Effects of normoxic and hypoxic conditions on the immune response and gut microbiota of Bostrichthys sinensis

doi:10.1016/j.aquaculture.2020.735336

Aquaculture

Volume 525, 30 August 2020, 735336

https://doi.org/10.1016/j.aquaculture.2020.735336 Get rights and content

Highlights

•
Antioxidant response of B. sinensis were not changed in long-term low dissolved oxygen condition.
•
The diversity and richness of intestinal bacteria could be changed in B. sinensis under hypoxic condition.
•
Although Clostridia both occupied an important position in the two networks, the niche of Clostridia was notably altered.
•
Microbial functional pathways could be impacted by environmental factors to adapt living environment.

Abstract

Dissolved oxygen (DO) content is crucial for the development and health of aquatic animals. DO content is closely related to the antioxidant response of aquatic animals, while the interplay between DO content and the gut microbiota of aquatic animals is unclear. Thus, the objective of this study was to compare the changes in gut microbiota in Bostrichthys sinensis under normoxic (CT group) and hypoxic (Y group) conditions. Superoxide dismutase and catalase activities were similar in the CT and Y groups. The diversity and richness of the community decreased significantly in the Y group, concurrent with an altered composition in the gut microbiota. A dissimilarity test demonstrated that the structure of the gut microbiota was strictly separate between the CT and Y groups. The relative abundance of Gammaproteobacteria increased significantly while the relative abundance of Deltaproteobacteria decreased significantly in the Y group compared to the CT group. A significant increase in the relative abundance of Proteus was observed in the Y group, whereas the relative abundance of Desulfovibrio declined sharply. A network analysis revealed that average connectivity and sub-module numbers decreased in the Y group, suggesting that the complexity, efficiency, and robustness of the gut microbiota network in B. sinensis declined distinctly under the hypoxic condition. Clostridia was the main component serving as a module hub in the CT and Y group networks. Furthermore, most of the shared operational taxonomic units (OTUs) belonged to Clostridia. These results suggested that Clostridia both occupied an important position in the two networks of the B. sinensis gut microbiota, however the niche of Clostridia was notably altered based on its interactions with other species under the hypoxic condition. The interactions between Clostridia and other OTUs in the Y group network converted, indicating that a hypoxic condition could affect the function of Clostridia in the network. The homeostasis of the B. sinensis gut microbiota was disrupted under the hypoxic condition due to deterioration in the network structure resulting from a decrease in the number of module hubs and average connectivity. Microbial metabolism could be affected by the hypoxic conditions, and the abundant microbial functional pathways had advantage to the survival of B. sinensis. This study revealed the effects of DO on the composition of gut microbiota in B. sinensis and further illustrated the importance of interspecific interactions and species roles for evaluating the development and health of B. sinensis using an ecological network analysis of the gut microbiota.

Introduction

The culture environment is a critical factor that directly affects the health status, survival, growth and gut microbiota of reared animals (De Schryver and Vadstein, 2004; Flint et al., 2012; Lemonnier et al., 2010; Sharma et al., 2017). Dissolved oxygen (DO) is a primary requirement for aquatic animals. Many studies have demonstrated that the vast majority of aquatic animals maintain normal physiological and biochemical functions at DO concentrations >5 mg/L (Diaz and Breitburg, 2009; Gray et al., 2002). However, fish have evolved a relatively complete physiological response to avoid organism damage under hypoxic conditions, such as controlling respiration and circulation (Randall, 1982), increasing blood oxygen circulation (Silkin and Silkina, 2005), and improving the metabolism of substances and energy (Hochachka, 1997). Wannamaker and Rice (2000) demonstrated that aquatic animals can live under a hypoxic condition because of their behavioral and physiological adaptations. Braun et al. (2006) reported that the growth and metabolic parameters of silver catfish remained unchanged under different DO levels (1.96–6.16 mg/L). Filho et al. (2005) determined that the antioxidant response is enhanced in Megaleporinus obtusidens (piapara) under a low DO condition.

Many studies have observed the physiologic and biochemical responses of aquatic animals under hypoxic conditions. However, the mechanism for the gut microbiota to develop and maintain health of the host under a hypoxic condition has not been reported previously. It has been confirmed that the gut microbiota is a vital external organ of animals (O'Hara and Shanahan, 2006) that can regulate the development and physiology of the host (Sommer and Backhed, 2013). Although the gut microbiota plays a key role in maintaining the health and homeostasis of the host, variations in its composition induce metabolic shifts that may result in alterations of host phenotype (Turnbaugh et al., 2006; Visconti et al., 2019). Goodrich et al. (2016) and Xie et al. (2016) demonstrated that the structure of the gut microbiota is highly malleable and can be altered by environmental factors.

The composition and interspecific interactions of the gut microbiota in cultured sea cucumber were changed by a Bacillus cereus and rhubarb diet (Yang et al., 2019). Peng et al. (2019) reported that homeostasis of the gut microbiota in rice field eel becomes disturbed after they consume a high-fat diet. Ramírez and Romero (2017) demonstrated that the growth and the gut microbiota structure of cultured aquatic animals is influenced directly bythe environment.

However, the mechanism in controlling the homeostasis and health by the gut microbiota in aquatic animals under hypoxic conditions remains unclear. In our study, normoxic and hypoxic levels were chosen to investigate the effects of these two conditions on the immunity and gut microbiota of Bostrichthys sinensis. This is the first to analyze the changes in the gut microbiota of B. sinensis and provides a new perspective for understanding the response mechanism of the gut microbiota under hypoxic conditions.

