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An Update on Aeromonas

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A special issue of Microorganisms (ISSN 2076-2607).

Deadline for manuscript submissions: closed (31 July 2019) | Viewed by 65149

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Prof. Dr. María José Figueras

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Unit of Microbiology, Faculty of Medicine and Health Sciences, Pere Virgili Health Research Institute, University Rovira i Virgili, 43003 Tarragona, Spain
Interests: taxonomy; bacteria; virulence
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Dr. Marta Sanchis

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Unit of Microbiology, Institut d'Investigació Sanitària Pere Virgili, University Rovira i Virgili, Reus, Spain
Interests: immunology of infectious diseases; mycology; opportunistic fungi; in vivo models; environmental microbiology; basic molecular biology techniques; antifungal susceptibility testing; bacterial infections and mycoses
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Dr. Ana Fernández-Bravo

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Unit of Microbiology, Faculty of Medicine and Health Sciences, Pere Virgili Health Research Institute, University Rovira i Virgili, 43003 Tarragona, Spain
Interests: bacteria; virulence; immune system
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Dear Colleagues,

The genus Aeromonas includes Gram-negative, oxidase-positive bacilli that are autochthonous of aquatic environments. However, they can be isolated from an extensive variety of habitats including clinical samples. Until now, 32 species has been described and four are in process of description. Some species are considered to be emerging pathogens causing a wide spectrum of diseases, mainly gastroenteritis and septicemia, in immunocompromised patients and wound infections in healthy people. In addition, some species can produce diseases in fish, producing important economic losses in aquaculture. The presence of several virulence factors allow these bacteria to colonize, invade and overcome the immune host response. The strains associated with clinical cases correspond mainly (96.5%) to four species: A. caviae (29.9%), A. dhakensis (26.3%), A. veronii (24.8%) and A. hydrophila (15.5%). Based on this, Aeromonas infections will remain a health problem in the near future, considering the increased life expectancy that will result in more elderly persons with potential underlying diseases. This Special Issue will provide an updated, global review of the taxonomy, ecology, epidemiology and pathogenicity of the genus Aeromonas.

Prof. María José Figueras
Dr. Marta Sanchis
Ms. Ana Fernández-Bravo
Guest Editors

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Keywords

Aeromonas
infections
ecology
virulence factors
pathogenicity
taxonomy
epidemiology

Related Special Issue

An Update on Aeromonas 2.0 in Microorganisms (1 article)

Published Papers (9 papers)

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12 pages, 2286 KiB

Open AccessArticle

A Mesophilic Aeromonas salmonicida Strain Isolated from an Unsuspected Host, the Migratory Bird Pied Avocet

by Antony T. Vincent, Alex Bernatchez, Joachim Frey and Steve J. Charette

Microorganisms 2019, 7(12), 592; https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms7120592 - 20 Nov 2019

Cited by 16 | Viewed by 3645

Abstract

Aeromonas salmonicida is a Gram-negative bacterium, known as a fish pathogen since its discovery. Although the species was initially considered psychrophilic, a mesophilic subspecies (pectinolytica) and many other mesophilic strains still not attributed to subspecies have been described in the last two decades. These mesophilic strains were sampled from various sources, including humans, and some of them are known to be pathogenic. In this study, we describe a strain, JF2480, which was isolated from the spleen, and also found the kidney and liver of a dead pied avocet (Recurvirostra avosetta), a type of migratory bird inhabiting aquatic environments. A core genome phylogenomic analysis suggests that JF2480 is taxonomically distant from other known A. salmonicida subspecies. The genome sequence confirms that the strain possesses key virulence genes that are present in the typical A. salmonicida psychrophilic subspecies, with the exception of the genes encoding the type three secretion system (T3SS). Bacterial virulence assays conducted on the surrogate host Dictyostelium discoideum amoeba confirmed that the strain is virulent despite the lack of T3SS. Bacterial growth curves showed that strain JF2480 grow well at 40 °C, the body temperature of the pied avocet, and even faster at 41 °C, compared to other mesophilic strains. Discovery of this strain further demonstrates the extent of the phylogenomic tree of this species. This study also suggests that A. salmonicida can infect a wider array of hosts than previously suspected and that we need to rethink the way we perceive A. salmonicida’s natural environment. Full article

