Protective effects of Devosia sp. ANSB714 on growth performance, immunity function, antioxidant capacity and tissue residues in growing-finishing pigs fed with deoxynivalenol contaminated diets
Introduction
Deoxynivalenol (DON) is a natural-occurring type B trichothecene mainly produced by Fusarium species. DON contamination is commonly found in cereal grains, particularly in corn, wheat and barley as well as their processed products. A three-year survey showed that DON was the most frequently detected mycotoxin of corn in Central Europe and North America with the presence of positive samples over 70% in these regions (Rodrigues and Naehrer, 2012). In China, the incidence of DON was 93% for corn and 97% for complete feeds while 57 percent of corn sample exceeded the maximum limits allowed by local legislation (Li et al., 2014). Besides, it has to be pointed out that DON contamination fluctuates annually with climatic conditions and planting pattern affecting the prevalence of Fusarium (Bernhoft et al., 2012). DON is a very stable compound and can withstand common food or feed processing procedures at high temperatures and high pressure; thus, this mycotoxin is transferred to human and animal food chains (Wu et al., 2011). The residues of DON in animal edible tissues and products, such as liver, meat, black pudding (a traditional sausage made by pig blood in China) and so on, could be a hazard for human health. Thus, the potential health risks to human and animals from DON exposure have attracted broad attention. DON can cause malabsorption of nutrients, nausea, vomiting, emesis and diarrhea in humans (Pestka and Smolinski, 2005; Sobrova et al., 2010). In China, gastroenteritis outbreaks (1984–1991) affecting 130000 people were linked to consumption of DON and other trichothecene-contaminated foods. At the cellular level, DON toxicity is associated with its ability to inhibit protein and nucleic acid synthesis as well as induce ribotoxic stress response (Pestka, 2010; Pinton et al., 2012). Gastrointestinal tract and immune system are central targets of DON toxicity (Rotter et al., 1996). DON is known to induce either immunostimulation or immunosuppression depending on dose, exposure duration and type of immune function assay (Rotter et al., 1996; Pestka et al., 2004; Sobrova et al., 2010).
Swine exhibits the highest sensitivity to DON among domestic animals (Rotter et al., 1996). The maximum tolerated DON concentration at which no obvious detrimental effects are expected, is 0.9 mg/kg in porcine feed according to European Commission Recommendation (Official Journal of the European Union, 2006). However, Alizadeh et al. (2015) documented that DON treatment of pigs at dose of 0.9 mg/kg feed for ten days caused distinct histological and biochemical changes in the intestinal tract. Growth depression and intestinal barrier impairment are initial toxic effects of DON in swine. Besides, DON intoxication disrupts the vaccinal immune response in pigs, which may increase host susceptibility to infectious disease even in properly vaccinated populations (Chen et al., 2008; Pinton et al., 2008). The adverse effect of DON in pigs was also manifested as induction of oxidative stress (Xiao et al., 2013; Van Le Thanh et al., 2016). It is shown that intracellular oxidative damage generated by DON resulted in production of lipid peroxidation, DNA fragment and protein carbonylation (Mishra et al., 2014). To date, several nutritional additives like arginine-family amino acids, exogenous antioxidants and composite antimicrobial peptides have been reported to mitigate DON toxicosis in pigs (Xiao et al., 2013; Van Le Thanh et al., 2016). Alleviation of DON toxicity by most nutritional treatments is due to the improvement of immune function, antioxidant ability and nutrient metabolism. A study indicated that dietary non-enzymatic antioxidants failed to prevent DON absorption in intestinal, as reflected by no reduction of DON residues in piglets serum (Mishra et al., 2014).
Academics have been trying over the decades to develop effective strategies for mycotoxin detoxification or inactivation. The multifaceted approaches reported previously could be simply categorized into physical, chemical and biological methods. Amongst them, biological approaches, namely bio-degradation taking the form of microbial and enzymatic transformation of mycotoxins, tend to predominate for its high efficiency and specificity. Several microorganisms as well as their cultures from diversified sources, such as Eubacterium strain BBSH 797 from rumen fluid (Fuchs et al., 2002), Bacillus sp. LS100 from chicken digesta (Yu et al., 2010), gram-negative bacterium strain E3-39 from enriched soil (Shima et al., 1997), and microbial culture C133 from fish gut (Guan et al., 2009) have been reported to display DON transformation capacity. However, systematic study on the potential of pure bacterial culture incorporated in feed industry was scanty, which to some extend limited the development of biological control of DON contamination. So far, Eubacterium strain BBSH 797 is the only microorganism that has been applied as feed additive (He and Zhou, 2010). Devosia sp. ANSB714 originating from soil could degrade 97.34% DON for 24 h, and the bacteria was shown to remarkably reduce the detrimental impacts of dietary DON on mice in our previous study (Zhao et al., 2016). In order to further evaluate the application potential of Devosia sp. ANSB714 in livestock production, this study was conducted to investigate the efficiency of Devosia sp. ANSB714 in counteracting DON-induced negative effects in growing-finishing pigs.
Section snippets
Preparation of moldy rice
The deoxynivalenol producer, Fusarium graminearum 37687, was kindly provided by the Agricultural Culture Collection of China (ACCC). The fungal was inoculated on Potato-dextrose Agar (PDA) and cultivated at 25 °C for 7 days. Mycotoxin production assays were carried either on 250 mL Erlenmeyer flasks containing 25 g of rice added with 25 mL water. Recipients were filled with rice. These substrates were tested for deoxynivalenol content before use. They were autoclaved at 121 °C for 20 min and
Growth performance
Effects of Devosia sp. ANSB714 on growth performance of growing-finishing pigs exposed to DON are presented in Table 2. Pigs exposed to DON had reduced (P < 0.05) average daily gain (ADG) in contrast to the CON, while average daily feed intake (ADFI) and feed: gain ratio (F: G) were not significantly affected (P > 0.05) by dietary DON. Compared with the CON, the supplement of the Devosia sp. ANSB714 in the drinking water of DON-contaminated diet group significantly increased (P < 0.05) ADG by
Growth performance
DON is by far the most prevalent trichothecene produced by several species of the genus Fusarium that colonize various cereals. Due to the infection of Fusarium in the field and during the storage, DON contamination is commonly found in feed and feedstuffs, which poses enormous economic losses to animal husbandry industry worldwide. In swine, the initial detrimental effect is growth depression after DON exposure. In a recent report, reduced ADG was observed in growing piglets after ten-day
Notes
The authors declare no competing financial interest.
Acknowledgement
This study was supported by the National Natural Science Foundation of China (grant number 31301981), the Special Fund for Agro-scientific Research in the Public Interest (grant number 201403047), the Program of State Key Laboratory of Animal Nutrition of China (2016-2020), and the Beijing Municipal Natural Science Foundation (grant numbers 6172017, 6132021). We thank the participants of the study.
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These authors are equal contribution to this work.