Cited by 222Aquaculture disease management and microbiotaGut microbiota and healthInvertebrate Immune Response Mechanisms

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Bacterial dynamics in intestines of the black tiger shrimp and the Pacific white shrimp during Vibrio harveyi exposure

Rungrassamee, Wanilada, Klanchui, Amornpan, Maibunkaew, Sawarot, Karoonuthaisiri, Nitsara·2016·Journal of Invertebrate Pathology

DOI 10.1016/j.jip.2015.11.004

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Abstract

The intestinal microbiota play important roles in health of their host, contributing to maintaining the balance and resilience against pathogen. To investigate effects of pathogen to intestinal microbiota, the bacterial dynamics upon a shrimp pathogen, Vibrio harveyi, exposures were determined in two economically important shrimp species; the black tiger shrimp (BT) and the Pacific white shrimp (PW). Both shrimp species were reared under the same diet and environmental conditions. Shrimp survival rates after the V. harveyi exposure revealed that the PW shrimp had a higher resistance to the pathogen than the BT shrimp. The intestinal bacterial profiles were determined by denaturing gradient gel electrophoresis (DGGE) and barcoded pyrosequencing of the 16S rRNA sequences under no pathogen challenge control and under pathogenic V. harveyi challenge. The DGGE profiles showed that the presence of V. harveyi altered the intestinal bacterial patterns in comparison to the control in BT and PW intestines. This implies that bacterial balance in shrimp intestines was disrupted in the presence of V. harveyi. The barcoded pyrosequencing analysis showed the similar bacterial community structures in intestines of BT and PW shrimp under a normal condition. However, during the time course exposure to V. harveyi, the relative abundance of bacteria belong to Vibrio genus was higher in the BT intestines at 12h after the exposure, whereas relative abundance of vibrios was more stable in PW intestines. The principle coordinates analysis based on weighted-UniFrac analysis showed that intestinal bacterial population in the BT shrimp lost their ability to restore their bacterial balance during the 72-h period of exposure to the pathogen, while the PW shrimp were able to reestablish their bacterial population to resemble those seen in the unexposed control group. This observation of bacterial disruption might correlate to different mortality rates observed between the two shrimp species. Our findings provide evidence of intestinal bacterial population altered by a presence of the pathogen in shrimp intestines and intestinal bacterial stability might provide colonization resistance against the invading pathogen in the host shrimp. Hence, intestinal microbial ecology management may potentially contribute to disease prevention in aquaculture.