(This article belongs to the Special Issue An Update on Aeromonas)

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24 pages, 2128 KiB

Open AccessArticle

Comparative Study on A Novel Pathogen of European Seabass. Diversity of Aeromonas veronii in the Aegean Sea

by Maria Smyrli, Adriana Triga, Nancy Dourala, Panos Varvarigos, Michael Pavlidis, Viet Ha Quoc and Pantelis Katharios

Microorganisms 2019, 7(11), 504; https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms7110504 - 29 Oct 2019

Cited by 17 | Viewed by 4330

Abstract

Aeromonas veronii is an emerging pathogen causing severe pathology and mortalities in European seabass aquaculture in the Aegean Sea, Mediterranean. More than 50 strains of the pathogen were characterized biochemically and genetically in order to study the epidemiology of the disease, as well as the phylogeny and virulence of the bacterium. Based on the phenotypic characteristics, the isolates form three groups consisting of: (a) the West Aegean Sea, non-motile, non-pigment-producing strains, (b) the West Aegean Sea, motile, and pigment-producing strains and (c) the East Aegean Sea motile strains that produce minute amounts of pigment. All strains were highly similar at the genomic level; however, the pattern of West/East geographic origin was reflected in biochemical properties, in general genomic level comparison and in the putative virulent factors studied. Type VI secretion system was not detected in the western strains. The outer membrane protein (OMP) profile which contains proteins that are putative antigenic factors, was very similar between strains from the different areas. Although most of the OMPs were detected in all strains with great sequence similarity, diversification according to geographic origin was evident in known antigenic factors such as the maltoporin LamB. A systematic comparative analysis of the strains is presented and discussed in view of the emergence of A. veronii as a significant pathogen for the Mediterranean aquaculture. Full article

(This article belongs to the Special Issue An Update on Aeromonas)

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20 pages, 3488 KiB

Open AccessArticle

Aeromonas hydrophila, an Emerging Causative Agent of Freshwater-Farmed Whiteleg shrimp Litopenaeus vannamei

by Huihua Zhou, Chunlei Gai, Guifang Ye, Jian An, Kai Liu, La Xu and Haipeng Cao

Microorganisms 2019, 7(10), 450; https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms7100450 - 14 Oct 2019

Cited by 38 | Viewed by 5433

Abstract

Aeromonas hydrophila is a well-known bacterial pathogen associated with mass mortalities in aquaculture. Yet, few reports are available on whiteleg shrimp-pathogenic A. hydrophila. In the present study, a virulent isolate WS05 was confirmed as a causative agent of diseased freshwater-cultured whiteleg shrimp and showed a mean lethal dose (LD₅₀) value of 4.8 × 10⁴ CFU mL⁻¹. It was identified phenotypically and molecularly as an A. hydrophila strain, and exhibited susceptibility to several veterinary antibiotics extensively used in aquaculture, including cotrimoxazole, doxycycline, florfenicol, neomycin, and tetracycline. In view of the strongest inhibition zone of florfenicol against isolate WS05, the synergistic effect of the combinations of florfenicol and herb extracts was further evaluated, and the result indicated that Punica granatum extract was a potential synergist of florfenicol against isolate WS05 and the fractional inhibitory concentration index (FICI) for the florfenicol-P. granatum extract was calculated as 0.31. When combined with 7.81 mg mL⁻¹ P. granatum extract, the minimum inhibitory concentration (MIC) of florfenicol against isolate WS05 was reduced from 0.50 to 0.03 mg L⁻¹, and its activity against isolate WS05 was also enhanced with a significant reduction of ≥3.61 log in cell density after 24 h of treatment compared with that in the single drug treatment. In addition, the protective effect was potentiated by the combination of florfenicol and P. granatum extract, with a cumulative mortality of 36.66% (p < 0.05) and 33.33% (p < 0.05) lower than that in the single treatment with florfenicol and P. granatum extract after the challenge with isolate WS05 for seven days. As far as we know, this is the first study to describe whiteleg shrimp-pathogenic A. hydrophila and suggest P. granatum extract as a potential synergist of florfenicol against the A. hydrophila pathogen. Full article

