Impacts of oral Vibrio mimicus double-targeted DNA vaccine on the gut microbiota in grass carps (Ctenopharyngodon idella) and correlations with intestinal mucosa innate immunity

Cao, Shoulin; Guo, Jia-Jing; Zhao, Weigang; Yang, Wen-Fei; Zhang, Shuliu; HuiZhu, Tao; Li, Jinnian

doi:10.1016/j.aquaculture.2020.736201

Cited by 14 publications

(13 citation statements)

References 29 publications

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“…The anti-Shigella LPS antibody response of cynomolgus macaques had positive correlations with Weissella, Catabacteriaceae, and Clostridium (Seekatz et al, 2013). The expression of immunerelated genes in the hindgut of grass carp was positively correlated with Bacteroides abundance (Cao et al, 2021). A comparison of RVV responders and non-responders among Ghanaian infants revealed that RVV responses were associated with a decreased abundance of the phylum Bacteroidetes and an increased abundance of Streptococcus bovis (Harris et al, 2017).…”

Section: Discussionmentioning

confidence: 95%

“…In broiler chickens, different Salmonella typhimurium vaccine strains had varying effects on the cecal microbiota but did not affect its relative abundance (Park et al, 2017). The gut bacterial population of grass carp was altered 21 days after vaccination with an oral Vibrio mimicus double-targeted DNA vaccine, and gut macrophage activity and hindgut immune-related gene expression were positively linked to Bacteroides (Cao et al, 2021). In grass carp, no notable alterations in the dominant genus of the intestinal tract were observed after exposure to recombinant Aeromonas hydrophila vaccine (Aera), but the relative abundance of Aeromonas changed (Liu et al, 2015).…”

Section: Introductionmentioning

confidence: 99%

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Attenuated Streptococcus agalactiae WC1535 ∆Sia perturbs the gut microbiota of Oreochromis niloticus, massively colonizes the intestine, and induces intestinal mucosal immunity after intraperitoneal inoculation

Hao

Wang²,

Yang³

et al. 2022

Front. Microbiol.

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We previously developed and assessed the effectiveness of the attenuated Streptococcus agalactiae (Group B Streptococcus, GBS) strain WC1535 ∆Sia (with neuA-D gene cluster deletion) vaccine in tilapia (Oreochromis niloticus). In this study, we characterized the bacterial communities of the tilapia intestines by 16S rRNA high-throughput sequencing and assessed the serum antibody response, expression of immune-related genes, and histological changes following formalin-killed GBS vaccine (FKV) and the live attenuated vaccine ∆Sia (LAV). Results showed that FKV and LAV induced robust systemic and intestinal mucosal immune responses in tilapia without causing obvious pathological changes in the hindgut, spleen, and head kidney but exerted different effects on intestinal bacterial communities. The richness or diversity of the intestinal bacterial community of FKV tilapia showed no significant changes compared with that of the control fish (p > 0.05) at either day 21 post-initial vaccination (21 dpiv) or day 35 (day 14 after the second immunization) (35 dpiv). The community composition of FKV tilapia and controls was significantly similar, although the relative abundance of some genera was significantly altered. Relative to control fish, the gut ecosystem of LAV tilapia was significantly disturbed with a substantial increase in community diversity at 21 dpiv (p < 0.05) and a significant decrease at 35 dpiv in fish with high serum antibody response (ΔSia35H) (p < 0.05). However, there was no significant difference between ΔSia35H and ΔSia35L (low serum antibody response) fish (p > 0.05). Moreover, the community composition of LAV tilapia at 21 dpiv or 35 dpiv was considerably different from that of the controls. Particularly, GBS ∆Sia was found to be abundant in the intestine at 21 and 35 dpiv. This result suggested that the parenteral administration of the LAV (∆Sia) may also have the effect of oral vaccination in addition to the immune effect of injection vaccination. In addition, a significant correlation was found between the expression of immune-related genes and certain bacterial species in the intestinal mucosal flora. Our findings will contribute to a better understanding of the effects of inactivated and attenuated vaccines on gut microbiota and their relationship with the immune response.

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Section: Discussionmentioning

confidence: 95%

Section: Introductionmentioning

confidence: 99%

Attenuated Streptococcus agalactiae WC1535 ∆Sia perturbs the gut microbiota of Oreochromis niloticus, massively colonizes the intestine, and induces intestinal mucosal immunity after intraperitoneal inoculation

Hao

Wang²,

Yang³

et al. 2022

Front. Microbiol.

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show abstract

“…Intestinal microorganisms form a symbiotic ecosystem, which helps maintain the steady balance in intestine and is essential to the health of humans and animals ( 14 , 55 ). It is reported that intestinal inflammation will lead to changes in intestinal microorganisms, thus affecting the normal function of organisms ( 56 ).…”

Section: Discussionmentioning

confidence: 99%

“…In the principal coordinate analysis, we found that the distance between the CMCS-20H group and the other three groups (gcIFN-20H, CMCS, and PBS) was significantly different. The different distance between groups is caused by the difference of bacteria in each genus in the group ( 50 , 55 ), in which different genera have been listed ( Aeromonas , Rhodobacter , and Cetabacterium ). We conclude that the intestinal inflammation in grass carp after oral administration of CMCS-20H is mild and the intestinal microbial richness is relatively stable, which is conducive to the normal function in grass carp.…”

