High Genetic Diversity among Strains of the Unindustrialized Lactic Acid Bacterium Carnobacterium maltaromaticum in Dairy Products as Revealed by Multilocus Sequence Typing

Rahman, Abdur; Cailliez‐Grimal, Catherine; Bontemps, Cyril; Payot, Sophie; Chaillou, Stéphane; Revol-Junelles, Anne-Marie; Borges, Frédéric

doi:10.1128/aem.00681-14

Cited by 20 publications

(24 citation statements)

References 40 publications

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“…It has not only been applied to epidemiological studies of many bacterial pathogens, but also in the studies of population structure and genetic evolution of other bacteria (Cai et al, 2007;Rahman et al, 2014;Dan et al, 2015;Sun et al, 2015). In our study, a new MLST scheme for Lb.…”

Section: Discussionmentioning

confidence: 98%

“…Clonal complexes were defined as groups of profiles differing by no more than one gene from at least one other profile of the group (Rahman et al, 2014). Overall, a total of 171 ST were clustered into 25 CC and 71 singletons [ Figure 1 and Supplemental Figure S3 (http://dx.doi.org/10.3168/ jds.2016-10857)].…”

Section: Isolate Relationships Based On Allelic Profilesmentioning

confidence: 99%

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Multilocus sequence typing of Lactobacillus casei isolates from naturally fermented foods in China and Mongolia

Bao

Song

et al. 2016

Journal of Dairy Science

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Lactobacillus casei is a lactic acid bacterium used in manufacturing of many fermented food products. To investigate the genetic diversity and population biology of this food-related bacterium, 224 Lb. casei isolates and 5 reference isolates were examined by multilocus sequence typing (MLST). Among them, 224 Lb. casei isolates were isolated from homemade fermented foods, including naturally fermented dairy products, acidic gruel, and Sichuan pickles from 38 different regions in China and Mongolia. The MLST scheme was developed based on the analysis of 10 selected housekeeping genes (carB, clpX, dnaA, groEL, murE, pyrG, pheS, recA, rpoC, and uvrC). All 229 isolates could be allocated to 171 unique sequence types, including 25 clonal complexes and 71 singletons. The high index of association value (1.3524) and standardized index of association value (0.1503) indicate the formation of an underlying clonal population by all the isolates. However, split-decomposition, relative frequency of occurrence of recombination and mutation, and relative effect of recombination and mutation in the diversification values confirm that recombination may have occurred, and were more frequent than mutation during the evolution of Lb. casei. Results from Structure analyses (version 2.3; http://pritch.bsd.uchicago.edu/structure.html) demonstrated that there were 5 lineages in the Lb. casei isolates, and the overall relatedness built by minimum spanning tree showed no clear relationship between the clonal complexes with either the isolation sources or sampling locations of the isolates. Our newly developed MLST scheme of Lb. casei was an easy and valuable tool that, together with the construction of an MLST database, will contribute to further detailed studies on the evolution and population genetics of Lb. casei from various niches.

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Section: Discussionmentioning

confidence: 98%

Section: Isolate Relationships Based On Allelic Profilesmentioning

confidence: 99%

Multilocus sequence typing of Lactobacillus casei isolates from naturally fermented foods in China and Mongolia

Bao

Song

et al. 2016

Journal of Dairy Science

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“…The values from Tajima's D test (D), which measures deviation from the standard neutral model of evolution, ranged from Ϫ1.87 to 1.18. These values imply balancing (neutral) selection for all the selected genes, which is typical for housekeeping genes (24). Population structure.…”

Section: Resultsmentioning

confidence: 99%

Multilocus Sequence Typing of Leuconostoc gelidum subsp. gasicomitatum, a Psychrotrophic Lactic Acid Bacterium Causing Spoilage of Packaged Perishable Foods

