Supplemental effects of Haematococcus pluvialis in a low-fish meal diet for Litopenaeus vannamei at varying temperatures: growth performance, innate immunity and gut bacterial community
. 2024 Dec 10:15:1501753.
doi: 10.3389/fimmu.2024.1501753.
eCollection 2024.
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Front Immunol.
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Abstract
This study examined the effects of Haematococcus pluvialis on the growth performance, innate immunity, and gut microbiota of Litopenaeus vannamei under different water temperature conditions. Feeding regimens included a 20% fishmeal diet (control), a low-fish meal (LFM) diet with 10% fishmeal and an LFM diet supplemented with 0.03% H. pluvialis. These diets were administered to six groups of L. vannamei at normal (30°C) (NT) and low (20°C) (LT) temperatures (NT_C, NT_LFM, NT_LFM_HP, LT_C, LT_LFM, and LT_LFM_HP) over 8 weeks. The weight gain rate of L. vannamei in group NT_LFM_HP was significantly higher compared to group NT_LFM. Astaxanthin levels and body pigmentation intensity in L. vannamei were significantly increased in the NT_LFM_HP and LT_LFM_HP groups. Moreover, hepatopancreatic antioxidant capacities, such as superoxide dismutase (SOD) activity and total antioxidant capacity (T-AOC), were lower in normal-temperature groups compared to the low-temperature groups. Nevertheless, antioxidant capacity was significantly higher in both the NT_LFM_HP and LT_LFM_HP groups compared to the control group. Meanwhile, the expression levels of antioxidants were significantly higher at lower temperatures compared to higher temperatures, with the NT_LFM_HP and LT_LFM_HP groups exhibiting the highest expression levels. Additionally, the mRNA levels of genes associated with the Toll and IMD pathways indicated immunoregulatory effects in the organism. The expression levels of immune genes were significantly higher at lower temperatures, especially in the NT_LFM_HP and LT_LFM_HP groups compared to the control groups. Notably, significant differences in gut microbial composition were observed in the NT_LFM_HP group compared to other groups, with variations influenced by temperature and fishmeal content. Specifically, Vibrionaceae abundance was significantly lower in the LT_LFM_HP group compared to the control group. The results also revealed that the abundance of Actinomarinales was significantly higher in low-temperature groups, with the LT_LFM_HP group displaying the greatest increase. Overall, these findings suggest that L. vannamei may be susceptible to reduced fishmeal levels, potentially impacting growth and immune function. Furthermore, H. pluvialis supplementation may assist L. vannamei in acclimating to prolonged low-temperature conditions.
Keywords:
Haematococcus Pluvialis; Litopenaeus vannamei; growth performance; innate immunity; temperature.
Copyright © 2024 Lin, Chen, Chen, Li, Liu, Zhang, Hou, Tan and Niu.
Conflict of interest statement
Authors YML, YFL, PNZ and XYH were employed by Algae Health Science Co., Ltd. The remaining authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Figures
Figure 1
Effect of the addition of H. pluvialis at varying water temperatures on the body colour of L. vannamei. (A) Normal water temperature group of live shrimp; (B) Normal water temperature group after cooking shrimp; (C) Low water temperature group of live shrimp; (D) Low water temperature group after cooking shrimp.
Figure 2
Effect of the addition of H. pluvialis at varying water temperatures on the astaxanthin content of shrimp shells of L. vannamei. Data represent the means ± SEM (n = 4). * indicates significant differences in the same treatment group at different temperatures (** 0.001<P<0.01).
Figure 3
Effect of the addition of H. pluvialis at varying water temperatures on the hepatopancreas morphology of L. vannamei. Scale bar: 100 μm. Magnification: 20×. (A) NT_C group; (B) NT_LFM group; (C) NT_LFM_HP group; (D) LT_C group; (E) LT_LFM group; (F) LT_LFM_HP group. (A: stellate lumen, C: basement membrane, B: B cell, R: R cell, E: E cell).
Figure 4
Effect of incorporating H. pluvialis at varying water temperatures on the hepatopancreatic antioxidant enzyme activities of L. vannamei. MDA, malondialdehyde; T-AOC, total antioxidant capacity; SOD, superoxide dismutase. Data represent the means ± SEM (n = 4).* indicates significant differences in the same treatment group at different temperatures (* 0.01<P<0.05; ** 0.001<P<0.01; **** P<0.0001). # indicates significant differences in the same treatment group at different temperatures (## 0.001<P<0.01; ### P<0.001).
Figure 5
Effect of the addition of H. pluvialis at varying water temperatures on the expression of antioxidant genes in the hepatopancreas of L. vannamei. Data represent the means ± SEM (n = 4). * indicates significant differences in the same treatment group at different temperatures (* 0.01<P<0.05; ** 0.001<P<0.01; *** P<0.001). # indicates significant differences in the same treatment group at different temperatures (# 0.01<P<0.05; ## 0.001<P<0.01; ### P<0.001).
Figure 6
Effect of the addition of H. pluvialis at varying water temperatures on the expression of immune genes related to the Toll pathway of L. vannamei. Data represent the means ± SEM (n = 4). * indicates significant differences in the same treatment group at different temperatures (** 0.001<P<0.01; *** P<0.001; **** P<0.0001). # indicates significant differences in the same treatment group at different temperatures (# 0.01<P<0.05; ## 0.001<P<0.01; ### P<0.001).
Figure 7
Effect of the addition of H. pluvialis at varying water temperatures on the expression of immune genes related to the IMD pathway of L. vannamei. Data represent the means ± SEM (n = 4). * indicates significant differences in the same treatment group at different temperatures (* 0.01<P<0.05; ** 0.001<P<0.01; *** P<0.001; **** P<0.0001). # indicates significant differences in the same treatment group at different temperatures (# 0.01<P<0.05; ## 0.001<P<0.01; ### P<0.001).
Figure 8
Venn diagram of OTUs Comparison of gut microbiota of the addition of H. pluvialis at varying water temperatures in L. vannamei.
Figure 9
Alpha diversity index statistics of gut microbiota of the addition of (H) pluvialis at varying water temperatures in L. vannamei. Data represent the means ± SEM (n = 4). # indicates significant differences in the same treatment group at different temperatures (P<0.05). (A) Shannon index; (B) Simpson index; (C) Ace index; (D) Chao1 index.
Figure 10
Beta diversity analysis of gut microbiota of the addition of H. pluvialis at varying water temperatures in L. vannamei. (A) PCA on OTU level; (B) PCoA on OTU level.
Figure 11
Relative abundance of bacterial community at (A) phylum, (B) class, (C) family, and (D) genus levels of gut microbiota of the addition of H. pluvialis at varying water temperatures in L. vannamei. (E) The significant difference among different treatments at the genus level.
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MeSH terms
Grants and funding
The author(s) declare financial support was received for the research, authorship, and/or publication of this article. The research received funding from multiple sources, including the National Key Research and Development Program of China (2023YFD2401705), Project of Algae health Science Co., Ltd. (HT99982023-0347), Project of Science and Technology of Guangxi Province (AA23062047), Project of National Natural Science Foundation of China (32172982), and Project of China Agriculture Research System of MOF and MARA 48 (CARS 48). The funders had no role in the study design, data collection and analysis, decision to publish, and preparation of the manuscript.
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