(This article belongs to the Special Issue An Update on Aeromonas)

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13 pages, 2375 KiB

Open AccessArticle

The Metallochaperone Encoding Gene hypA Is Widely Distributed among Pathogenic Aeromonas spp. and Its Expression Is Increased under Acidic pH and within Macrophages

by Ana Fernández-Bravo, Loida López-Fernández and Maria José Figueras

Microorganisms 2019, 7(10), 415; https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms7100415 - 02 Oct 2019

Cited by 7 | Viewed by 2668

Abstract

Metallochaperones are essential proteins that insert metal ions or metal cofactors into specific enzymes, that after maturation will become metalloenzymes. One of the most studied metallochaperones is the nickel-binding protein HypA, involved in the maturation of nickel-dependent hydrogenases and ureases. HypA was previously described in the human pathogens Escherichia coli and Helicobacter pylori and was considered a key virulence factor in the latter. However, nothing is known about this metallochaperone in the species of the emerging pathogen genus Aeromonas. These bacteria are native inhabitants of aquatic environments, often associated with cases of diarrhea and wound infections. In this study, we performed an in silico study of the hypA gene on 36 Aeromonas species genomes, which showed the presence of the gene in 69.4% (25/36) of the Aeromonas genomes. The similarity of Aeromonas HypA proteins with the H. pylori orthologous protein ranged from 21−23%, while with that of E. coli it was 41−45%. However, despite this low percentage, Aeromonas HypA displays the conserved characteristic metal-binding domains found in the other pathogens. The transcriptional analysis enabled the determination of hypA expression levels under acidic and alkaline conditions and after macrophage phagocytosis. The transcriptional regulation of hypA was found to be pH-dependent, showing upregulation at acidic pH. A higher upregulation occurred after macrophage infection. This is the first study that provided evidence that the HypA metallochaperone in Aeromonas might play a role in acid tolerance and in the defense against macrophages. Full article

(This article belongs to the Special Issue An Update on Aeromonas)

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14 pages, 1188 KiB

Open AccessArticle

Wild Nutria (Myocastor coypus) Is a Potential Reservoir of Carbapenem-Resistant and Zoonotic Aeromonas spp. in Korea

by Se Ra Lim, Do-Hun Lee, Seon Young Park, Seungki Lee, Hyo Yeon Kim, Moo-Seung Lee, Jung Ro Lee, Jee Eun Han, Hye Kwon Kim and Ji Hyung Kim

Microorganisms 2019, 7(8), 224; https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms7080224 - 30 Jul 2019

Cited by 10 | Viewed by 3707

Abstract

The emergence and spread of antibiotic-resistant Aeromonas spp. is a serious public and animal health concern. Wild animals serve as reservoirs, vectors, and sentinels of these bacteria and can facilitate their transmission to humans and livestock. The nutria (Myocastor coypus), a semi-aquatic rodent, currently is globally considered an invasive alien species that has harmful impacts on natural ecosystems and carries various zoonotic aquatic pathogens. This study aimed to determine the prevalence of antibiotic-resistant zoonotic Aeromonas spp. in wild invasive nutrias captured in Korea during governmental eradication program. Three potential zoonotic Aeromonas spp. (A. hydrophila, A. caviae, and A. dhakensis) were identified among isolates from nutria. Some strains showed unexpected resistance to fluoroquinolones, third-generation cephalosporins, and carbapenems. In carbapenem-resistant isolates, the cphA gene, which is related to intrinsic resistance of Aeromonas to carbapenems, was identified, and phylogenetic analysis based on this gene revealed the presence of two major groups represented by A. hydrophila (including A. dhakensis) and other Aeromonas spp. These results indicate that wild nutrias in Korea are a potential reservoir of zoonotic and antibiotic-resistant Aeromonas spp. that can cause infection and treatment failure in humans. Thus, measures to prevent contact of wild nutrias with livestock and humans are needed. Full article

(This article belongs to the Special Issue An Update on Aeromonas)

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Review

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39 pages, 3365 KiB

Open AccessReview

An Update on the Genus Aeromonas: Taxonomy, Epidemiology, and Pathogenicity

by Ana Fernández-Bravo and Maria José Figueras

Microorganisms 2020, 8(1), 129; https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms8010129 - 17 Jan 2020

