Implication of Lateral Genetic Transfer in the Emergence of Aeromonas hydrophila Isolates of Epidemic Outbreaks in Channel Catfish

Hossain, M. Jahangir; Waldbieser, Geoffrey C.; Sun, Dawei; Capps, Nancy K.; Hemstreet, William B.; Carlisle, K.; Griffin, Matt J.; Khoo, Lester H.; Goodwin, Andrew E.; Sonstegard, Tad S.; Schroeder, Steven G.; Hayden, Karl J.; Newton, Joseph C.; Terhune, Jeffery S.; Liles, Mark R.

doi:10.1371/journal.pone.0080943

Cited by 85 publications

(103 citation statements)

References 69 publications

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“…O-antigen modification is a well-recognized phenomenon in Gram-negative bacteria and may be generated by horizontal gene transfer (43,44) or bacteriophage-mediated mechanisms (45,46). Indeed, horizontal gene transfer involving O-antigen biosynthesis gene clusters has contributed to LPS diversity in the Aeromonas hydrophila strains responsible for septicemia in catfish (47). However, mutations within a key set of genes have been responsible for the vaccinedriven evolution of the capsular operon of the fish pathogen Streptococcus iniae (48), and this process cannot be discounted to explain the emergence of the O8 O antigen in Y. ruckeri.…”

Section: Discussionmentioning

confidence: 99%

Yersinia ruckeri Isolates Recovered from Diseased Atlantic Salmon (Salmo salar) in Scotland Are More Diverse than Those from Rainbow Trout (Oncorhynchus mykiss) and Represent Distinct Subpopulations

Ormsby

Caws

Burchmore

et al. 2016

Appl Environ Microbiol

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Yersinia ruckeri is the etiological agent of enteric redmouth (ERM) disease of farmed salmonids. Enteric redmouth disease is traditionally associated with rainbow trout (Oncorhynchus mykiss, Walbaum), but its incidence in Atlantic salmon (Salmo salar) is increasing. Yersinia ruckeri isolates recovered from diseased Atlantic salmon have been poorly characterized, and very little is known about the relationship of the isolates associated with these two species. Phenotypic approaches were used to characterize 109 Y. ruckeri isolates recovered over a 14-year period from infected Atlantic salmon in Scotland; 26 isolates from infected rainbow trout were also characterized. Biotyping, serotyping, and comparison of outer membrane protein profiles identified 19 Y. ruckeri clones associated with Atlantic salmon but only five associated with rainbow trout; none of the Atlantic salmon clones occurred in rainbow trout and vice versa. These findings suggest that distinct subpopulations of Y. ruckeri are associated with each species. A new O serotype (designated O8) was identified in 56 biotype 1 Atlantic salmon isolates and was the most common serotype identified from 2006 to 2011 and in 2014, suggesting an increased prevalence during the time period sampled. Rainbow trout isolates were represented almost exclusively by the same biotype 2, serotype O1 clone that has been responsible for the majority of ERM outbreaks in this species within the United Kingdom since the 1980s. However, the identification of two biotype 2, serotype O8 isolates in rainbow trout suggests that vaccines containing serotypes O1 and O8 should be evaluated in both rainbow trout and Atlantic salmon for application in Scotland. IMPORTANCEVaccination plays an important role in protecting Atlantic salmon against the bacterial pathogen Yersinia ruckeri, but, in recent years, there has been an increasing incidence of vaccine breakdown in salmon. This is largely because current vaccines are aimed at rainbow trout and are based on serotypes specific for this species. A wider range of serotypes is responsible for infection in Atlantic salmon, but very little is known about the diversity of these strains and their relationships to those recovered from rainbow trout. In the present study, we demonstrate that Y. ruckeri isolates recovered from diseased Atlantic salmon in Scotland are more diverse than those from rainbow trout; furthermore, isolates from the two species represent distinct subpopulations. In addition, a new O serotype was identified that is responsible for a significant proportion of the disease in Atlantic salmon. Our findings are likely to have important implications for the development of improved vaccines against Y. ruckeri. The Gram-negative bacterium Yersinia ruckeri is the etiological agent of enteric redmouth (ERM) disease of cultured salmonids and causes significant economic losses to the fish-farming industry. Yersinia ruckeri was first isolated in 1956 from diseased rainbow trout (Oncorhynchus mykiss, Walbaum) in the Hagerman Valle...