Section snippets

Sample collection

Thirty healthy B. sinensis (~120 g each) were obtained from a farm in Guangxi Province. Fifteen individuals were obtained as the CT (normoxic) group from five normal feeding ponds where the DO was >6 mg/L. Sampling method: ten individuals were randomly caught from each pond and then three individuals (similar size) were randomly chosen from the ten individuals in each pond. The other 15 individuals were collected as the Y (hypoxic) group from a low-DO system (3–4.5 mg/L; Fig. S1). The low-DO

Water quality indices and antioxidant enzyme activities

The environmental factor results showed that pH and the concentrations of NH₄⁺-N, NO₂⁻-N and NO₃⁻-N, and PO₄⁻³-P were similar between the CT and Y groups, while DO content in the Y group was significantly lower than that in the CT group (P < .05) (Fig. S2). The SOD and CAT activities in the gill, hindgut, and liver were similar between the CT and Y groups (P > .05) (Fig. 1). Thus, the antioxidant system was not disrupted and crucial organs were not injured in B. sinensis under the hypoxic

Discussion

B. sinensis is distributed in the South Sea, Taiwan Strait, and the East Sea Coast and is widely cultured in southern coastal areas of China. Previous research has confirmed that B. sinensis can live in hypoxic conditions because of the skin-assisted respiration (Huang, 2018). However, the B. sinensis response mechanism under a hypoxic condition remains unclear. Superoxide dismutase (SOD) and catalase (CAT) are important antioxidant enzyme systems in aquatic animals, which can be used to

Conclusion

In this study, the effects of normoxic and hypoxic conditions on the responses of antioxidant enzymes and the gut microbiota were explored in B. sinensis. The results showed that the antioxidant response of B. sinensis did not change over the long-term under the hypoxic condition. The hypoxic condition altered the composition of the gut microbiota and decreased the diversity and richness of the intestinal microbial community in B. sinensis. Although Clostridia both occupied an important

Acknowledgement

This study was funded by the National Ocean Public Welfare Scientific Research Project of China (201505020-4) and the Basic Scientific Fund of the National Public Research Institutes of China (2011G20). The authors declared that they have no conflict of interests.

Declaration of Competing Interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

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Effects of normoxic and hypoxic conditions on the immune response and gut microbiota of Bostrichthys sinensis

Highlights

Abstract

Introduction

Section snippets

Sample collection

Water quality indices and antioxidant enzyme activities

Discussion

Conclusion

Acknowledgement

Declaration of Competing Interest

FEBS Lett.

Basic Appl. Ecol.

Toxicon

Fish Physiol.

Cell Host Microbe

Cell.

Mar. Pollut. Bull.

Aquaculture.

Phys. Lett. A

Aquaculture.

Aquaculture.

Aquaculture.

Aquaculture.

Fish Shellfish Immunol.

J. Exp.Mar. Biol. Ecol.

Aquaculture.

Merging mythology and morphology: the multifaceted lifestyle of Proteus mirabilis

Nat. Rev. Microbiol.

Network biology: understanding the cell’s functional organization

Nat. Rev. Genet.

Desulfovibrio putealis sp. nov., a novel sulfate-reducing bacterium isolated from a deep subsurface aquifer

Int. J. Syst. Evol. Microbiol.

Survival, growth and biochemical parameters of silver catfish, Rhamdia quelen (Quoy & Gaimard, 1824), juveniles exposed to different dissolved oxygen levels

Aquac. Res.

Comment on the utilization of dietary carbohydrates in fish

Acta Hydro Biol. Sin.

QIIME allows analysis of high-throughput community sequencing data

Nat. Methods

Microbiome evolution along divergent branches of the vertebrate tree of life: what is known and unknown

Mol. Ecol.

The ecology of microbiome, network, competition and stability

Science.

Proteus alimentorum sp. nov., isolated from pork and lobster in Ma’anshan city, China

Int. J. Syst. Evol. Microbiol.

Proteus columbae sp. nov., isolated from a pigeon in Ma’anshan, China

Int. J. Syst. Evol. Microbiol.

Ecological theory as a foundation to control pathogenic invasion in aquaculture

The ISME J.

Molecular ecological network analyses

BMC Bioinform.

Effect of different oxygen tensions on weight gain, feed conversion, and antioxidant status in piapara, Leporinus elongatus (Valenciennes, 1847)

Aquaculture.

The role of the gut microbiota in nutrition and health

Nat. Rev. Gastroenterol. Hepatol.

Desulfovibrio desulfuricans bacteremia and review of human Desulfovibrio infections

J. Clin. Microbiol.

Effects of hypoxia and organic enrichment on the marine environment

Mar. Ecol. Prog. Ser.

Dietary threonine requirement of juvenile Japanese seabass (Lateolabrax japonicus)

J. Fish. China

Oxygen-a key regulatory metabolite in metabolic defense against hypoxia

Am. Zool.

Acidified Sea Water Cause Skin Ulceration in Chinese Black Sleeper (Bostrychus sinensis)

Proteus mirabilis and urinary tract infections

Microbiol. Spectr.

The robustness of pollination networks to the loss of species and interactions: a quantitative approach incorporating pollinator behaviour

Ecol. Lett.

Microbial diversity of intestinal contents and mucus in rainbow trout (Oncorhynchus mykiss)

J.Appl.Microbiol.

Biological robustness

Nat. Rev. Genet.