Cited by 300 | Viewed by 16089

Abstract

The genus Aeromonas belongs to the Aeromonadaceae family and comprises a group of Gram-negative bacteria widely distributed in aquatic environments, with some species able to cause disease in humans, fish, and other aquatic animals. However, bacteria of this genus are isolated from many other habitats, environments, and food products. The taxonomy of this genus is complex when phenotypic identification methods are used because such methods might not correctly identify all the species. On the other hand, molecular methods have proven very reliable, such as using the sequences of concatenated housekeeping genes like gyrB and rpoD or comparing the genomes with the type strains using a genomic index, such as the average nucleotide identity (ANI) or in silico DNA–DNA hybridization (isDDH). So far, 36 species have been described in the genus Aeromonas of which at least 19 are considered emerging pathogens to humans, causing a broad spectrum of infections. Having said that, when classifying 1852 strains that have been reported in various recent clinical cases, 95.4% were identified as only four species: Aeromonas caviae (37.26%), Aeromonas dhakensis (23.49%), Aeromonas veronii (21.54%), and Aeromonas hydrophila (13.07%). Since aeromonads were first associated with human disease, gastroenteritis, bacteremia, and wound infections have dominated. The literature shows that the pathogenic potential of Aeromonas is considered multifactorial and the presence of several virulence factors allows these bacteria to adhere, invade, and destroy the host cells, overcoming the immune host response. Based on current information about the ecology, epidemiology, and pathogenicity of the genus Aeromonas, we should assume that the infections these bacteria produce will remain a great health problem in the future. The ubiquitous distribution of these bacteria and the increasing elderly population, to whom these bacteria are an opportunistic pathogen, will facilitate this problem. In addition, using data from outbreak studies, it has been recognized that in cases of diarrhea, the infective dose of Aeromonas is relatively low. These poorly known bacteria should therefore be considered similarly as enteropathogens like Salmonella and Campylobacter. Full article

(This article belongs to the Special Issue An Update on Aeromonas)

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11 pages, 1616 KiB

Open AccessReview

Horizontal Gene Transfer and Its Association with Antibiotic Resistance in the Genus Aeromonas spp.

by J. Manuel Bello-López, Omar A. Cabrero-Martínez, Gabriela Ibáñez-Cervantes, Cecilia Hernández-Cortez, Leda I. Pelcastre-Rodríguez, Luis U. Gonzalez-Avila and Graciela Castro-Escarpulli

Microorganisms 2019, 7(9), 363; https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms7090363 - 18 Sep 2019

Cited by 97 | Viewed by 18235

Abstract

The evolution of multidrug resistant bacteria to the most diverse antimicrobials known so far pose a serious problem to global public health. Currently, microorganisms that develop resistant phenotypes to multiple drugs are associated with high morbidity and mortality. This resistance is encoded by a group of genes termed ‘bacterial resistome’, divided in intrinsic and extrinsic resistome. The first one refers to the resistance displayed on an organism without previous exposure to an antibiotic not involving horizontal genetic transfer, and it can be acquired via mutations. The latter, on the contrary, is acquired exclusively via horizontal genetic transfer involving mobile genetic elements that constitute the ‘bacterial mobilome’. This transfer is mediated by three different mechanisms: transduction, transformation, and conjugation. Recently, a problem of public health due to implications in the emergence of multi-drug resistance in Aeromonas spp. strains in water environments has been described. This is derived from the genetic material transfer via conjugation events. This is important, since bacteria that have acquired antibiotic resistance in natural environments can cause infections derived from their ingestion or direct contact with open wounds or mucosal tissue, which in turn, by their resistant nature, makes their eradication complex. Implications of the emergence of resistance in Aeromonas spp. by horizontal gene transfer on public health are discussed. Full article

(This article belongs to the Special Issue An Update on Aeromonas)

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25 pages, 343 KiB

Open AccessReview

The Significance of Mesophilic Aeromonas spp. in Minimally Processed Ready-to-Eat Seafood

by Sunniva Hoel, Olav Vadstein and Anita N. Jakobsen

Microorganisms 2019, 7(3), 91; https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms7030091 - 23 Mar 2019