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Section: Discussionmentioning

confidence: 99%

Yersinia ruckeri Isolates Recovered from Diseased Atlantic Salmon (Salmo salar) in Scotland Are More Diverse than Those from Rainbow Trout (Oncorhynchus mykiss) and Represent Distinct Subpopulations

Ormsby

Caws

Burchmore

et al. 2016

Appl Environ Microbiol

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“…In addition, an Edwardsiella hoshinae strain (ATCC 35051), an Escherichia coli strain (ATCC 25922), 2 Flavobacterium columnare strains (94-081 and ATCC 49512), and 2 Aeromonas hydrophila strains (ML 09-119 and TN 97-08), including a highly virulent strain (ML 09-119) attributed to disease outbreaks in farm-raised catfish 18 were also included in the validation process. …”

Section: Bacterial Cultures and Isolation Of Genomic Dnamentioning

confidence: 99%

Real-time polymerase chain reaction assays for the detection and quantification of Edwardsiella tarda, Edwardsiella piscicida, and Edwardsiella piscicida–like species in catfish tissues and pond water

et al. 2015

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Abstract.Researchers have proposed the adoption of 3 distinct genetic taxa among bacteria previously classified as Edwardsiella tarda; namely E. tarda, E. piscicida, and a taxon presently termed E. piscicida-like. Individual real-time polymerase chain reaction (qPCR) assays were developed, based on published primers, for E. tarda, E. piscicida, and E. piscicida-like sp. to provide rapid quantitative confirmatory tests for these phenotypically ambiguous bacteria. The qPCR assays were shown to be repeatable and reproducible, with high degrees of sensitivity and specificity. Each assay showed a linear dynamic range covering 8 orders of magnitude and a sensitivity limit of 5 copies of target DNA in a 15-µL reaction. In addition, each assay was found specific to their respective targets with no observed amplification from nontarget organisms, including the closely related E. ictaluri and E. hoshinae. Under the conditions used in this study, the 3 assays had a quantifiable limit ranging from 10 3 (E. piscicida) to 10 2 (E. piscicida-like and E. tarda) colony forming units in kidney tissue biopsies (approximately 25 mg), pond water samples (35 mL), and broth culture (20 µL). In experimental challenges, the assays were able to detect their respective targets in both clinically and subclinically infected channel catfish (Ictalurus punctatus) fingerlings. In addition to quantifying target bacteria from various substrates, the assays provide rapid identification, differentiation, and confirmation of the phenotypically indistinguishable E. tarda, E. piscicida, and E. piscicida-like sp., a valuable tool for diagnostic assessments. 13 Speciesspecific polymerase chain reaction (PCR) assays targeting the fimbrial gene cluster were developed for each individual taxa and were demonstrated specific to their respective target organisms. 13,26 In the current study, real-time PCR (qPCR) assays were developed using these established primer sets and were validated for the detection and quantification of E. tarda, E. piscicida, and E. piscicida-like sp. from catfish kidney tissues, pond water, and broth culture. Materials and methods Bacterial cultures and isolation of genomic DNAThe Edwardsiella strains used in the validation of the assays in the current study were characterized as part of an earlier study 13 and identified by gyrB sequencing and speciesspecific PCR (Table 1). In addition, an Edwardsiella hoshinae strain (ATCC 35051), an Escherichia coli strain (ATCC 25922), 2 Flavobacterium columnare strains (94-081 and ATCC 49512), and 2 Aeromonas hydrophila strains (ML 09-119 and TN 97-08), including a highly virulent strain (ML 09-119) attributed to disease outbreaks in farm-raised catfish 18 were also included in the validation process. Design of primer and probe setsThe development of the qPCR assays specific to E. tarda, E. piscicida, and E. piscicida-like sp. was based on previously published PCR primers. 13,26 Oligonucleotide probes corresponding to each primer set were designed using primer design software 25 and synthesized...

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“…AspecGI-8 includes a novel cluster of genes involved in the biosynthesis of the O-antigen polysaccharide that differs in genetic organization compared to the corresponding genes in other Aeromonas strains (77). AspecGI-9 has a Vibrio core oligosaccharide biosynthesis gene cluster and also encodes transcriptional regulators, including a phage regulator, and carries two genes similar to those of restriction modification systems.…”

Section: Melanin Biosynthesis One Of the Most Distinctive Phenotypicmentioning

confidence: 99%

Living in an Extremely Polluted Environment: Clues from the Genome of Melanin-Producing Aeromonas salmonicida subsp. pectinolytica 34mel ^T

