Prevalence and genomic diversity of Salmonella enterica recovered from river water in a major agricultural region in northwestern Mexico

Authors: GONZALEZ-LOPEZ, IRVIN - Center For Research In Food And Development (CIAD); MEDRANO-FELIX, JOSE - Center For Research In Food And Development (CIAD); CASTRO-DEL CAMPO, NOHELIA - Center For Research In Food And Development (CIAD); LOPEZ-CUEVAS, OSVALDO - Center For Research In Food And Development (CIAD); GONZALEZ-GOMEZ, JEAN - Center For Research In Food And Development (CIAD); VALDEZ-TORRES, J - Center For Research In Food And Development (CIAD); AGUIRRE-SANCHEZ, JOSE - Center For Research In Food And Development (CIAD); MARTINEZ-URTAZA, JAIME - Autonomous University Of Barcelona; GOMEZ-GIL, BRUNO - Center For Research In Food And Development (CIAD); Lee, Bertram; Quinones, Beatriz; CHAIDEZ, CRISTOBAL - Center For Research In Food And Development (CIAD)

Submitted to: Microorganisms
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 6/12/2022
Publication Date: 6/14/2022
Citation: Gonzalez-Lopez, I., Medrano-Felix, J.A., Castro-del Campo, N., Lopez-Cuevas, O., Gonzalez-Gomez, J.P., Valdez-Torres, J.B., Aguirre-Sanchez, J.R., Martinez-Urtaza, J., Gomez-Gil, B., Lee, B.G., Quinones, B., Chaidez, C. 2022. Prevalence and genomic diversity of Salmonella enterica recovered from river water in a major agricultural region in northwestern Mexico. Microorganisms. 10(6). Article 1214. https://doi.org/10.3390/microorganisms10061214.
DOI: https://doi.org/10.3390/microorganisms10061214

Interpretive Summary: Salmonella enterica is globally recognized as a significant causative agent of human gastrointestinal infections from foodborne and waterborne sources. Human salmonellosis is associated with the consumption of a diverse variety of food commodities, such as various fruits, vine vegetables, leafy greens, spices, tree nuts, poultry, beef, sprouts, flour, and ready-to-eat foods. The health benefits associated with eating a well-balanced diet including fresh fruits and vegetables have contributed to an increase in the consumption of fresh produce in Mexico and many other countries. However, this higher consumption of fresh and minimally processed ready-to-eat produce has been associated with an increased incidence in foodborne related outbreaks and sporadic illnesses. Approximately 2,600 S. enterica serotypes have been currently identified, and the highest incidence in human illnesses has been associated with serotypes Enteritidis, Typhimurium, Newport, Heidelberg, and Montevideo. However, the S. enterica serotypes with the highest prevalence in various environments in the agricultural Culiacan Valley in Northwestern Mexico have been determined to be S. enterica Oranienburg, Saintpaul and Give. The low environmental prevalence of the clinically-relevant serotypes Enteritidis, Typhimurium, Newport, Heidelberg, and Montevideo provides a challenge for accurate source tracking. Although S. enterica commonly resides in the gastrointestinal tract of animals, this pathogen is highly persistent in the environment due to its ability to prevail for prolonged periods in soils and sediments and to successfully adapt to stressful conditions of fluctuating temperatures and pH, desiccation, and nutrient deprivation. Previous reports have indicated that S. enterica prevalence in the Culiacan Valley shows a seasonal behavior, particularly when high temperatures and rainfall are present in sub-tropical regions, providing conducive environmental conditions for the growth of this pathogen. To implement strategies that allow an improved detection sensitivity of S. enterica in the agricultural environments within the Culiacan Valley, the present study employed an ultrafiltration system, as an effective in the recovery method for S. enterica from samples collected from the mayor rivers in the Culiacan Valley, a mayor agricultural region in Mexico of various fresh produce commodities for domestic and international consumption. The effect of several water physicochemical parameters on the S. enterica recovery levels were further investigated, and genome sequencing and bioinformatics tools were subsequently employed to identify the serotypes and determine the phylogenetic relationships of the S. enterica isolates recovered from irrigation rivers in this important agricultural region in Mexico.

Technical Abstract: Salmonella enterica is a leading cause of waterborne and foodborne diseases worldwide. To determine environmental factors that may promote the growth and survival of S. enterica, the present study examined the contribution of environmental and water conditions on the recovery and detection of S. enterica from major rivers used for irrigation in the agricultural Culiacan Valley, a major region for fresh produce production in Mexico. During a period of 17 months, a total of 143 samples were collected for the isolation and quantification of S. enterica from river water. To determine the relationship between physicochemical parameters and S. enterica levels, a Poisson regression model was performed, and high-resolution genome sequencing was conducted to subsequently examine phylogenetic relationships among the recovered isolates. The results from this study indicated S. enterica was detected from 78 river water samples (54.5%), and the detection levels ranged between 0.67 to 2.26 most probable number (MPN)/100 ml in the winter months, and from 11.8 to 23.5 MPN/100 mL in the summer months. Regression analyses showed a negative correlation between the detected levels of S. enterica and the following physicochemical parameters pH, salinity, electrical conductivity, total dissolved solids of the river water (P<0.1). A positive correlation was observed between the river water temperatures and the detected S. enterica levels (P<0.05). No significant correlation was identified between the relative humidity and the detected S. enterica levels at all river sampling sites. By employing the Salmonella In Silico Typing Resource (SISTR) platform, twenty-eight serotypes were identified among the recovered S. enterica isolates, and the most prevalent S. enterica serotypes were Oranienburg (21%), Anatum (7%), Pomona (6%) and Saintpaul (6%). In particular, S. Oranienburg isolates were found to be the most prevalent in the river water in this agricultural region and were identified in 91% of the sampling sites, mainly in the summer months. Thus, the findings from the present study have identified relevant environmental factors influencing the temporal and spatial detection of S. enterica from distinct river sites in a major agricultural region for fresh produce and have provided relevant information for the development of mitigation practices for the control of this foodborne and waterborne pathogen.