Typhimurium. PLoS One 6: e18855.   DOI
6 Lee H, Kim SI, Park S, Nam E, Yoon H. 2018. Understanding Comprehensive tanscriptional response of Salmonella enterica spp. in contact with cabbage and napa cabbage. J. Microbiol. Biotechnol. 28: 1896-1907.   DOI
7 Schikora A, Carreri A, Charpentier E, Hirt H. 2008. The dark side of the salad: Salmonella Typhimurium overcomes the innate immune response of Arabidopsis thaliana and shows an endopathogenic lifestyle. PLoS One 3: e2279.   DOI
8 Martin CJ, Evans WJ. 1986. Phytic acid-metal ion interactions. II. The effect of pH on Ca(II) binding. J. Inorg. Biochem. 27: 17-30.   DOI
9 Dalebroux ZD, Swanson MS. 2012. ppGpp: magic beyond RNA polymerase. Nat. Rev. Microbiol. 10: 203-212.   DOI
10 Kim NH, Rhee MS. 2016. Phytic acid and sodium chloride show marked synergistic bactericidal effects against nonadapted and acid-adapted Escherichia coli O157:H7 strains. Appl. Environ. Microbiol. 82: 1040-1049.   DOI
11 Kroupitski Y, Golberg D, Belausov E, Pinto R, Swartzberg D, Granot D, et al. 2009. Internalization of Salmonella enterica in leaves is induced by light and involves chemotaxis and penetration through open stomata. Appl. Environ. Microbiol. 75: 6076-6086.   DOI
12 Bennett SD, Sodha SV, Ayers TL, Lynch MF, Gould LH, Tauxe RV. 2018. Produce-associated foodborne disease outbreaks, USA, 1998-2013. Epidemiol. Infect. 146: 1397-1406.   DOI
13 Bogino PC, Oliva Mde L, Sorroche FG, Giordano W. 2013. The role of bacterial biofilms and surface components in plant-bacterial associations. Int. J. Mol. Sci. 14: 15838-15859.   DOI
14 Wiedemann A, Virlogeux-Payant I, Chausse AM, Schikora A, Velge P. 2014. Interactions of Salmonella with animals and plants. Front. Microbiol. 5: 791.   DOI
15 Schikora A, Virlogeux-Payant I, Bueso E, Garcia AV, Nilau T, Charrier A, et al. 2011. Conservation of Salmonella infection mechanisms in plants and animals. PLoS One 6: e24112.   DOI
16 Jackson BR, Griffin PM, Cole D, Walsh KA, Chai SJ. 2013. Outbreak-associated Salmonella enterica serotypes and food Commodities, United States, 1998-2008. Emerg. Infect. Dis. 19: 1239-1244.   DOI
17 Barak JD, Kramer LC, Hao LY. 2011. Colonization of tomato plants by Salmonella enterica is cultivar dependent, and type 1 trichomes are preferred colonization sites. Appl. Environ. Microbiol. 77: 498-504.   DOI
18 Kljujev I, Raicevic V, Vujovic B, Rothballer M, Schmid M. 2018. Salmonella as an endophytic colonizer of plants - A risk for health safety vegetable production. Microb. Pathog. 115: 199-207.   DOI
19 Havelaar AH, Kirk MD, Torgerson PR, Gibb HJ, Hald T, Lake RJ, et al. 2015. World health organization global estimates and regional comparisons of the burden of foodborne disease in 2010. PLoS Med. 12: e1001923.   DOI
20 Crum-Cianflone NF. 2008. Salmonellosis and the gastrointestinal tract: more than just peanut butter. Curr. Gastroenterol. Rep. 10: 424-431.   DOI
21 Hendriksen RS, Vieira AR, Karlsmose S, Lo Fo Wong DM, Jensen AB, Wegener HC, et al. 2011. Global monitoring of Salmonella serovar distribution from the World Health Organization Global Foodborne Infections Network Country Data Bank: results of quality assured laboratories from 2001 to 2007. Foodborne Pathog. Dis. 8: 887-900.   DOI