Rahkila

Johansson

Säde

et al. 2015

Appl Environ Microbiol

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Leuconostoc gelidum subsp. gasicomitatum is a psychrotrophic lactic acid bacterium (LAB) that causes spoilage of a variety of modified-atmosphere-packaged (MAP) cold-stored food products. During the past 10 years, this spoilage organism has been increasingly reported in MAP meat and vegetable products in northern Europe. In the present study, the population structure within 252 L. gelidum subsp. gasicomitatum strains was determined based on a novel multilocus sequence-typing (MLST) scheme employing seven housekeeping genes. These strains had been isolated from meat and vegetable sources over a time span of 15 years, and all 68 previously detected pulsed-field gel electrophoresis (PFGE) genotypes were represented. A total of 46 sequence types (STs) were identified, with a majority of the strains (>60%) belonging to three major STs, which were grouped into three clonal complexes (CCs) and 17 singletons by Global Optimal eBURST (goeBURST). The results by Bayesian analysis of population structure (BAPS) mostly correlated with the grouping by goeBURST. Admixture analysis by BAPS indicated a very low level of exchange of genetic material between the subpopulations. Niche specificity was observed within the subpopulations: CC1 and BAPS cluster 1 consisted mostly of strains from a variety of MAP meats, whereas vegetable strains grouped together with strains from MAP poultry within CC2 and BAPS cluster 2. The MLST scheme presented in this study provides a shareable and continuously growing sequence database enabling global comparison of strains associated with spoilage cases. This will further advance our understanding of the microbial ecology of this industrially important LAB. L euconostoc gelidum is a psychrotrophic lactic acid bacterium (LAB) currently comprising three genetically distinct subspecies, Leuconostoc gelidum subsp. gelidum, Leuconostoc gelidum subsp. gasicomitatum, and Leuconostoc gelidum subsp. aenigmaticum, associated with modified-atmosphere-packaged (MAP) nutrient-rich foods (1). L. gelidum subsp. gasicomitatum was first encountered in spoiled MAP tomato-marinated raw broiler meat strips in 1997 (2). The spoiled packages were bulging due to rapid accumulation of CO 2 within 4 to 5 days of manufacture. L. gelidum subsp. gasicomitatum has also been prevalent in Finnish high-oxygen MAP beef and pork products (3, 4).In MAP meat, L. gelidum subsp. gasicomitatum spoilage is typically characterized by gas formation, buttery or sour off odors, and/or green discoloration of the meat (2, 3). In addition, L. gelidum subsp. gasicomitatum has been shown to form slime and gas in acetic-acid-preserved herring (5) and in cooked vegetable "sausages" packaged under vacuum (6). Recently, the LAB has been associated with similar spoilage changes in cooked, brined eggs (slime formation) and various packaged meat and vegetable products (off odors) in Belgium (7-9).Our previous study employing pulsed-field gel electrophoresis (PFGE) typing for characterization of 384 L. gelidum subsp. gasicomitatum isolates from various me...

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“…An multilocus sequence typing (MLST) scheme is available for C. maltaromaticum and was successfully applied to a collection of 47 strains originating from food products and from the environment (Rahman et al . ). This method distinguished strains with a high discriminatory index, as it delineated 36 genotypes among the 47 strains (Rahman et al .…”

Section: Introductionmentioning

confidence: 97%

“…This method distinguished strains with a high discriminatory index, as it delineated 36 genotypes among the 47 strains (Rahman et al . ). However, the collection only contained one strain isolated from diseased fish, the strain C. maltaromaticum ATCC 35586 (Rahman et al .…”

Section: Introductionmentioning

confidence: 97%

Multilocus sequence typing ofCarnobacterium maltaromaticumstrains associated with fish disease and dairy products

et al. 2018

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Aims: Carnobacterium maltaromaticum is a lactic acid bacterium of technological interest in the field of dairy ripening and food bioprotection and is generally recognized as safe in the United States. As it is associated with fish infections, the European Food Safety Agency did not include this species in the qualified presumption safety list of micro-organisms. This implies that the risk assessment for the species has to be performed at the strain level. Methods and Results: Multilocus sequence typing (MLST) is a tool that (i) potentially allows to discriminate strains isolated from diseased fish from apathogenic strains and (ii) to assess the genetic relatedness between both groups of strains. In this study, we characterized by MLST 21 C. maltaromaticum strains including 16 strains isolated from diseased fish and 5 apathogenic dairy strains isolated from cheese. The resulting population structure was investigated by integrating these new data to the previously published population structure (available at http://pubmlst.org), which represents an overall of 71 strains. Conclusions: This analysis revealed that none of the strains isolated from diseased fish is assigned to a clonal complex containing cheese isolates, and that 11 strains exhibit singleton genotypes suggesting that the population of diseased fish isolates is not clonal. Significance and Impact of the Study: This study thus provides a population structure of C. maltaromaticum that could serve in the future as a reference that could contribute to the risk assessment of C. maltaromaticum strains intended to be used in the food chain.

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High Genetic Diversity among Strains of the Unindustrialized Lactic Acid Bacterium Carnobacterium maltaromaticum in Dairy Products as Revealed by Multilocus Sequence Typing

Cited by 20 publications

References 40 publications

Multilocus sequence typing of Lactobacillus casei isolates from naturally fermented foods in China and Mongolia

Multilocus sequence typing of Lactobacillus casei isolates from naturally fermented foods in China and Mongolia

Multilocus Sequence Typing of Leuconostoc gelidum subsp. gasicomitatum, a Psychrotrophic Lactic Acid Bacterium Causing Spoilage of Packaged Perishable Foods

Multilocus sequence typing ofCarnobacterium maltaromaticumstrains associated with fish disease and dairy products

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