Aeromonas salmonicida: Genomics, Taxonomy, Diversity, Pathogenesis, Treatments and Beyond

A special issue of Microorganisms (ISSN 2076-2607). This special issue belongs to the section "Environmental Microbiology".

Deadline for manuscript submissions: closed (30 November 2022) | Viewed by 14287

Special Issue Editor


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Guest Editor
Institut de Biologie Intégrative et des Systèmes (IBIS), Université Laval, Quebec, QC G1V 0A6, Canada
Interests: Aeromonas salmonicida; type three secretion system; antibiotic resistance; plasmid; insertion sequence; genomic island; phage; bacterial lifestyle; virulence; Dictyostelium discoideum

Special Issue Information

Dear Colleagues,

Aeromonas salmonicida is a Gram-negative bacterium initially well known as a fish pathogen. However, especially in the last decade, thanks to genomic sequencing, this bacterial species has revealed its great diversity. In A. salmonicida, we find psychrophilic subspecies infecting fish of different species, but more particularly salmonids, which gave the name to this bacterial species. There is also a mesophilic subspecies found in the environment, as well as a myriad of mesophilic strains not yet classified at the taxonomic level which come, for example, from food, human samples, sick fish, or a sick bird. Even greater diversity in mesophilic strains of A. salmonicida is expected and will surely be revealed in the next few years. The health risks of this bacterial species are probably underestimated as much for infections in animals as in humans. With a genome rich in mobile genetic elements (plasmids, prophages, genomic islands, etc.), A. salmonicida strains exhibit resistance to numerous antibiotics, which is forcing the development of new alternative therapeutic approaches to combat the infections caused by these bacteria. This Special Issue aims to cover all recent developments in relation to research on A. salmonicida. This includes but is not limited to its taxonomy, virulence, antibiotic resistance, metabolism, ecological context, and treatments for infections caused by this species.

Prof. Dr. Steve Charette
Guest Editor

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Published Papers (6 papers)

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Editorial

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3 pages, 203 KiB  
Editorial
Aeromonas salmonicida: Genomics, Taxonomy, Diversity, Pathogenesis, Treatments and Beyond
by Steve J. Charette
Microorganisms 2023, 11(5), 1189; https://doi.org/10.3390/microorganisms11051189 - 1 May 2023
Viewed by 1055
Abstract
For a long time, the bacterial species Aeromonas salmonicida seemed to be limited to a regrouping of psychrophilic subspecies that infect fish, particularly salmonids [...] Full article