22 Olsen SJ, Bishop R, Brenner FW, Roels TH, Bean N, Tauxe RV, et al. 2001. The changing epidemiology of salmonella: trends in serotypes isolated from humans in the United States, 1987-1997. J. Infect. Dis. 183: 753-761.   DOI
23 Ispahani P, Slack RC. 2000. Enteric fever and other extraintestinal salmonellosis in University Hospital, Nottingham, UK, between 1980 and 1997. Eur. J. Clin. Microbiol. Infect. Dis. 19: 679-687.   DOI
24 Matheson N, Kingsley RA, Sturgess K, Aliyu SH, Wain J, Dougan G, et al. 2010. Ten years experience of Salmonella infections in Cambridge, UK. J. Infect. 60: 21-25.   DOI
25 Risso D, Ngai J, Speed TP, Dudoit S. 2014. Normalization of RNA-seq data using factor analysis of control genes or samples. Nat. Biotechnol. 32: 896-902.   DOI
26 Weinberger M, Solnik-Isaac H, Shachar D, Reisfeld A, Valinsky L, Andorn N, et al. 2006. Salmonella enterica serotype Virchow: epidemiology, resistance patterns and molecular characterisation of an invasive Salmonella serotype in Israel. Clin. Microbiol. Infect. 12: 999-1005.   DOI
27 Bertrand S, Weill FX, Cloeckaert A, Vrints M, Mairiaux E, Praud K, et al. 2006. Clonal emergence of extended-spectrum betalactamase (CTX-M-2)-producing Salmonella enterica serovar Virchow isolates with reduced susceptibilities to ciprofloxacin among poultry and humans in Belgium and France (2000 to 2003). J. Clin. Microbiol. 44: 2897-2903.   DOI
28 Cho SH, Kim J, Oh KH, Hu JK, Seo J, Oh SS, et al. 2014. Outbreak of enterotoxigenic Escherichia coli O169 enteritis in schoolchildren associated with consumption of kimchi, Republic of Korea, 2012. Epidemiol. Infect. 142: 616-623.   DOI
29 Kim SI, Yoon H. 2019. Roles of YcfR in Biofilm Formation in Salmonella Typhimurium ATCC 14028. Mol. Plant Microbe. Interact. 32: 708-716.   DOI
30 Schroeder A, Mueller O, Stocker S, Salowsky R, Leiber M, Gassmann M, et al. 2006. The RIN: an RNA integrity number for assigning integrity values to RNA measurements. BMC Mol. Biol. 7: 3.   DOI
31 Robinson MD, Oshlack A. 2010. A scaling normalization method for differential expression analysis of RNA-seq data. Genome Biol. 11: R25.   DOI
32 Dillies MA, Rau A, Aubert J, Hennequet-Antier C, Jeanmougin M, Servant N, et al. 2013. A comprehensive evaluation of normalization methods for Illumina high-throughput RNA sequencing data analysis. Brief. Bioinform. 14: 671-683.   DOI
33 Robinson MD, McCarthy DJ, Smyth GK. 2010. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26: 139-140.   DOI
34 Cooley M, Carychao D, Crawford-Miksza L, Jay MT, Myers C, Rose C, et al. 2007. Incidence and tracking of Escherichia coli O157:H7 in a major produce production region in California. PLoS One 2: e1159.   DOI
35 Tatusov RL, Koonin EV, Lipman DJ. 1997. A genomic perspective on protein families. Science 278: 631-637.   DOI
36 Perez-Llamas C, Lopez-Bigas N. 2011. Gitools: analysis and visualisation of genomic data using interactive heat-maps. PLoS One 6: e19541.   DOI
37 Ban GH, Kang DH, Yoon H. 2015. Transcriptional response of selected genes of Salmonella enterica serovar Typhimurium biofilm cells during inactivation by superheated steam. Int. J. Food Microbiol. 192: 117-123.   DOI
