Cross-talk among flesh-eating<i>Aeromonas hydrophila</i>strains in mixed infection leading to necrotizing fasciitis

Ponnusamy, Duraisamy; Kozlova, Elena; Sha, Jian; Erova, Tatiana E.; Azar, Sasha R.; Fitts, Eric C.; Kirtley, Michelle L.; Tiner, Bethany L.; Andersson, Jourdan A.; Grim, Christopher J.; Isom, Richard; Hasan, Nur A.; Colwell, Rita R.; Chopra, Ashok K.

doi:10.1073/pnas.1523817113

Cited by 115 publications

(109 citation statements)

References 23 publications

(31 reference statements)

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“…Interestingly, in some cases, strain diversity of pathogens within a mixed infection may augment the corresponding disease. This outcome was demonstrated in a necrotizing fasciitis model with two Aeromonas hydrophila strain types that occupied distinct niches within the host, with one strain exhibiting increased virulence due to the secretion of exotoxin A by the other strain (43).…”

Section: Discussionmentioning

confidence: 92%

Intraspecific Competition Impacts Vibrio fischeri Strain Diversity during Initial Colonization of the Squid Light Organ

Sun

LaSota

Cecere

et al. 2016

Appl Environ Microbiol

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Animal development and physiology depend on beneficial interactions with microbial symbionts. In many cases, the microbial symbionts are horizontally transmitted among hosts, thereby making the acquisition of these microbes from the environment an important event within the life history of each host. The light organ symbiosis established between the Hawaiian squid Euprymna scolopes and the bioluminescent bacterium Vibrio fischeri is a model system for examining how hosts acquire horizontally transmitted microbial symbionts. Recent studies have revealed that the light organ of wild-caught E. scolopes squid contains polyclonal populations of V. fischeri bacteria; however, the function and development of such strain diversity in the symbiosis are unknown. Here, we report our phenotypic and phylogenetic characterizations of FQ-A001, which is a V. fischeri strain isolated directly from the light organ of an E. scolopes individual. Relative to the type strain ES114, FQ-A001 exhibits similar growth in rich medium but displays increased bioluminescence and decreased motility in soft agar. FQ-A001 outcompetes ES114 in colonizing the crypt spaces of the light organs. Remarkably, we find that animals cocolonized with FQ-A001 and ES114 harbor singly colonized crypts, in contrast to the cocolonized crypts observed from competition experiments involving single genotypes. The results with our two-strain system suggest that strain diversity within the squid light organ is a consequence of diversity in the single-strain colonization of individual crypt spaces. IMPORTANCEThe developmental programs and overall physiologies of most animals depend on diverse microbial symbionts that are acquired from the environment. However, the basic principles underlying how microbes colonize their hosts remain poorly understood. Here, we report our findings of bacterial strain competition within the coevolved animal-microbe symbiosis composed of the Hawaiian squid and bioluminescent bacterium Vibrio fischeri. Using fluorescent proteins to differentially label two distinct V. fischeri strains, we find that the strains are unable to coexist in the same niche within the host. Our results suggest that strain competition for distinct colonization sites dictates the strain diversity associated with the host. Our study provides a platform for studying how strain diversity develops within a host. Microbes directly contribute to the physiology, development, and evolution of metazoans (1). Many metazoan-microbe symbioses are established through horizontal transmission, i.e., animals acquire microbial symbionts from their environment (2). Coevolution of host-microbe pairs can result in genetic factors that promote remarkably high specificity between the partners, thereby assisting in the acquisition of symbionts from typically unpredictable environments (3). An important but understudied topic in coevolved metazoan-microbe symbioses is how strain diversity impacts the establishment of these associations.A particularly powerful model system to explo...