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Result
The Effect of Disease and Season to Hepatopancreas and Intestinal Mycobiota of Litopenaeus vannamei
Li, J., Jiang, H., Li, L., Zhang, X., & Chen, J. (2019) · Frontiers in Microbiology · doi:10.3389/fmicb.2019.00889 · Cited by 42
Taxonomic and functional changes in the microbiota of the white shrimp (Litopenaeus vannamei) associated with postlarval ontogenetic development
Garibay-Valdéz, E., Martínez‐Porchas, M., Calderón, K., Vargas‐Albores, F., Gollas‐Galván, T., & Martínez‐Córdova, L. R. (2019) · Aquaculture · doi:10.1016/j.aquaculture.2019.734842 · Cited by 42
Microbes and pathogens associated with shrimps - implications and review of possible control strategies
Bhassu, S., Shama, M., Tiruvayipati, S., Soo, T. C. C., Ahmed, N., & Yusoff, K. (2024) · Frontiers in Marine Science · doi:10.3389/fmars.2024.1397708 · Cited by 38
“On the other hand, recovery of the gut bacterial composition has shown to increase survival rate in shrimps (Rungrassamee et al., 2016).”
Background
The intestinal bacterial community of healthy and diseased animals and its association with the aquaculture environment
Sun, F., Wang, C., Chen, L., Weng, G., & Zheng, Z. (2019) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-019-10236-z · Cited by 38
The Effect of Dietary Saccharomyces cerevisiae on Growth Performance, Oxidative Status, and Immune Response of Sea Bream (Sparus aurata)
El-Bab, A. F. F., Saghir, S. A. M., El-Naser, I. A. A., El-Kheir, S. M. M. A., El‐Kader, M. F. A., Alruhaimi, R. S., Alqhtani, H. A., Mahmoud, A. M., Naiel, M. A. E., & El‐Raghi, A. A. (2022) · Life · doi:10.3390/life12071013 · Cited by 37
“Vibrio species in aquaculture under intensive culture causes serious economic loss by increasing mortality [88].”
Background
Significant differences in intestinal microbial communities in aquatic animals from an aquaculture area
Sun, F., & Xu, Z. (2021) · Journal of Marine Science and Engineering · doi:10.3390/jmse9020104 · Cited by 35
“Several members of the Vibrio genus are considered primary disease pathogens, causing death in aquaculture animals, and seriously endangering aquaculture systems [29,30].”
Background
Gut microbiota of Pacific white shrimp ( Litopenaeus vannamei ) exhibits distinct responses to pathogenic and non-pathogenic Vibrio parahaemolyticus
Chang, Y.-T., Ko, H.-T., Wu, P.-L., Kumar, R., Wang, H., & Lu, H. (2023) · Microbiology Spectrum · doi:10.1128/spectrum.01180-23 · Cited by 38
“In the aquaculture system, gut microbiota dysbiosis (the altered composition of bacterial communities) could significantly disrupt the stability of normal gut functions, leading to disease aggravation (14).”
Background
The role of gut microbial community and metabolomic shifts in adaptive resistance of Atlantic killifish (Fundulus heteroclitus) to polycyclic aromatic hydrocarbons
Redfern, L. K., Jayasundara, N., Singleton, D. R., Giulio, R. T. D., Carlson, J., Sumner, S., & Gunsch, C. K. (2021) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2021.145955 · Cited by 35
Metagenomic comparison of structure and function of microbial community between water, effluent and shrimp intestine of higher place Litopenaeus vannamei ponds
He, Z., Pan, L., Zhang, M., Zhang, M., Huang, F., & Gao, S. (2020) · Journal of Applied Microbiology · doi:10.1111/jam.14610 · Cited by 34
“In aquaculture ecosystems, animals are directly exposed to high loads of ambient microbes, which leads to a close correlation between the microbiota of shrimp intestine and surroundings (Rungrassamee et al. 2016; Xiong et al. 2017).”
Background
White spot syndrome virus (WSSV) disturbs the intestinal microbiota of shrimp (Penaeus vannamei) reared in biofloc and clear seawater
Valente, C. D. S., Rodiles, A., Marques, M. R. F., & Merrifield, D. L. (2020) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-020-10816-4 · Cited by 34
Investigating host-gut microbial relationship in Penaeus monodon upon exposure to Vibrio harveyi
Angthong, P., Uengwetwanit, T., Uawisetwathana, U., Koehorst, J. J., Arayamethakorn, S., Schaap, P. J., dos Santos, V. A. P. M., Phromson, M., Karoonuthaisiri, N., Chaiyapechara, S., et al. (2023) · Aquaculture · doi:10.1016/j.aquaculture.2023.739252 · Cited by 33
Effects of the Dietary Probiotic Clostridium butyricum on Intestine Digestive and Metabolic Capacities, SCFA Content and Body Composition in Marsupenaeus japonicus
