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Antibiotic Resistance and Phylogeny of Pseudomonas Spp. Isolated Over Three Decades from Chicken Meat in the Norwegian Food Chain

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Antibiotic Resistance and Phylogeny of Pseudomonas Spp. Isolated Over Three Decades from Chicken Meat in the Norwegian Food Chain microorganisms Article Antibiotic Resistance and Phylogeny of Pseudomonas spp. Isolated over Three Decades from Chicken Meat in the Norwegian Food Chain Even Heir 1,*, Birgitte Moen 1, Anette Wold Åsli 1, Marianne Sunde 2 and Solveig Langsrud 1 1 Nofima, Norwegian Institute of Food, Fisheries and Aquaculture Research, P. O. Box 210, N-1431 Ås, Norway; birgitte.moen@nofima.no (B.M.); anette.asli@nofima.no (A.W.Å.); solveig.langsrud@nofima.no (S.L.) 2 Department of Animal Health and Food Safety, Section of Food Safety and Emerging Health Threats, Norwegian Veterinary Institute, P.O. Box 750 Sentrum, N-0106 Oslo, Norway; [email protected] * Correspondence: even.heir@nofima.no; Tel.: +47-64970211 Abstract: Pseudomonas is ubiquitous in nature and a predominant genus in many foods and food processing environments, where it primarily represents major food spoilage organisms. The food chain has also been reported to be a potential reservoir of antibiotic-resistant Pseudomonas. The pur- pose of the current study was to determine the occurrence of antibiotic resistance in psychrotrophic Pseudomonas spp. collected over a time span of 26 years from retail chicken in Norway and character- ize their genetic diversity, phylogenetic distribution and resistance genes through whole-genome sequence analyses. Among the 325 confirmed Pseudomonas spp. isolates by 16S rRNA gene sequenc- ing, antibiotic susceptibility profiles of 175 isolates to 12 antibiotics were determined. A subset of 31 isolates being resistant to ≥3 antibiotics were whole-genome sequenced. The isolates were Citation: Heir, E.; Moen, B.; dominated by species of the P. fluorescens lineage. Isolates susceptible to all antibiotics or resistant Åsli, A.W.; Sunde, M.; Langsrud, S. to ≥3 antibiotics comprised 20.6% and 24.1%, respectively. The most common resistance was to Antibiotic Resistance and Phylogeny aztreonam (72.6%), colistin (30.2%), imipenem (25.6%) and meropenem (12.6%). Resistance prop- of Pseudomonas spp. Isolated over erties appeared relatively stable over the 26-year study period but with taxa-specific differences. Three Decades from Chicken Meat in Whole-genome sequencing showed high genome variability, where isolates resistant to ≥3 antibiotics the Norwegian Food Chain. Microorganisms 2021, 9, 207. belonged to seven species. A single metallo-betalactmase gene (cphA) was detected, though intrinsic https://doi.org/10.3390/ resistance determinants dominated, including resistance–nodulation (RND), ATP-binding cassette microorganisms9020207 (ABC) and small multidrug resistance (Smr) efflux pumps. This study provides further knowledge on the distribution of psychrotrophic Pseudomonas spp. in chicken meat and their antibiotic resistance Academic Editor: properties. Further monitoring should be encouraged to determine food as a source of antibiotic Giovanni Bonaventura resistance and maintain the overall favorable situation with regard to antibiotic resistance in the Received: 20 December 2020 Norwegian food chain. Accepted: 18 January 2021 Published: 20 January 2021 Keywords: antibiotic resistance; Pseudomonas; phylogeny; poultry; whole-genome sequencing Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affil- 1. Introduction iations. Pseudomonas has been described as one of the most ubiquitous bacterial genera in the world, and it has been found in a wide variety of outer environments (e.g., seawater, fresh water, soil, rhizosphere, bird droppings, cyanobacterial mat samples in Antarctica, Atacama desert), human environments (e.g., drinking water, kitchens, oil fields, thermal power Copyright: © 2021 by the authors. plants, sludge, food production plants), clinical specimens (e.g., pus, lungs with cystic Licensee MDPI, Basel, Switzerland. fibrosis, urinary tract infection, septicemia) and infected plants (e.g., leaf spots, brown This article is an open access article blotch disease in mushrooms; [1]). The genus is as diverse as its habitats, with nearly distributed under the terms and conditions of the Creative Commons 200 species and a complex phylogeny [2]. Foodborne psychrotrophic Pseudomonas spp. Attribution (CC BY) license (https:// have high metabolic versatility, adaptive capacity and growth abilities at low temperatures, creativecommons.org/licenses/by/ supporting their dominating prevalence in various parts of the food chain [3,4]. This genus 4.0/). includes the opportunistic human pathogen P. aeruginosa, which is a troublesome clinical, Microorganisms 2021, 9, 207. https://doi.org/10.3390/microorganisms9020207 https://www.mdpi.com/journal/microorganisms Microorganisms 