Suhuai suckling piglet hindgut microbiome-metabolome responses to different dietary copper levels

Abstract

Unabsorbed copper accumulates in the hindgut of pigs that consume high levels of dietary copper, which enhances the coselection of antibiotic-resistant bacteria and is considered detrimental to the environment and to porcine health. In our study, a combination of 16S rRNA pyrosequencing and nontargeted metabolomics was used to investigate the microbiome-metabolome responses to dietary copper levels in the hindgut of suckling piglets. The results showed that the dietary copper level affected the abundance of several Clostridia genera and that the relative abundance of butyrate-producing bacteria, such as Coprococcus , Roseburia , and Acidaminococcus , was reduced in the 300 mg kg −1 (high) Cu group. Metabolomic analysis revealed that dietary copper levels affected protein and carbohydrate metabolites, protein biosynthesis, the urea cycle, galactose metabolism, gluconeogenesis, and amino acid metabolism (including the metabolism of arginine, proline, β-alanine, phenylalanine, tyrosine, and methionine). Furthermore, Pearson’s correlation analysis showed that the abundance levels of Coprococcus (family Lachnospiraceae ) and operational taxonomic unit (OTU) 18 (family Ruminococcaceae ) were positively correlated with energy metabolism pathways (gluconeogenesis, glycolysis, and the pentose phosphate pathway). The abundance of Streptococcus was negatively correlated with amino acid metabolism pathways (protein biosynthesis, glycine, serine, threonine, methionine, phenylalanine, and tyrosine metabolism), and OTU583 and OTU1067 (family Rikenellaceae ) were positively correlated with amino acid metabolism pathways. These results suggest that the copper levels consumed by LC (low-copper group) versus HC (high-copper group) animals alter the composition of the gut microbiota and modulate microbial metabolic pathways, which may further affect the health of suckling piglets. Electronic supplementary material The online version of this article (10.1007/s00253-018-9533-0) contains supplementary material, which is available to authorized users.

Effect of Dietary Copper on Intestinal Microbiota and Antimicrobial Resistance Profiles of Escherichia coli in Weaned Piglets

“…As most bacterial species in the gut are yet to be cultured, 16S rRNA gene sequencing is recommended for the analysis of gut microbial communities. In the present study, unweighted pair-group method with arithmetic mean analysis showed that Firmicutes, Bacteroidetes, and Proteobacteria were the most abundant phyla in the ileum and cecum, which is similar to previous findings in piglets (Xiong et al, 2019;Zhang et al, 2019). Linear discriminant analysis effect size analysis also showed that the differences included, but were not limited to, the phylum Firmicutes, the family, Clostridiaceae, and the genera, Streptococcus, Lactococcus, and Ruminococcaceae, which were found to be affected in previous studies in which Cu was supplemented at high levels (200-300 mg/kg) as CuSO 4 (Fuller et al, 1960;Kellogg et al, 1966;Varel et al, 1987;Hojberg et al, 2005;Xia et al, 2005;Namkung et al, 2006;Mei et al, 2010;Wang et al, 2012;Song et al, 2013;Zhang et al, 2019).…”

“…In our study, α diversity indices, including observed_species, Shannon, Simpson, Chao1, ACE, and PD_whole_tree indices were not affected by dietary Cu. Our results were consistent with those of a previous study of high dietary Cu levels (300 mg/kg) in suckling piglets (Zhang et al, 2019) but in contrast to previous studies reporting that high dietary Cu levels (100-200 mg/kg, as CuSO 4 ) significantly affect microbial species in the ileac, cecal, and colonic chyme of piglets (Varel et al, 1987;Hojberg et al, 2005;Namkung et al, 2006;Mei et al, 2010). A possible reason for these differences is that the method used to investigate the microbial flora is inconsistent among the different studies.…”

“…Meanwhile, there are increasing concerns regarding the potential adverse effects of Cu accumulation on the intestinal microbiota, i.e., microbial drug resistance (Hasman and Aarestrup, 2005;Hasman et al, 2006;Djoko et al, 2008;Amachawadi et al, 2011;Zimmermann et al, 2012;Agga et al, 2014;Yazdankhah et al, 2014). The effects of Cu on the counts of coliforms and microbial drug resistance have previously been reported (Djoko et al, 2008; Zimmermann et al, 2012;Zhang et al, 2019). Thus, the present research focused on microbial diversity, composition, and function, as well as the potential risks of E. coli resistance in the intestine of piglets after pharmacological doses of Cu.…”

“…Meanwhile, excess amounts of Cu in the gut can affect the intestinal microbial community and result in reduced counts of streptococci, ureolytic bacteria, and total anaerobes in the feces (Fuller et al, 1960;Kellogg et al, 1966;Varel et al, 1987). Recently, it has been found that feeding piglets with 300 mg Cu/kg feed affected the abundance of Clostridium genera and decreased the relative abundance of butyrate-producing bacteria, such as Acidaminococcus, Coprococcus, and Roseburia in fecal microbiota (Zhang et al, 2019). It also altered the gut microbiota and decreased the counts of Lactobacilli and Enterobacteriaceae in the cecum and ileum of weaned piglets (Ole et al, 2005;Mei et al, 2010).…”

Gut Microbiota Changes in Patients with Bipolar Depression

“…[12,20] In our study, MADRS scores were negatively correlated with Acetanaerobacterium, Stenotrophomonas, Anaerotruncus, and Raoultella levels, and positively correlated with Acinetobacter and Cronobacter levels. [34] Therefore, lower Ruminococcaceae in BD patients was possibly related to abnormal glucose metabolism. [13] We also found higher abundance of Ruminococcaceae family in HCs.…”