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Applied and Environmental Microbiology, August 2005, p. 4388-4399, Vol. 71, No. 8
0099-2240/05/$08.00+0     doi:10.1128/AEM.71.8.4388-4399.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.

Correlation of Phenotype with the Genotype of Egg-Contaminating Salmonella enterica Serovar Enteritidis

Cesar A. Morales,1 Steffen Porwollik,3 Jonathan G. Frye,2 Hailu Kinde,4 Michael McClelland,3 and Jean Guard-Bouldin1*

Egg Safety and Quality Research Unit,1 Bacterial Epidemiology and Antibiotic Resistance Unit, Agricultural Research Service, United States Department of Agriculture, Athens, Georgia 30605,2 Sidney Kimmel Cancer Center, San Diego, California 92093,3 California Animal Health and Food Safety Laboratory System, San Bernardino, California 924084

Received 4 November 2004/ Accepted 21 February 2005

The genotype of Salmonella enterica serovar Enteritidis was correlated with the phenotype using DNA-DNA microarray hybridization, ribotyping, and Phenotype MicroArray analysis to compare three strains that differed in colony morphology and phage type. No DNA hybridization differences were found between two phage type 13A (PT13A) strains that varied in biofilm formation; however, the ribotype patterns were different. Both PT13A strains had DNA sequences similar to that of bacteriophage Fels2, whereas the PT4 genome to which they were compared, as well as a PT4 field isolate, had a DNA sequence with some similarity to the bacteriophage ST64b sequence. Phenotype MicroArray analysis indicated that the two PT13A strains and the PT4 field isolate had similar respiratory activity profiles at 37°C. However, the wild-type S. enterica serovar Enteritidis PT13A strain grew significantly better in 20% more of the 1,920 conditions tested when it was assayed at 25°C than the biofilm-forming PT13A strain grew. Statistical analysis of the respiratory activity suggested that S. enterica serovar Enteritidis PT4 had a temperature-influenced dimorphic metabolism which at 25°C somewhat resembled the profile of the biofilm-forming PT13A strain and that at 37°C the metabolism was nearly identical to that of the wild-type PT13A strain. Although it is possible that lysogenic bacteriophage alter the balance of phage types on a farm either by lytic competition or by altering the metabolic processes of the host cell in subtle ways, the different physiologies of the S. enterica serovar Enteritidis strains correlated most closely with minor, rather than major, genomic changes. These results strongly suggest that the pandemic of egg-associated human salmonellosis that came into prominence in the 1980s is primarily an example of bacterial adaptive radiation that affects the safety of the food supply.


* Corresponding author. Mailing address: Egg Safety and Quality Research Unit, Agricultural Research Service, U.S. Department of Agriculture, 950 College Station Rd., Athens, GA 30605. Phone: (706) 546-3446. Fax: (706) 546-3161. E-mail: jbouldin{at}seprl.usda.gov.


Applied and Environmental Microbiology, August 2005, p. 4388-4399, Vol. 71, No. 8
0099-2240/05/$08.00+0     doi:10.1128/AEM.71.8.4388-4399.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.




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