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Establishment of a striped catfish skin explant model for studying the skin response in Aeromonas hydrophila infections.

ABSTRACT: Teleost fish skin serves as the first line of defense against pathogens. The interaction between pathogen and host skin determines the infection outcome. However, the mechanism(s) that modulate infection remain largely unknown. A proper tissue culture model that is easier to handle but can quantitatively and qualitatively monitor infection progress may shed some lights. Here, we use striped catfish (Pangasius hypophthalmus) to establish an ex vivo skin explant tissue culture model to explore host pathogen interactions. The skin explant model resembles in vivo skin in tissue morphology, integrity, and immune functionality. Inoculation of aquatic pathogen Aeromonas hydrophila in this model induces epidermal exfoliation along with epithelial cell dissociation and inflammation. We conclude that this ex vivo skin explant model could serve as a teleost skin infection model for monitoring pathogenesis under various infection conditions. The model can also potentially be translated into a platform to study prevention and treatment of aquatic infection on the skin in aquaculture applications.

SUBMITTER: Siao RF

PROVIDER: S-EPMC8463585 | biostudies-literature | 2021 Sep

REPOSITORIES: biostudies-literature

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Establishment of a striped catfish skin explant model for studying the skin response in Aeromonas hydrophila infections.

Siao Ru-Fang RF Lin Chia-Hsuan CH Chen Li-Hsuan LH Wang Liang-Chun LC

Scientific reports 20210924 1

Teleost fish skin serves as the first line of defense against pathogens. The interaction between pathogen and host skin determines the infection outcome. However, the mechanism(s) that modulate infection remain largely unknown. A proper tissue culture model that is easier to handle but can quantitatively and qualitatively monitor infection progress may shed some lights. Here, we use striped catfish (Pangasius hypophthalmus) to establish an ex vivo skin explant tissue culture model to explore hos ...[more]

PMID: 34561532

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Project description:Bacterial pathogens are well equipped to adhere to and initiate infection in teleost fish. Fish skin mucus serves as the first barrier against environmental pathogens. The mucus harbors commensal microbes that impact host physiological and immunological responses. However, how the skin mucosal microbiota responds to the presence of pathogens remains largely unexplored. Thus, little is known about the status of skin mucus prior to infection with noticeable symptoms. In this study, we investigated the interactions between pathogens and the skin mucosal microbiota as well as the fish skin immune responses in the presence of pathogens. Striped catfish (Pangasianodon hypophthalmus) were challenged with different concentrations of the bacterial pathogen Aeromonas hydrophila (AH), and the skin immune response and the mucosal microbiota were examined by quantitative PCR (qPCR) and 16S rRNA gene sequence analysis. We determined that the pathogen concentration needed to stimulate the skin immune response was associated with significant mucosal microbiota changes, and we reconfirmed these observations using an ex vivo fish skin model. Further analysis indicated that changes in the microbiota were attributed to a significant increase in opportunistic pathogens over AH. We concluded that the presence and increase of AH result in dysbiosis of the mucosal microbiota that can stimulate skin immune responses. We believe that our work sheds light on host-pathogen-commensal microbiota interactions and therefore contributes to aquaculture fish health. IMPORTANCE The fish skin mucosal microbiota is essential in modulating the host response to the presence of pathogens. Our study provides a platform to study both the correlation and causation of the interactions among the pathogen, fish skin, and the skin mucosal microbiota. Based on these findings, we provide the first mechanistic information on how mucosal microbiota changes induced by the pathogen AH result in skin disturbance with immune stimulation in striped catfish in the natural state and a potential direction for early-infection screening. Thus, this study is highly significant in the prevention of fish disease.

Project description:IntroductionAeromonads are ubiquitous in aquatic environments and several species are opportunistic pathogens of fish. Disease losses caused by motile Aeromonas species, particularly Aeromonas hydrophila, can be challenging in intensive aquaculture, such as at striped catfish (Pangasianodon hypophthalmus) farms in Vietnam. Outbreaks require antibiotic treatments, but their application is undesirable due to risks posed by resistance. Vaccines are an attractive prophylactic and they must protect against the prevalent strains responsible for ongoing outbreaks.MethodsThis present study aimed to characterize A. hydrophila strains associated with mortalities in striped catfish culture in the Mekong Delta by a polyphasic genotyping approach, with a view to developing more effective vaccines.ResultsDuring 2013-2019, 345 presumptive Aeromonas spp. isolates were collected at farms in eight provinces. Repetitive element sequence-based PCR, multi-locus sequence typing and whole-genome sequencing revealed most of the suspected 202 A. hydrophila isolates to belong to ST656 (n = 151), which corresponds to the closely-related species Aeromonas dhakensis, with a lesser proportion belonging to ST251 (n = 51), a hypervirulent lineage (vAh) of A. hydrophila already causing concern in global aquaculture. The A. dhakensis ST656 and vAh ST251 isolates from outbreaks possessed unique gene sets compared to published A. dhakensis and vAh ST251 genomes, including antibiotic-resistance genes. The sharing of resistance determinants to sulphonamides (sul1) and trimethoprim (dfrA1) suggests similar selection pressures acting on A. dhakensis ST656 and vAh ST251 lineages. The earliest isolate (a vAh ST251 from 2013) lacked most resistance genes, suggesting relatively recent acquisition and selection, and this underscores the need to reduce antibiotics use where possible to prolong their effectiveness. A novel PCR assay was designed and validated to distinguish A. dhakensis and vAh ST251 strains.DiscussionThis present study highlights for the first time A. dhakensis, a zoonotic species that can cause fatal human infection, to be an emerging pathogen in aquaculture in Vietnam, with widespread distribution in recent outbreaks of motile Aeromonas septicaemia in striped catfish. It also confirms vAh ST251 to have been present in the Mekong Delta since at least 2013. Appropriate isolates of A. dhakensis and vAh should be included in vaccines to prevent outbreaks and reduce the threat posed by antibiotic resistance.

Dataset Information

Establishment of a striped catfish skin explant model for studying the skin response in Aeromonas hydrophila infections.

Publications

Establishment of a striped catfish skin explant model for studying the skin response in Aeromonas hydrophila infections.

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