Duan, Y., Dong, H., Wang, Y., Zhang, Y., & Zhang, J. (2018) · Journal of Ocean University of China · doi:10.1007/s11802-018-3464-3 · Cited by 33
“So intestine structural integrity plays a pivotal role in maintaining intestine health in aquatic animals (Rungrassamee et al., 2016; Luis-Villaseñor et al., 2013).”
Background
Changes in the intestinal microbiota of Pacific white shrimp (Litopenaeus vannamei) with different severities of Enterocytozoon hepatopenaei infection
Shen, H., Dou, Y., Li, H., Qiao, Y., Jiang, G., Wan, X., Cheng, J., Fan, X., Li, H., Wang, L., et al. (2022) · Journal of Invertebrate Pathology · doi:10.1016/j.jip.2022.107763 · Cited by 33
Shrimp microbiome and immune development in the early life stages
Angthong, P., Chaiyapechara, S., & Rungrassamee, W. (2023) · Developmental & Comparative Immunology · doi:10.1016/j.dci.2023.104765 · Cited by 33
A gelatinized lipopeptide diet effectively modulates immune response, disease resistance and gut microbiome in Penaeus vannamei challenged with Vibrio parahaemolyticus
Prathiviraj, R., Rajeev, R., Fernandes, H., Rathna, K., Lipton, A. N., Selvin, J., & Kiran, G. S. (2021) · Fish & Shellfish Immunology · doi:10.1016/j.fsi.2021.02.018 · Cited by 31
Epimicrobiome Shifts With Bleaching Disease Progression in the Brown Seaweed Saccharina japonica
Fan, L., Egan, S., Zhuang, Y., Chang, L., Xiao, L., Qin, Y., & Wang, G. (2022) · Frontiers in Marine Science · doi:10.3389/fmars.2022.865224 · Cited by 30
Shrimp Intestinal Microbiota Homeostasis: Dynamic Interplay Between the Microbiota and Host Immunity
Zhou, K., Liu, P., Yao, J., Vasta, G. R., Wang, J., & Wang, X. (2024) · Reviews in Aquaculture · doi:10.1111/raq.12986 · Cited by 30
Effects of high temperature on water quality, growth performance, enzyme activity and the gut bacterial community of shrimp (Litopenaeus vannamei)
Al‐Masqari, Z. A., Guo, H., Wang, R., Yan, H., Dong, P., Wang, G., & Zhang, D. (2022) · Aquaculture Research · doi:10.1111/are.15836 · Cited by 30
High-throughput sequencing analysis of the microbial community in coastal intensive mariculture systems
Wang, J., Lu, J. J., Zhang, Y., Wu, J., Zhang, C., Yu, X., Zhang, Z., Liu, H., & Wang, W. (2018) · Aquacultural Engineering · doi:10.1016/j.aquaeng.2018.10.001 · Cited by 30
Elevated temperature disrupts the mucosal structure and induces an immune response in the intestine of whiteleg shrimp Litopenaeus vannamei (Boone, 1931) (Decapoda: Dendrobranchiata: Penaeidae)
Duan, Y., Wang, Y., Zhang, J., & Xiong, D. (2018) · Journal of Crustacean Biology · doi:10.1093/jcbiol/ruy055 · Cited by 29
Effects of taurine supplementation in low fishmeal diet on growth, immunity and intestinal health of Litopenaeus vannamei
Shi, M., Yao, X., Qu, K., Liu, Y., Tan, B., & Xie, S. (2023) · Aquaculture Reports · doi:10.1016/j.aqrep.2023.101713 · Cited by 28
Studies on exploring the potentials of gut microbiomes to mitigate the bacterial and viral diseases of fish and shellfish in aquaculture farming
Diwan, A. D., Harke, S. N., & Panche, A. N. (2023) · The Microbe · doi:10.1016/j.microb.2023.100031 · Cited by 28
Understanding the effects of salinity and Vibrio harveyi on the gut microbiota profiles of Litopenaeus vannamei
Deris, Z. M., Iehata, S., Gan, H. M., Ikhwanuddin, M., Musa, N., Asaduzzaman, M., Wang, M., Liang, Y., Danish‐Daniel, M., Sung, Y. Y., et al. (2022) · Frontiers in Marine Science · doi:10.3389/fmars.2022.974217 · Cited by 30
“An environmentally abundant pathogen may reach a distressed shrimp gut through the oral route, resulting in indirect alteration of shrimp gut microbiota (Rungrassamee et al., 2016; Dong et al., 2021; Prathiviraj et al., 2021).”
BackgroundResult
BALOs Improved Gut Microbiota Health in Postlarval Shrimp (Litopenaeus vannamei) After Being Subjected to Salinity Reduction Treatment
Cao, Q., Najnine, F., Han, H., Wu, B., & Cai, J. (2020) · Frontiers in Microbiology · doi:10.3389/fmicb.2020.01296 · Cited by 27
Vibrio harveyi co-infected with Cryptocaryon irritans to orange-spotted groupers Epinephelus coioides
Lai, X., Wu, H., Guo, W., Li, X., Wang, J.-L., Duan, Y., Zhang, P., Huang, Z., Li, Y., Dong, G., et al. (2023) · Fish & Shellfish Immunology · doi:10.1016/j.fsi.2023.108879 · Cited by 27
Effects of Dietary Lipid Sources on Alleviating the Negative Impacts Induced by the Fishmeal Replacement With Clostridium autoethanogenum Protein in the Diet of Pacific White Shrimp (Litopenaeus vannamei)
Zheng, C., Gong, S., Cao, J., Dong, X., Chi, S., Yang, Q., Liu, H., Zhang, S., Xie, S., & Tan, B. (2022) · Frontiers in Marine Science · doi:10.3389/fmars.2022.879364 · Cited by 26