2021, 9, 207 2 of 19 antibiotic-resistant bacterium, though with variable and generally low prevalence in foods and food environments [5]. For the chicken meat industry, Pseudomonas is primarily an important spoilage organism. The plucking and scalding processes usually reduce the number of bacteria, including Pseudomonas, to low numbers. However, as shown in multiple studies across several decades and continents, remaining Pseudomonas from the raw materials or from processing surfaces, chilling air or water can grow rapidly in the food product, especially under aerobic storage [6]. At the end of the shelf life, Pseudomonas dominates and spoils the meat through proteolytic, lipolytic, saccharolytic and biosurfactant processes [7]. A range of different methods with variable accuracy and discriminatory power have been and are at present used to identify Pseudomonas, making it difficult to draw general conclusions about which species are most prevalent on chicken meat. In a study from 2017, using both 16S rRNA gene sequencing and Illumina MiSeq to describe the microbiota of chicken meat, 21 different species were found, with a dominance of P. weihenstephanensis (new species 2016) and P. congelans [8]. Most likely, a variety of Pseudomonas may be present on the raw materials, but different growth abilities between Pseudomonas lead to selection of some groups over others. In early studies from Norway and Belgium, using carbohydrate and fatty acid profiles, it was reported that most isolates from spoiled poultry were similar to P. fluorescens, P. lundensis and P. fragi [9]. The same species were dominant on spoiled, marinated, poultry from Chile, when using specific PCR for identification to species level [7]. In a US study, P. fluorescens, P. putida, P. chloroaphis and P. syringae were isolated from poultry carcasses after storage, using fatty acid profiling for identification [6]. The increasing use of genomic analyses will likely provide more accurate species identification and thereby improved understanding of Pseudomonas phylogeny and characteristics in the food chain [2,10–12]. The predominance and persistence of Pseudomonas spp. in foods and on food pro- cessing surfaces have also been related to the ability of these microorganisms to form a biofilm, which enhances their tolerance to adverse conditions including antimicrobial treat- ments [12,13]. Studies have increasingly reported the role of various parts of the food chain as possible reservoirs for antibiotic-resistant bacteria and resistance genes. This includes reports on antibiotic-resistant Pseudomonas spp. in chicken and other meats [14,15], milk and dairy products [11,12,16] and vegetables [17]. Furthermore, the extraordinary ability of P. aeruginosa to acquire new mechanisms of resistance through horizontal acquisition of resistance genes carried on plasmid, integrons or transposons has been demonstrated [18]. Antibiotic-resistant Pseudomonas spp. could therefore act as potential reservoirs of antibiotic resistance in the food chain, with the ability of resistance gene transfer to other bacteria including potential pathogens. In Norway, antimicrobial resistance has since 2000 been monitored through the Nor- wegian monitoring program for antimicrobial resistance in feed, food and animals, NORM- VET (http://www.vetinst.no/overvaking/antibiotikaresistens-norm-vet). The prevalence of antibiotic-resistant bacteria in the animal food production chain in Norway is low com- pared to most other European countries [19]. Use of antimicrobial agents in the Norwegian livestock production is also low, as demonstrated by the ESCVAC (European Medicines Agency, European Surveillance of Veterinary Antimicrobial Consumption) report [20]. However, the application of selective methods for the detection of antibiotic-resistant bac- teria showed that 50% of investigated turkey meat samples harbored quinolone-resistant E. coli, although at very low quantitative levels [21,22]. Selective methods also identified high prevalence (around 40%) of resistant E. coli in fecal samples from broilers and retail chicken meat, respectively [23], prevalence that was reduced according to similar data from 2016 [24]. Transferrable plasmid-mediated resistance has been reported for both these resis- tance traits [21,25]. In NORM-VET, susceptibility testing of E. coli and Enterococcus spp. is generally used as an indicator of the occurrence of antimicrobial resistance in the bacterial population. The recent history of common though unexpected detection of antibiotic- resistant E. coli in the Norwegian poultry production chain, along with the known high Microorganisms 2021, 9, 207 3 of 19 prevalence of Pseudomonas spp. in the food chain and their reported potential for resistance gene transfer, support the need for more knowledge on the role of Pseudomonas spp. in antibiotic resistance prevalence, distribution and resistance
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