The Genome Sequence of an Oxytetracycline-Resistant Isolate of the Fish Pathogen Piscirickettsia salmonis Harbors a Multidrug Resistance Plasmid

Bohle, H.; Henríquez, Patricio; Grothusen, Horst; Navas, Esteban; Bustamante, Fernando; Bustos, Patricio; Mancilla, Marcos

doi:10.1128/genomea.01571-16

Cited by 12 publications

(9 citation statements)

References 7 publications

(7 reference statements)

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“…Recent work has determined that antibiotic resistance genes found in fish stock pathogens can be traced to fish feed (21). The Piscirickettsia plasmids present in the NCBI plasmid database come from strains isolated from salmon farms in southern Chile across multiple studies by two research groups over several years (22, 23). Since these plasmids came from one geographic region, they may not represent the global diversity of Piscirickettsia plasmids - but even if these plasmids had all come from a single study the mosaic fraction would be notably high.…”

Section: Discussionmentioning

confidence: 99%

Mosaic Plasmids are Abundant and Unevenly Distributed Across Prokaryotic Taxa

Pesesky

Tilley

Beck

2018

Preprint

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24Mosaic plasmids, plasmids composed of genetic elements from distinct 25 sources, are associated with the spread of antibiotic resistance genes. Transposons 26 are considered the primary mechanism for mosaic plasmid formation, though other 27 mechanisms have been observed in specific instances. The frequency with which 28 mosaic plasmids have been described suggests they may play an important role in 29 plasmid population dynamics. Our survey of the confirmed plasmid sequences 30 available from complete and draft genomes in the RefSeq database shows that 46% 31 of them fit a strict definition of mosaic. Mosaic plasmids are also not evenly 32 distributed over the taxa represented in the database. Plasmids from some genera, 33 including Piscirickettsia and Yersinia, are almost all mosaic, while plasmids from 34 other genera, including Borrelia, are rarely mosaic. While some mosaic plasmids 35 share identical regions with hundreds of others, the median mosaic plasmid only 36 shares with 8 other plasmids. 37 When considering only plasmids from finished genomes (51.6% of the total), 38 mosaic plasmids have significantly higher proportions of transposases and 39 antibiotic resistance genes. Conversely, only 56.6% of mosaic fragments (DNA 40 fragments shared between mosaic plasmids) contain a recognizable transposase, 41 and only 1.2% of mosaic fragments are flanked by inverted repeats. Mosaic 42 fragments associated with the IS26 transposase are 3.8-fold more abundant than 43 any other sequence shared between mosaic plasmids in the database, though this is 44 at least partly due to overrepresentation of Enterobacteriaceae plasmids. 45 Mosaic plasmids are a complicated trait of some plasmid populations, only 46 partly explained by transposition. Though antibiotic resistance genes led to the 47 identification of many mosaic plasmids, mosaic plasmids are a broad phenomenon 48 encompassing many more traits than just antibiotic resistance. Further research 49 will be required to determine the influence of ecology, host repair mechanisms, 50 conjugation, and plasmid host range on the formation and influence of mosaic 51 plasmids. 52 53 Author Summary 54 Plasmids are extrachromosomal genetic entities that are found in many 55 prokaryotes. They serve as flexible storage for genes, and individual cells can make 56 substantial changes to their characteristics by acquiring, losing, or modifying a 57 plasmid. In some pathogenic bacteria, such as Escherichia coli, antibiotic resistance 58 genes are known to spread primarily on plasmids. By analyzing a database of 8,59259 plasmid sequences we determined that many of these plasmids have exchanged 60 genes with each other, becoming mosaics of genes from different sources. We next 61 separated these plasmids into groups based on the organism they were isolated 62 from and found that different groups had different fractions of mosaic plasmids. 63 This result was unexpected and suggests that the mechanisms and selective 64 pressures causing mosaic plasmids do not occur evenly over all s...

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Section: Discussionmentioning

confidence: 99%

Mosaic Plasmids are Abundant and Unevenly Distributed Across Prokaryotic Taxa

Pesesky

Tilley

Beck

2018

Preprint

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“…Refinement of antibiotic resistance marker prediction was done with tools to be encountered in the Comprehensive Antibiotic Research Database, CARD 1 (McArthur et al, 2013 ). This analysis was extended to the entire genome of AY3800B and the reference LF-89 strains (Pulgar et al, 2015 ; Bohle et al, 2017 ). Primer design was done with the Primer3 webtool 2…”

Section: Methodsmentioning

confidence: 99%

“…However, accessory genes contained in additional replicons such as plasmids carried by P. salmonis field isolates have not yet been studied in detail. As recently reported, our laboratory accomplished the sequencing of P. salmonis AY3800B (Bohle et al, 2017 ). This isolate is representative of a genovariant that displays a phenotype associated with high in vitro minimal inhibitory concentrations (MIC) of OTC (128–256 μg/mL).…”

Section: Introductionmentioning

confidence: 99%

Isolation, Functional Characterization and Transmissibility of p3PS10, a Multidrug Resistance Plasmid of the Fish Pathogen Piscirickettsia salmonis

Saavedra¹,

Grandón²,

Villalobos-González

et al. 2018

Front. Microbiol.