“If the structural integrity of the intestine is compromised, pathogens, and toxins can penetrate the intestinal epithelium and disrupt host immunity (Rungrassamee et al., 2016).”
Background
16S rRNA gene sequencing analysis reveals an imbalance in the intestinal flora of Eriocheir sinensis with hepatopancreatic necrosis disease
Zhan, M., Xi, C., Gong, J., Zhu, M., Shui, Y., Xu, Z., Xu, G., & Shen, H. (2022) · Comparative Biochemistry and Physiology Part D Genomics and Proteomics · doi:10.1016/j.cbd.2022.100988 · Cited by 24
Potential lineage transmission within the active microbiota of the eggs and the nauplii of the shrimp Litopenaeus stylirostris : possible influence of the rearing water and more
Giraud, C., Callac, N., Beauvais, M., Mailliez, J.-R., Ansquer, D., Selmaoui-Folcher, N., Pham, D., Wabete, N., & Boulo, V. (2021) · PeerJ · doi:10.7717/peerj.12241 · Cited by 23
The implication of metabolically active Vibrio spp. in the digestive tract of Litopenaeus vannamei for its post-larval development
Garibay-Valdéz, E., Martínez‐Córdova, L. R., López‐Torres, M. A., Almendáriz-Tapia, F. J., Martínez‐Porchas, M., & Calderón, K. (2020) · Scientific Reports · doi:10.1038/s41598-020-68222-9 · Cited by 23
Characterization of a novel shrimp pathogen, Vibrio brasiliensis , isolated from Pacific white shrimp, Penaeus vannamei
Li, G., Xie, G., Wang, H., Wan, X., Li, X., Shi, C., Wang, Z., Gong, M., Li, T., Wang, P., et al. (2021) · Journal of Fish Diseases · doi:10.1111/jfd.13475 · Cited by 23
Bacterial diversity and community composition in the gut and rearing water of Pacific White shrimp Penaeus vannamei during an outbreak of white feces disease
Kurniawinata, M. I., Sukenda, S., Wahjuningrum, D., & Widanarni, W. (2022) · Aquaculture · doi:10.1016/j.aquaculture.2022.738431 · Cited by 23
Shrimp AHPND Causing Vibrio anguillarum Infection: Quantitative Diagnosis and Identifying Antagonistic Bacteria
Shen, H., Song, T.-T., Lü, J., Qiu, Q., Chen, J., & Xiong, J. (2021) · Marine Biotechnology · doi:10.1007/s10126-021-10079-8 · Cited by 22
“harveyi exposure, compared with the restoration of gut microbiota in black tiger shrimp (Rungrassamee et al. 2016).”
Background
Host-microbiota interactions and responses of Metapenaeus ensis infected with decapod iridescent virus 1
Liao, M., Liao, X., Long, X., Zhao, J., He, Z., Zhang, J., Wu, T., & Sun, C. (2023) · Frontiers in Microbiology · doi:10.3389/fmicb.2022.1097931 · Cited by 22
The immune response of the C-Jun in the black tiger shrimp ( Penaeus monodon ) after bacterial infection
Shi, G., Zhao, C., Fu, M., & Qiu, L. (2016) · Fish & Shellfish Immunology · doi:10.1016/j.fsi.2016.12.025 · Cited by 22
Effects of various levels of dietary copper supplementation with copper sulfate and copper hydroxychloride on Pacific white shrimp Litopenaeus vannamei performance and microbial communities
Zhou, Y., Zhang, D., Peatman, E., Rhodes, M. A., Liu, J., & Davis, D. A. (2017) · Aquaculture · doi:10.1016/j.aquaculture.2017.04.016 · Cited by 22
Profile of the gut microbiota of Pacific white shrimp under industrial indoor farming system
Li, M., Ghonimy, A., Chen, D.-Q., Li, J., He, Y., Greco, L. S. L., Dyzenchauz, F. J., & Chang, Z. (2024) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-024-13046-0 · Cited by 21
Effects of Replacing Fish Meal with Distillers’ Dried Grains with Solubles on the Growth Performance and Gut Microbiota in Juvenile Pacific Whiteleg Shrimp Litopenaeus vannamei
Gyan, R. W., Qihui, Y., Tan, B., Dong, X., Chi, S., Liu, H., & Zhang, S. (2021) · North American Journal of Aquaculture · doi:10.1002/naaq.10236 · Cited by 20
Gut bacterial profile associated with healthy and diseased (AHPND) shrimp Penaeus vannamei
Alvarez-Ruiz, S. A. P., Luna‐González, A., Escamilla‐Montes, R., Fierro-Coronado, A., Plata, G. D., García-Gutiérrez, C., & Peraza-Gómez, V. (2022) · Latin American Journal of Aquatic Research · doi:10.3856/vol50-issue2-fulltext-2839 · Cited by 20
“At the class level, Gammaproteobacteria are habitual in the gut of P. vannamei (Rungrassamee et al. 2016, Zheng et al. 2017).”
Background
White spot syndrome virus impact on the expression of immune genes and gut microbiome of black tiger shrimp Penaeus monodon
Jatuyosporn, T., Laohawutthichai, P., Ochoa‐Romo, J. P., Gallardo-Becerra, L., Sánchez, F., Tassanakajon, A., Ochoa‐Leyva, A., & Krusong, K. (2023) · Scientific Reports · doi:10.1038/s41598-023-27906-8 · Cited by 20