Section: Discussionmentioning

confidence: 99%

Oral Administration of Nanopeptide CMCS-20H Conspicuously Boosts Immunity and Precautionary Effect Against Bacterial Infection in Fish

et al. 2022

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Massive mortalities caused by bacterial infections in intensive aquaculture result in serious economic losses. In this study, a novel antimicrobial peptide gcIFN-20H was efficiently expressed in Pichia pastoris (GS115) and loaded on carboxylmethyl chitosan (CMCS) to prepare CMCS-20H nanoparticles. Through physical characterization assays (TEM, DLS, BCA, and Raman) and biological activity tests (antimicrobial activity and cytotoxicity), CMCS-20H nanopeptide was verified to be spherical nanoparticles with sustained release, antimicrobial activity, and negligible toxicity. CMCS-20H nanoparticles are more resistant to intestinal degradation than unloaded gcIFN-20H by indirect immunofluorescence assay. Oral administration was then carried out for 42 days. Complement C3 content, lysozyme, and total superoxide dismutase activities are highest in CMCS-20H group by serum biochemistry index assays. After challenge with Aeromonas hydrophila, the survival rate in CMCS-20H group is highest (46%), which is 64% higher than the control group (28%). Meanwhile, the tissue bacterial loads (intestine, spleen, head kidney, trunk kidney, hepatopancreas, muscle, and blood) in the CMCS-20H group are significantly lower than other groups. By PAS staining analysis, the number of intestinal villi goblet cells and the thickness of mucin in the CMCS-20H group obviously increased. CMCS-20H effectively enhances mRNA expressions of some important immune genes (IL-1β, IL-6, TNF-α, IL-2, IFN-γ2, and IgM). The minimal tissue lesions (Intestine, spleen, and trunk kidney) were seen in the CMCS-20H group by histopathological examination. 16S rRNA sequencing showed that oral CMCS-20H maintains the intestinal microbiome homeostasis in bacterial infection. The results indicate that the novel nanopeptide CMCS-20H as the immunopotentiator can remarkably boost fish immunity and precautionary effect by oral administration and address the theoretical mechanisms and insights into the promising application prospect in aquaculture.

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“…Therefore, probiotics can improve vaccine effectiveness by regulating the intestinal microbiota [ 31 , 32 ]. In recent years, several studies have focused on the correlation between fish intestinal microbiota and vaccine efficacy [ 33 – 35 ]. As reported previously, a new recombinant A .…”

Section: Introductionmentioning

confidence: 99%

Significant alterations of intestinal symbiotic microbiota induced by intraperitoneal vaccination mediate changes in intestinal metabolism of NEW Genetically Improved Farmed Tilapia (NEW GIFT, Oreochromis niloticus)

Zhang

Yang

et al. 2022

Microbiome

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Background After millions of years of coevolution, symbiotic microbiota has become an integral part of the host and plays an important role in host immunity, metabolism, and health. Vaccination, as an effective means of preventing infectious diseases, has been playing a vital role in the prevention and control of human and animal diseases for decades. However, so far, minimal is known about the effect of vaccination on fish symbiotic microbiota, especially mucosal microbiota, and its correlation with intestinal metabolism remains unclear. Methods Here we reported the effect of an inactivated bivalent Aeromonas hydrophila/Aeromonas veronii vaccine on the symbiotic microbiota and its correlation with the intestinal metabolism of farmed adult Nile tilapia (Oreochromis niloticus) by 16S rRNA gene high-throughput sequencing and gas chromatography-mass spectrometry metabolomics. Results Results showed that vaccination significantly changed the structure, composition, and predictive function of intestinal mucosal microbiota but did not significantly affect the symbiotic microbiota of other sites including gill mucosae, stomach contents, and stomach mucosae. Moreover, vaccination significantly reduced the relative abundance values of potential opportunistic pathogens such as Aeromonas, Escherichia–Shigella, and Acinetobacter in intestinal mucosae. Combined with the enhancement of immune function after vaccination, inactivated bivalent Aeromonas vaccination had a protective effect against the intestinal pathogen infection of tilapia. In addition, the metabolite differential analysis showed that vaccination significantly increased the concentrations of carbohydrate-related metabolites such as lactic acid, succinic acid, and gluconic acid but significantly decreased the concentrations of multiple lipid-related metabolites in tilapia intestines. Vaccination affected the intestinal metabolism of tilapia, which was further verified by the predictive function of intestinal microbiota. Furthermore, the correlation analyses showed that most of the intestinal differential microorganisms were significantly correlated with intestinal differential metabolites after vaccination, confirming that the effect of vaccination on intestinal metabolism was closely related to the intestinal microbiota. Conclusions In conclusion, this paper revealed the microbial and metabolic responses induced by inactivated vaccination, suggesting that intestinal microbiota might mediate the effect of vaccination on the intestinal metabolism of tilapia. It expanded the novel understanding of vaccine protective mechanisms from microbial and metabolic perspectives, providing important implications for the potential influence of vaccination on human intestinal microbiota and metabolism.

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Impacts of oral Vibrio mimicus double-targeted DNA vaccine on the gut microbiota in grass carps (Ctenopharyngodon idella) and correlations with intestinal mucosa innate immunity

Cited by 14 publications

References 29 publications

Attenuated Streptococcus agalactiae WC1535 ∆Sia perturbs the gut microbiota of Oreochromis niloticus, massively colonizes the intestine, and induces intestinal mucosal immunity after intraperitoneal inoculation

Attenuated Streptococcus agalactiae WC1535 ∆Sia perturbs the gut microbiota of Oreochromis niloticus, massively colonizes the intestine, and induces intestinal mucosal immunity after intraperitoneal inoculation

Oral Administration of Nanopeptide CMCS-20H Conspicuously Boosts Immunity and Precautionary Effect Against Bacterial Infection in Fish

Significant alterations of intestinal symbiotic microbiota induced by intraperitoneal vaccination mediate changes in intestinal metabolism of NEW Genetically Improved Farmed Tilapia (NEW GIFT, Oreochromis niloticus)

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