Paván

Pavan

López

et al. 2015

Appl Environ Microbiol

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d Aeromonas salmonicida subsp. pectinolytica 34mel T can be considered an extremophile due to the characteristics of the heavily polluted river from which it was isolated. While four subspecies of A. salmonicida are known fish pathogens, 34melT belongs to the only subspecies isolated solely from the environment. Genome analysis revealed a high metabolic versatility, the capability to cope with diverse stress agents, and the lack of several virulence factors found in pathogenic Aeromonas. The most relevant phenotypic characteristics of 34mel T are pectin degradation, a distinctive trait of A. salmonicida subsp. pectinolytica, and melanin production. Genes coding for three pectate lyases were detected in a cluster, unique to this microorganism, that contains all genes needed for pectin degradation. Melanin synthesis in 34melT is hypothesized to occur through the homogentisate pathway, as no tyrosinases or laccases were detected and the homogentisate 1,2-dioxygenase gene is inactivated by a transposon insertion, leading to the accumulation of the melanin precursor homogentisate. Comparative genome analysis of other melanogenic Aeromonas strains revealed that this gene was inactivated by transposon insertions or point mutations, indicating that melanin biosynthesis in Aeromonas occurs through the homogentisate pathway. Horizontal gene transfer could have contributed to the adaptation of 34mel T to a highly polluted environment, as 13 genomic islands were identified in its genome, some of them containing genes coding for fitness-related traits. Heavy metal resistance genes were also found, along with others associated with oxidative and nitrosative stresses. These characteristics, together with melanin production and the ability to use different substrates, may explain the ability of this microorganism to live in an extremely polluted environment.A eromonas salmonicida subsp. pectinolytica 34melT is a melanin-producing Aeromonas strain that degrades polypectate, which is an unusual characteristic among Aeromonas species (1). It was isolated from the heavily polluted water of the Riachuelo, the last part of the Matanza River, located in Buenos Aires, Argentina. This river has received the effluents of hundreds of tanneries and other industries, as well as urban sewage and fuels, for more than a century. Among the contaminants found in this environment, which has high organic matter and low dissolved oxygen contents, are hydrocarbons, polychlorinated biphenyls, pesticides, arsenic, and heavy metals, such as chromium, lead, copper, mercury, and nickel (2-4). A molecular analysis of the microbial diversity of river water and sediments from the isolation site showed the presence of bacteria belonging to several taxa. Analysis of 16S rRNA gene sequences revealed the presence of bacteria belonging to the Beta-, Gamma-, and Epsilonproteobacteria in the water, as well as a higher level of diversity in the sediments, in which Alpha-, Beta-, Gamma-, and Deltaproteobacteria, Firmicutes, and Bacteroidetes were detected (5).The ge...

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Implication of Lateral Genetic Transfer in the Emergence of Aeromonas hydrophila Isolates of Epidemic Outbreaks in Channel Catfish

Cited by 85 publications

References 69 publications

Yersinia ruckeri Isolates Recovered from Diseased Atlantic Salmon (Salmo salar) in Scotland Are More Diverse than Those from Rainbow Trout (Oncorhynchus mykiss) and Represent Distinct Subpopulations

Yersinia ruckeri Isolates Recovered from Diseased Atlantic Salmon (Salmo salar) in Scotland Are More Diverse than Those from Rainbow Trout (Oncorhynchus mykiss) and Represent Distinct Subpopulations

Real-time polymerase chain reaction assays for the detection and quantification of Edwardsiella tarda, Edwardsiella piscicida, and Edwardsiella piscicida–like species in catfish tissues and pond water

Living in an Extremely Polluted Environment: Clues from the Genome of Melanin-Producing Aeromonas salmonicida subsp. pectinolytica 34mel ^T

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Implication of Lateral Genetic Transfer in the Emergence of Aeromonas hydrophila Isolates of Epidemic Outbreaks in Channel Catfish

Cited by 85 publications

References 69 publications

Yersinia ruckeri Isolates Recovered from Diseased Atlantic Salmon (Salmo salar) in Scotland Are More Diverse than Those from Rainbow Trout (Oncorhynchus mykiss) and Represent Distinct Subpopulations

Yersinia ruckeri Isolates Recovered from Diseased Atlantic Salmon (Salmo salar) in Scotland Are More Diverse than Those from Rainbow Trout (Oncorhynchus mykiss) and Represent Distinct Subpopulations

Real-time polymerase chain reaction assays for the detection and quantification of Edwardsiella tarda, Edwardsiella piscicida, and Edwardsiella piscicida–like species in catfish tissues and pond water

Living in an Extremely Polluted Environment: Clues from the Genome of Melanin-Producing Aeromonas salmonicida subsp. pectinolytica 34mel T

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Living in an Extremely Polluted Environment: Clues from the Genome of Melanin-Producing Aeromonas salmonicida subsp. pectinolytica 34mel ^T