38 Casiano-Colon A, Marquis RE. 1988. Role of the arginine deiminase system in protecting oral bacteria and an enzymatic basis for acid tolerance. Appl. Environ. Microbiol. 54: 1318-1324.   DOI
39 Marquis RE, Bender GR, Murray DR, Wong A. 1987. Arginine deiminase system and bacterial adaptation to acid environments. Appl. Environ. Microbiol. 53: 198-200.   DOI
40 Choi Y, Choi J, Groisman EA, Kang DH, Shin D, Ryu S. 2012. Expression of STM4467-encoded arginine deiminase controlled by the STM4463 regulator contributes to Salmonella enterica serovar Typhimurium virulence. Infect. Immun. 80: 4291-4297.   DOI
41 Campos E, Montella C, Garces F, Baldoma L, Aguilar J, Badia J. 2007. Aerobic L-ascorbate metabolism and associated oxidative stress in Escherichia coli. Microbiology 153: 3399-3408.   DOI
42 Perez JM, Calderon IL, Arenas FA, Fuentes DE, Pradenas GA, Fuentes EL, et al. 2007. Bacterial toxicity of potassium tellurite: unveiling an ancient enigma. PLoS One 2: e211.   DOI
43 Domka J, Lee J, Wood TK. 2006. YliH (BssR) and YceP (BssS) regulate Escherichia coli K-12 biofilm formation by influencing cell signaling. Appl. Environ. Microbiol. 72: 2449-2459.   DOI
44 Boyer E, Bergevin I, Malo D, Gros P, Cellier MF. 2002. Acquisition of Mn(II) in addition to Fe(II) is required for full virulence of Salmonella enterica serovar Typhimurium. Infect. Immun. 70: 6032-6042.   DOI
45 Kehres DG, Janakiraman A, Slauch JM, Maguire ME. 2002. SitABCD is the alkaline Mn(2+) transporter of Salmonella enterica serovar Typhimurium. J. Bacteriol. 184: 3159-3166.   DOI
46 Kehres DG, Zaharik ML, Finlay BB, Maguire ME. 2000. The NRAMP proteins of Salmonella Typhimurium and Escherichia coli are selective manganese transporters involved in the response to reactive oxygen. Mol. Microbiol. 36: 1085-1100.   DOI
47 Agyei-Owusu K, Leeper FJ. 2009. Thiamin diphosphate in biological chemistry: analogues of thiamin diphosphate in studies of enzymes and riboswitches. FEBS J. 276: 2905-2916.   DOI
48 Webb E, Febres F, Downs DM. 1996. Thiamine pyrophosphate (TPP) negatively regulates transcription of some thi genes of Salmonella typhimurium. J. Bacteriol. 178: 2533-2538.   DOI
49 Lin JT, Stewart V. 1998. Nitrate assimilation by bacteria. Adv. Microb. Physiol. 39: 1-30, 379.
50 Berks BC, Ferguson SJ, Moir JW, Richardson DJ. 1995. Enzymes and associated electron transport systems that catalyse the respiratory reduction of nitrogen oxides and oxyanions. Biochim. Biophys. Acta 1232: 97-173.   DOI
51 Roth JR, Lawrence JG, Rubenfield M, Kieffer-Higgins S, Church GM. 1993. Characterization of the cobalamin (Vitamin B12) biosynthetic genes of Salmonella Typhimurium. J. Bacteriol. 175: 3303-3316.   DOI
52 Stewart V, Lu Y, Darwin AJ. 2002. Periplasmic nitrate reductase (NapABC enzyme) supports anaerobic respiration by Escherichia coli K-12. J. Bacteriol. 184: 1314-1323.   DOI
53 Lopez CA, Rivera-Chavez F, Byndloss MX, Baumler AJ. 2015. The periplasmic nitrate reductase NapABC supports luminal growth of Salmonella enterica serovar Typhimurium during colitis. Infect. Immun. 83: 3470-3478.   DOI