Cited by 50 | Viewed by 7225

Abstract

Minimally processed and ready-to-eat (RTE) seafood products are gaining popularity because of their availability in retail stores and the consumers’ perception of convenience. Products that are subjected to mild processing and products that do not require additional heating prior to consumption are eaten by an increasing proportion of the population, including people that are more susceptible to foodborne disease. Worldwide, seafood is an important source of foodborne outbreaks, but the exact burden is not known. The increased interest in seafood products for raw consumption introduces new food safety issues that must be addressed by all actors in the food chain. Bacteria belonging to genus Aeromonas are ubiquitous in marine environments, and Aeromonas spp. has held the title “emerging foodborne pathogen” for more than a decade. Given its high prevalence in seafood and in vegetables included in many RTE seafood meals, the significance of Aeromonas as a potential foodborne pathogen and a food spoilage organism increases. Some Aeromonas spp. can grow relatively uninhibited in food during refrigeration under a broad range of pH and NaCl concentrations, and in various packaging atmospheres. Strains of several Aeromonas species have shown spoilage potential by the production of spoilage associated metabolites in various seafood products, but the knowledge on spoilage in cold water fish species is scarce. The question about the significance of Aeromonas spp. in RTE seafood products is challenged by the limited knowledge on how to identify the truly virulent strains. The limited information on clinically relevant strains is partly due to few registered outbreaks, and to the disputed role as a true foodborne pathogen. However, it is likely that illness caused by Aeromonas might go on undetected due to unreported cases and a lack of adequate identification schemes. A rather confusing taxonomy and inadequate biochemical tests for species identification has led to a biased focus towards some Aeromonas species. Over the last ten years, several housekeeping genes has replaced the 16S rRNA gene as suitable genetic markers for phylogenetic analysis. The result is a more clear and robust taxonomy and updated knowledge on the currently circulating environmental strains. Nevertheless, more knowledge on which factors that contribute to virulence and how to control the potential pathogenic strains of Aeromonas in perishable RTE seafood products are needed. Full article

(This article belongs to the Special Issue An Update on Aeromonas)

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6 pages, 581 KiB

Open AccessCase Report

A Case of Aeromonas trota in an Immunocompromised Patient with Diarrhea

by Ana Fernández-Bravo, Isabel Fort-Gallifa, Frederic Ballester, Isabel Pujol, Frederic Gomez-Bertomeu, Mariola Domínguez, Miquel Micó, Eva Alcoceba, Josep Maria Simó-Sisó and Maria José Figueras

Microorganisms 2020, 8(3), 399; https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms8030399 - 12 Mar 2020

Cited by 6 | Viewed by 2599

Abstract

According to recent literature, 95.4% of the Aeromonas strains associated with human clinical cases correspond to four species: Aeromonas caviae, Aeromonas dhakensis, Aeromonas veronii and Aeromonas hydrophila. However, other less prevalent species such as Aeromonas trota, are also described from clinical samples. Based on its low incidence, the latter species can be regarded as rare and it is the only Aeromonas species susceptible to ampicillin. From the taxonomic point of view, A. trota is considered a synonym of the species Aeromonas enteropelogenes. The objective of this study is to present a new clinical case associated with A. trota in order to increase the knowledge about this species. The strain was recovered from the feces of a 69-year-old patient with a diarrheal syndrome and peritoneal psammocarcinoma. The preliminary identification as Aeromonas sp. was obtained with the API 20E, but it was characterized as Aeromonas jandei and also as Aeromonas enteropelogenes with different scores with the matrix-assisted laser desorption ionization time of flight (MALDI-TOF). Based on the sequence of the rpoD gene, it was confirmed to be A. trota. The antimicrobial resistance pattern showed that the strain was susceptible to ampicillin, penicillins in combination with beta-lactamase inhibitors, quinolones, carbapenems, aminoglycosides and cephalosporins, except cephalothin. In conclusion, the recognition of an Aeromonas strain susceptible to ampicillin should alert the clinical microbiologist of the possible involvement of this rare species. Furthermore, the MALDI-TOF database should be updated indicating that the species A. enteropelogenes, is a synonym of A. trota. Full article

(This article belongs to the Special Issue An Update on Aeromonas)

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