Research

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32 pages, 9416 KiB  
Article
Multi-Organ Transcriptome Response of Lumpfish (Cyclopterus lumpus) to Aeromonas salmonicida Subspecies salmonicida Systemic Infection
by Setu Chakraborty, Ahmed Hossain, Trung Cao, Hajarooba Gnanagobal, Cristopher Segovia, Stephen Hill, Jennifer Monk, Jillian Porter, Danny Boyce, Jennifer R. Hall, Gabriela Bindea, Surendra Kumar and Javier Santander
Microorganisms 2022, 10(11), 2113; https://doi.org/10.3390/microorganisms10112113 - 26 Oct 2022
Cited by 6 | Viewed by 2174
Abstract
Lumpfish is utilized as a cleaner fish to biocontrol sealice infestations in Atlantic salmon farms. Aeromonas salmonicida, a Gram-negative facultative intracellular pathogen, is the causative agent of furunculosis in several fish species, including lumpfish. In this study, lumpfish were intraperitoneally injected with [...] Read more.
Lumpfish is utilized as a cleaner fish to biocontrol sealice infestations in Atlantic salmon farms. Aeromonas salmonicida, a Gram-negative facultative intracellular pathogen, is the causative agent of furunculosis in several fish species, including lumpfish. In this study, lumpfish were intraperitoneally injected with different doses of A. salmonicida to calculate the LD50. Samples of blood, head-kidney, spleen, and liver were collected at different time points to determine the infection kinetics. We determined that A. salmonicida LD50 is 102 CFU per dose. We found that the lumpfish head-kidney is the primary target organ of A. salmonicida. Triplicate biological samples were collected from head-kidney, spleen, and liver pre-infection and at 3- and 10-days post-infection for RNA-sequencing. The reference genome-guided transcriptome assembly resulted in 6246 differentially expressed genes. The de novo assembly resulted in 403,204 transcripts, which added 1307 novel genes not identified by the reference genome-guided transcriptome. Differential gene expression and gene ontology enrichment analyses suggested that A. salmonicida induces lethal infection in lumpfish by uncontrolled and detrimental blood coagulation, complement activation, inflammation, DNA damage, suppression of the adaptive immune system, and prevention of cytoskeleton formation. Full article
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21 pages, 2642 KiB  
Article
Enhanced Hemolytic Activity of Mesophilic Aeromonas salmonicida SRW-OG1 Is Brought about by Elevated Temperatures
by Yunong Chen, Jiajia Wang, Hongyan Cai, Mao Lin, Youyu Zhang and Lixing Huang
Microorganisms 2022, 10(10), 2033; https://doi.org/10.3390/microorganisms10102033 - 14 Oct 2022
Cited by 7 | Viewed by 1622
Abstract
Aeromonas salmonicida is a well-known cold-water pathogenic bacterium. Previously, we reported the first isolation of pathogenic A. salmonicida from diseased Epinephelus coioides, a kind of warm-water fish, and it was proved to be a putative mesophilic strain with potent pathogenicity to humans. [...] Read more.
Aeromonas salmonicida is a well-known cold-water pathogenic bacterium. Previously, we reported the first isolation of pathogenic A. salmonicida from diseased Epinephelus coioides, a kind of warm-water fish, and it was proved to be a putative mesophilic strain with potent pathogenicity to humans. In order to investigate the mechanisms underlying mesophilic growth ability and virulence, the transcriptome of A. salmonicida SRW-OG1 at 18, 28, and 37 °C was analyzed. The transcriptome of A. salmonicida SRW-OG1 at different temperatures showed a clear separation boundary, which might provide valuable information for the temperature adaptation and virulence regulation of A. salmonicida SRW-OG1. Interestingly, aerA and hlyA, the hemolytic genes encoding aerolysin and hemolysin, were found to be significantly up-regulated at 28 and 37 °C. Since aerolysin and hemolysin are the most well-known and -characterized virulence factors of pathogenic Aeromonas strains, the induction of aerA and hlyA was associated with the mesophilic virulence. Further study proved that the extracellular products (ECPs) purchased from A. salmonicida SRW-OG1 cultured at 28 and 37 °C showed elevated hemolytic activity and virulence than those at 18 °C. Moreover, the silence of aerA and hlyA led to significantly decreased hemolysis and virulence. Taken together, our results revealed that the mesophilic virulence of A. salmonicida SRW-OG1 might be due to the enhanced expression of aerA and hlyA induced by elevated temperatures. Full article
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22 pages, 3663 KiB  
Article
Effect of Iron Limitation, Elevated Temperature, and Florfenicol on the Proteome and Vesiculation of the Fish Pathogen Aeromonas salmonicida
by Tobias Kroniger, Mina Mehanny, Rabea Schlüter, Anke Trautwein-Schult, Bernd Köllner and Dörte Becher
Microorganisms 2022, 10(9), 1735; https://doi.org/10.3390/microorganisms10091735 - 27 Aug 2022
Cited by 4 | Viewed by 2334
Abstract
We analyzed the proteomic response of the Gram-negative fish pathogen A. salmonicida to iron limitation, an elevated incubation temperature, and the antibiotic florfenicol. Proteins from different subcellular fractions (cytosol, inner membrane, outer membrane, extracellular and outer membrane vesicles) were enriched and analyzed. We [...] Read more.
We analyzed the proteomic response of the Gram-negative fish pathogen A. salmonicida to iron limitation, an elevated incubation temperature, and the antibiotic florfenicol. Proteins from different subcellular fractions (cytosol, inner membrane, outer membrane, extracellular and outer membrane vesicles) were enriched and analyzed. We identified several iron-regulated proteins that were not reported in the literature for A. salmonicida before. We could also show that hemolysin, an oxidative-stress-resistance chaperone, a putative hemin receptor, an M36 peptidase, and an uncharacterized protein were significantly higher in abundance not only under iron limitation but also with an elevated incubation temperature. This may indicate that these proteins involved in the infection process of A. salmonicida are induced by both factors. The analysis of the outer membrane vesicles (OMVs) with and without applied stresses revealed significant differences in the proteomes. OMVs were smaller and contained more cytoplasmic proteins after antibiotic treatment. After cultivation with low iron availability, several iron-regulated proteins were found in the OMVs, indicating that A. salmonicida OMVs potentially have a function in iron acquisition, as reported for other bacteria. The presence of iron-regulated transporters further indicates that OMVs obtained from ‘stressed’ bacteria might be suitable vaccine candidates that induce a protective anti-virulence immune response. Full article
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29 pages, 4855 KiB  
Article
Comparative Genomics of Typical and Atypical Aeromonas salmonicida Complete Genomes Revealed New Insights into Pathogenesis Evolution
by Ignacio Vasquez, Ahmed Hossain, Hajarooba Gnanagobal, Katherinne Valderrama, Briony Campbell, Michael Ness, Steve J. Charette, Anthony K. Gamperl, Rocco Cipriano, Cristopher Segovia and Javier Santander
Microorganisms 2022, 10(1), 189; https://doi.org/10.3390/microorganisms10010189 - 15 Jan 2022
Cited by 15 | Viewed by 3288
Abstract
Aeromonas salmonicida is a global distributed Gram-negative teleost pathogen, affecting mainly salmonids in fresh and marine environments. A. salmonicida strains are classified as typical or atypical depending on their origin of isolation and phenotype. Five subspecies have been described, where A. salmonicida [...] Read more.
Aeromonas salmonicida is a global distributed Gram-negative teleost pathogen, affecting mainly salmonids in fresh and marine environments. A. salmonicida strains are classified as typical or atypical depending on their origin of isolation and phenotype. Five subspecies have been described, where A. salmonicida subsp. salmonicida is the only typical subspecies, and the subsp. achromogenes, masoucida, smithia, and pectinolytica are considered atypical. Genomic differences between A. salmonicida subsp. salmonicida isolates and their relationship with the current classification have not been explored. Here, we sequenced and compared the complete closed genomes of four virulent strains to elucidate their molecular diversity and pathogenic evolution using the more accurate genomic information so far. Phenotypes, biochemical, and enzymatic profiles were determined. PacBio and MiSeq sequencing platforms were utilized for genome sequencing. Comparative genomics showed that atypical strains belong to the subsp. salmonicida, with 99.55% ± 0.25% identity with each other, and are closely related to typical strains. The typical strain A. salmonicida J223 is closely related to typical strains, with 99.17% identity with the A. salmonicida A449. Genomic differences between atypical and typical strains are strictly related to insertion sequences (ISs) activity. The absence and presence of genes encoding for virulence factors, transcriptional regulators, and non-coding RNAs are the most significant differences between typical and atypical strains that affect their phenotypes. Plasmidome plays an important role in A. salmonicida virulence and genome plasticity. Here, we determined that typical strains harbor a larger number of plasmids and virulence-related genes that contribute to its acute virulence. In contrast, atypical strains harbor a single, large plasmid and a smaller number of virulence genes, reflected by their less acute virulence and chronic infection. The relationship between phenotype and A. salmonicida subspecies’ taxonomy is not evident. Comparative genomic analysis based on completed genomes revealed that the subspecies classification is more of a reflection of the ecological niche occupied by bacteria than their divergences at the genomic level except for their accessory genome. Full article
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Other