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Antibiotic resistance is a major public health concern due to its association with the loss of efficacy of antimicrobial therapies. Horizontal transfer events may play a significant role in the dissemination of resistant bacterial phenotypes, being mobilizable plasmids a well-known mechanism. In this study, we aimed to gain insights into the genetics underlying the development of antibiotic resistance by Piscirickettsia salmonis isolates, a bacterial fish pathogen and causative agent of salmonid piscirickettsiosis, and the main target of antibiotics used in Chilean salmon farming. We provide experimental evidence that the plasmid p3PS10, which harbors multidrug resistance genes for chloramphenicol (cat2), tetracyclines [tet(31)], aminoglycosides (sat1 and aadA1), and sulfonamides (sul2), is carried by a group of P. salmonis isolates exhibiting a markedly reduced susceptibility to oxytetracycline in vitro (128–256 μg/mL of minimal inhibitory concentration, MIC). Antibiotic susceptibility analysis extended to those antibiotics showed that MIC of chloramphenicol, streptomycin, and sulfamethoxazole/trimethoprim were high, but the MIC of florfenicol remained at the wild-type level. By means of molecular cloning, we demonstrate that those genes encoding putative resistance markers are indeed functional. Interestingly, mating assays clearly show that p3PS10 is able to be transferred into and replicate in different hosts, thereby conferring phenotypes similar to those found in the original host. According to epidemiological data, this strain is distributed across aquaculture settings in southern Chile and is likely to be responsible for oxytetracycline treatment failures. This work demonstrates that P. salmonis is more versatile than it was thought, capable of horizontally transferring DNA, and probably playing a role as a vector of resistance traits among the seawater bacterial population. However, the low transmission frequency of p3PS10 suggests a negligible chance of resistance markers being spread to human pathogens.

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“…Antibiotics and vaccination are commercially used to treat and prevent this disease, albeit with limited success [6]. Since antibiotic treatments can lead to drug residues in animal products and result in antibiotic resistance of the pathogen [7][8][9], the formulation of improved and more effective vaccines is desirable.…”

Section: Introductionmentioning

confidence: 99%

Subcellular Location of Piscirickettsia salmonis Heat Shock Protein 60 (Hsp60) Chaperone by Using Immunogold Labeling and Proteomic Analysis

et al. 2020

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Piscirickettsia salmonis is the causative bacterial agent of piscirickettsiosis, a systemic fish disease that significantly impacts the Chilean salmon industry. This bacterium possesses a type IV secretion system (T4SS), several proteins of the type III secretion system (T3SS), and a single heat shock protein 60 (Hsp60/GroEL). It has been suggested that due to its high antigenicity, the P. salmonis Hsp60 could be surface-exposed, translocated across the membrane, and (or) secreted into the extracellular matrix. This study tests the hypothesis that P. salmonis Hsp60 could be located on the bacterial surface. Immunogold electron microscopy and proteomic analyses suggested that although P. salmonis Hsp60 was predominantly associated with the bacterial cell cytoplasm, Hsp60-positive spots also exist on the bacterial cell envelope. IgY antibodies against P. salmonis Hsp60 protected SHK-1 cells against infection. Several bioinformatics approaches were used to assess Hsp60 translocation by the T4SS, T3SS, and T6SS, with negative results. These data support the hypothesis that small amounts of Hsp60 must reach the bacterial cell surface in a manner probably not mediated by currently characterized secretion systems, and that they remain biologically active during P. salmonis infection, possibly mediating adherence and (or) invasion.

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The Genome Sequence of an Oxytetracycline-Resistant Isolate of the Fish Pathogen Piscirickettsia salmonis Harbors a Multidrug Resistance Plasmid

Cited by 12 publications

References 7 publications

Mosaic Plasmids are Abundant and Unevenly Distributed Across Prokaryotic Taxa

Mosaic Plasmids are Abundant and Unevenly Distributed Across Prokaryotic Taxa

Isolation, Functional Characterization and Transmissibility of p3PS10, a Multidrug Resistance Plasmid of the Fish Pathogen Piscirickettsia salmonis

Subcellular Location of Piscirickettsia salmonis Heat Shock Protein 60 (Hsp60) Chaperone by Using Immunogold Labeling and Proteomic Analysis

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