Functional genomic characterization of virulence factors from necrotizing fasciitis-causing strains of Aeromonas hydrophila

Christopher J. Grim, Elena V. Kozlova, Duraisamy Ponnusamy, Eric C. Fitts, Jian Sha, Michelle L. Kirtley, Christina J. van Lier, Bethany L. Tiner, Tatiana E. Erova, Sandeep J. Joseph, Timothy D. Read, Joshua R. Shak, Sam W. Joseph, Ed Singletary, Tracy Felland, Wallace B. Baze, Amy J. Horneman, Ashok Chopra

Research output: Contribution to journalArticle

22 Citations (Scopus)

Abstract

The genomes of 10 Aeromonas isolates identified and designated Aeromonas hydrophila WI, Riv3, and NF1 to NF4; A. dhakensis SSU; A. jandaei Riv2; and A. caviae NM22 and NM33 were sequenced and annotated. Isolates NF1 to NF4 were from a patient with necrotizing fasciitis (NF). Two environmental isolates (Riv2 and -3) were from the river water from which the NF patient acquired the infection. While isolates NF2 to NF4 were clonal, NF1 was genetically distinct. Outside the conserved core genomes of these 10 isolates, several unique genomic features were identified. The most virulent strains possessed one of the following four virulence factors or a combination of them: cytotoxic enterotoxin, exotoxin A, and type 3 and 6 secretion system effectors AexU and Hcp. In a septicemic-mouse model, SSU, NF1, and Riv2 were the most virulent, while NF2 was moderately virulent. These data correlated with high motility and biofilm formation by the former three isolates. Conversely, in a mouse model of intramuscular infection, NF2 was much more virulent than NF1. Isolates NF2, SSU, and Riv2 disseminated in high numbers from the muscular tissue to the visceral organs of mice, while NF1 reached the liver and spleen in relatively lower numbers on the basis of colony counting and tracking of bioluminescent strains in real time by in vivo imaging. Histopathologically, degeneration of myofibers with significant infiltration of polymorphonuclear cells due to the highly virulent strains was noted. Functional genomic analysis provided data that allowed us to correlate the highly infectious nature of Aeromonas pathotypes belonging to several different species with virulence signatures and their potential ability to cause NF.

Original languageEnglish (US)
Pages (from-to)4162-4183
Number of pages22
JournalApplied and Environmental Microbiology
Volume80
Issue number14
DOIs
StatePublished - 2014

Fingerprint

Aeromonas hydrophila
Necrotizing Fasciitis
Aeromonas
Virulence Factors
virulence
Aeromonas jandaei
genomics
genome
animal models
Aeromonas punctata
pathotype
exotoxins
pathotypes
enterotoxins
motility
river water
secretion
infection
Genome
biofilm

ASJC Scopus subject areas

  • Applied Microbiology and Biotechnology
  • Food Science
  • Biotechnology
  • Ecology

Cite this

Functional genomic characterization of virulence factors from necrotizing fasciitis-causing strains of Aeromonas hydrophila. / Grim, Christopher J.; Kozlova, Elena V.; Ponnusamy, Duraisamy; Fitts, Eric C.; Sha, Jian; Kirtley, Michelle L.; van Lier, Christina J.; Tiner, Bethany L.; Erova, Tatiana E.; Joseph, Sandeep J.; Read, Timothy D.; Shak, Joshua R.; Joseph, Sam W.; Singletary, Ed; Felland, Tracy; Baze, Wallace B.; Horneman, Amy J.; Chopra, Ashok.

In: Applied and Environmental Microbiology, Vol. 80, No. 14, 2014, p. 4162-4183.

Research output: Contribution to journalArticle

Grim, CJ, Kozlova, EV, Ponnusamy, D, Fitts, EC, Sha, J, Kirtley, ML, van Lier, CJ, Tiner, BL, Erova, TE, Joseph, SJ, Read, TD, Shak, JR, Joseph, SW, Singletary, E, Felland, T, Baze, WB, Horneman, AJ & Chopra, A 2014, 'Functional genomic characterization of virulence factors from necrotizing fasciitis-causing strains of Aeromonas hydrophila', Applied and Environmental Microbiology, vol. 80, no. 14, pp. 4162-4183. https://doi.org/10.1128/AEM.00486-14
Grim, Christopher J. ; Kozlova, Elena V. ; Ponnusamy, Duraisamy ; Fitts, Eric C. ; Sha, Jian ; Kirtley, Michelle L. ; van Lier, Christina J. ; Tiner, Bethany L. ; Erova, Tatiana E. ; Joseph, Sandeep J. ; Read, Timothy D. ; Shak, Joshua R. ; Joseph, Sam W. ; Singletary, Ed ; Felland, Tracy ; Baze, Wallace B. ; Horneman, Amy J. ; Chopra, Ashok. / Functional genomic characterization of virulence factors from necrotizing fasciitis-causing strains of Aeromonas hydrophila. In: Applied and Environmental Microbiology. 2014 ; Vol. 80, No. 14. pp. 4162-4183.
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abstract = "The genomes of 10 Aeromonas isolates identified and designated Aeromonas hydrophila WI, Riv3, and NF1 to NF4; A. dhakensis SSU; A. jandaei Riv2; and A. caviae NM22 and NM33 were sequenced and annotated. Isolates NF1 to NF4 were from a patient with necrotizing fasciitis (NF). Two environmental isolates (Riv2 and -3) were from the river water from which the NF patient acquired the infection. While isolates NF2 to NF4 were clonal, NF1 was genetically distinct. Outside the conserved core genomes of these 10 isolates, several unique genomic features were identified. The most virulent strains possessed one of the following four virulence factors or a combination of them: cytotoxic enterotoxin, exotoxin A, and type 3 and 6 secretion system effectors AexU and Hcp. In a septicemic-mouse model, SSU, NF1, and Riv2 were the most virulent, while NF2 was moderately virulent. These data correlated with high motility and biofilm formation by the former three isolates. Conversely, in a mouse model of intramuscular infection, NF2 was much more virulent than NF1. Isolates NF2, SSU, and Riv2 disseminated in high numbers from the muscular tissue to the visceral organs of mice, while NF1 reached the liver and spleen in relatively lower numbers on the basis of colony counting and tracking of bioluminescent strains in real time by in vivo imaging. Histopathologically, degeneration of myofibers with significant infiltration of polymorphonuclear cells due to the highly virulent strains was noted. Functional genomic analysis provided data that allowed us to correlate the highly infectious nature of Aeromonas pathotypes belonging to several different species with virulence signatures and their potential ability to cause NF.",
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AU - Sha, Jian

AU - Kirtley, Michelle L.

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AU - Joseph, Sandeep J.

AU - Read, Timothy D.

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AU - Joseph, Sam W.

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AU - Horneman, Amy J.

AU - Chopra, Ashok

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