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8 pages, 730 KiB  
Perspective
To Be or Not to Be Mesophilic, That Is the Question for Aeromonas salmonicida
by Antony T. Vincent and Steve J. Charette
Microorganisms 2022, 10(2), 240; https://doi.org/10.3390/microorganisms10020240 - 22 Jan 2022
Cited by 11 | Viewed by 2032
Abstract
The bacterium Aeromonas salmonicida has long been known to be one of the most feared pathogens in fish farming. However, the more we discover about this bacterial species, the more we question whether it is really exclusively an aquatic pathogen. In recent years, [...] Read more.
The bacterium Aeromonas salmonicida has long been known to be one of the most feared pathogens in fish farming. However, the more we discover about this bacterial species, the more we question whether it is really exclusively an aquatic pathogen. In recent years, it has become obvious that this bacterial species includes a myriad of strains with various lifestyle and ecological niches, including the well-known strict psychrophiles, the first bacteria known of the species, and the newly described mesophilic strains. The mesophiles are able to grow at low temperatures, but even better at temperatures of approximately 37 °C, which strict psychrophiles cannot do. In this perspective article, we address some aspects surrounding this dual lifestyle in A. salmonicida, including the impact of mobile genetic elements, and how future research around this bacterial species may focus on the psychrophilic/mesophilic dichotomy, which makes A. salmonicida an increasingly interesting and relevant model for the study of speciation. Full article
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