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Section: Discussionmentioning

confidence: 92%

Intraspecific Competition Impacts Vibrio fischeri Strain Diversity during Initial Colonization of the Squid Light Organ

Sun

LaSota

Cecere

et al. 2016

Appl Environ Microbiol

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“…Indeed, an antagonistic effect through direct and host-mediated elimination was shown. In parallel, authors have observed a synergistic effect on the dissemination via local tissue barrier damage (Ponnusamy et al, 2016). …”

Section: Fields Impacted By the Multi-cellular Behavior Of Aeromonasmentioning

confidence: 96%

“…The exact mechanism of pathogenicity and aeromonads interactions during mixed infections remains unsolved, but intercellular communication likely plays a critical role in cooperation and/or competition behaviors. Ponnusamy et al (2016) have also reported complex cross-talk in which two different clones of A. hydrophila affect each other, leading to a changing course of infection in a murine model. Indeed, an antagonistic effect through direct and host-mediated elimination was shown.…”

Section: Fields Impacted By the Multi-cellular Behavior Of Aeromonasmentioning

confidence: 99%

The Social Life of Aeromonas through Biofilm and Quorum Sensing Systems

2017

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Bacteria of the genus Aeromonas display multicellular behaviors herein referred to as “social life”. Since the 1990s, interest has grown in cell-to-cell communication through quorum sensing signals and biofilm formation. As they are interconnected, these two self-organizing systems deserve to be considered together for a fresh perspective on the natural history and lifestyles of aeromonads. In this review, we focus on the multicellular behaviors of Aeromonas, i.e., its social life. First, we review and discuss the available knowledge at the molecular and cellular levels for biofilm and quorum sensing. We then discuss the complex, subtle, and nested interconnections between the two systems. Finally, we focus on the aeromonad multicellular coordinated behaviors involved in heterotrophy and virulence that represent technological opportunities and applied research challenges.

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“…It is the most common opportunistic pathogen found in poikilotherms such as fish, and is also an important human pathogen [3,4]. Different strains of A .…”

Section: Introductionmentioning

confidence: 99%

Identifying genetic diversity of O antigens in Aeromonas hydrophila for molecular serotype detection

Cao

Wang

et al. 2018

PLoS ONE

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Aeromonas hydrophila is a globally occurring, potentially virulent, gram-negative opportunistic pathogen that is known to cause water and food-borne diseases around the world. In this study, we use whole genome sequencing and in silico analyses to identify 14 putative O antigen gene clusters (OGCs) located downstream of the housekeeping genes acrB and/or oprM. We have also identified 7 novel OGCs by analyzing 15 publicly available genomes of different A. hydrophila strains. From the 14 OGCs identified initially, we have deduced that O antigen processing genes involved in the wzx/wzy pathway and the ABC transporter (wzm/wzt) pathway exhibit high molecular diversity among different A. hydrophila strains. Using these genes, we have developed a multiplexed Luminex-based array system that can identify up to 14 A. hydrophila strains. By combining our other results and including the sequences of processing genes from 13 other OGCs (7 OGCs identified from publicly available genome sequences and 6 OGCs that were previously published), we also have the data to create an array system that can identify 25 different A. hydrophila serotypes. Although clinical detection, epidemiological surveillance, and tracing of pathogenic bacteria are typically done using serotyping methods that rely on identifying bacterial surface O antigens through agglutination reactions with antisera, molecular methods such as the one we have developed may be quicker and more cost effective. Our assay shows high specificity, reproducibility, and sensitivity, being able to classify A. hydrophila strains using just 0.1 ng of genomic DNA. In conclusion, our findings indicate that a molecular serotyping system for A. hydrophila could be developed based on specific genes, providing an important molecular tool for the identification of A. hydrophila serotypes.

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Cross-talk among flesh-eatingAeromonas hydrophilastrains in mixed infection leading to necrotizing fasciitis

Cited by 115 publications

References 23 publications

Intraspecific Competition Impacts Vibrio fischeri Strain Diversity during Initial Colonization of the Squid Light Organ

Intraspecific Competition Impacts Vibrio fischeri Strain Diversity during Initial Colonization of the Squid Light Organ

The Social Life of Aeromonas through Biofilm and Quorum Sensing Systems

Identifying genetic diversity of O antigens in Aeromonas hydrophila for molecular serotype detection

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