Authors: Rungrassamee, W., Klanchui, A., Maibunkaew, S., & Karoonuthaisiri, N.
Affiliations: National Center for Genetic Engineering and Biotechnology (TH)
Corresponding author: Rungrassamee, Wanilada
ORCID: Rungrassamee, Wanilada
Karoonuthaisiri, Nitsara
Venue: Journal of Invertebrate Pathology
Publisher: Elsevier BV
Published: 2016-01
Volume: 133
Pages: 12-19
ISSN: 0022-2011 (ISSN-L)
DOI: 10.1016/j.jip.2015.11.004
OpenAlex: W2172537579
Cited by: 222
References: 31
Citations by year: 2026: 10 · 2025: 17 · 2024: 27 · 2023: 33 · 2022: 27 · 2021: 23 · 2020: 26 · 2019: 14 · 2018: 29 · 2017: 9 · 2016: 6
FWCI: 7.21
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
doi.org/10.15223/policy-017 (stm-asf)
doi.org/10.15223/policy-037 (stm-asf)
doi.org/10.15223/policy-012 (stm-asf)
doi.org/10.15223/policy-029 (stm-asf)
doi.org/10.15223/policy-004 (stm-asf)
Locations: Journal of Invertebrate Pathology (publishedVersion)
PubMed (publishedVersion)
Funders: Thailand Research Fund (TRG5480014)
National Center for Genetic Engineering and Biotechnology (P-13-50417)
Topics: Life Sciences › Immunology and Microbiology › Immunology › Aquaculture disease management and microbiota
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
Life Sciences › Immunology and Microbiology › Immunology › Invertebrate Immune Response Mechanisms
Keywords: Vibrio harveyi, Penaeus monodon, Litopenaeus vannamei, gut microbiota, bacterial community dynamics, shrimp disease resistance, colonization resistance, shrimp mortality, aquaculture disease prevention, microbial ecology
MeSH terms: Gastrointestinal Microbiome, Animals, Vibrio, Penaeidae, Biodiversity, Disease Resistance

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Bacterial dynamics in intestines of the black tiger shrimp and the Pacific white shrimp during Vibrio harveyi exposure

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