Altered Fecal Microbiome and Correlations of the Metabolome with Plasma Metabolites in Dairy Cows with Left Displaced Abomasum

Luo, Zhengzhong; Yong, Kang; Luo, Qiao; Du, Zhenlong; Ma, Li; Huang, Yi-Xin; Zhou, Tao; Yao, Xueping; Shen, Liuhong; Yu, Shumin; Deng, Junliang; Ren, Zhihua; Zhang, Yong; Yan, Zuoting; Zuo, Zhicai; Cao, Suizhong

doi:10.1128/spectrum.01972-22

Cited by 6 publications

(9 citation statements)

References 59 publications

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“…Accumulating evidence suggests that the BCAAs, as gut microbiota-derived metabolites, can induce the insulin resistance by activating mammalian target of rapamycin complex 1 ( 29 , 61 ). We previously reported that the levels of isoleucine and leucine were markedly increased in dairy cows with left displaced abomasum events and were strongly correlated with the abundances of Akkermansia and Oscillospira in the feces ( 38 ). However, unlike leucine, an increase in isoleucine and valine levels adversely affects metabolic health by disturbing glucose homeostasis ( 62 ).…”

Section: Discussionmentioning

confidence: 99%

“…After sample pre-treatment, fecal metabolome profiling was performed using ultra-high-performance liquid chromatography (UHPLC; Agilent 1290 Infinity II, Santa Clara, CA, USA) with tandem mass spectrometer (MS/MS; Triple Time-of-Flight 6600, AB SCIEX, Framingham, MA, USA). The pre-treatment conditions and equipment parameters are described in our previous report ( 38 ). The mass/charge ratio, retention time, and peak area of the metabolomic features were extracted using the XCMS ( https://xcmsonline.scripps.edu ) platform.…”

Section: Methodsmentioning

confidence: 99%

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Alterations in the gut microbiota and its metabolites contribute to metabolic maladaptation in dairy cows during the development of hyperketonemia

Luo,

Du,

Huang

et al. 2024

mSystems

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Metabolic maladaptation in dairy cows after calving can lead to long-term elevation of ketones, such as β-hydroxybutyrate (BHB), representing the condition known as hyperketonemia, which greatly influences the health and production performance of cows during the lactation period. Although the gut microbiota is known to alter in dairy cows with hyperketonemia, the association of microbial metabolites with development of hyperketonemia remains unknown. In this study, we performed a multi-omics analysis to investigate the associations between fecal microbial community, fecal/plasma metabolites, and serum markers in hyperketonemic dairy cows during the transition period. Dynamic changes in the abundance of the phyla Verrucomicrobiota and Proteobacteria were detected in the gut microbiota of dairy cows, representing an adaptation to enhanced lipolysis and abnormal glucose metabolism after calving. Random forest and univariate analyses indicated that Frisingicoccus is a key bacterial genus in the gut of cows during the development of hyperketonemia, and its abundance was positively correlated with circulating branched-chain amino acid levels and the ketogenesis pathway. Taurodeoxycholic acid, belonging to the microbial metabolite, was strongly correlated with an increase in blood BHB level, and the levels of other secondary bile acid in the feces and plasma were altered in dairy cows prior to the diagnosis of hyperketonemia, which link the gut microbiota and hyperketonemia. Our results suggest that alterations in the gut microbiota and its metabolites contribute to excessive lipolysis and insulin insensitivity during the development of hyperketonemia, providing fundamental knowledge about manipulation of gut microbiome to improve metabolic adaptability in transition dairy cows. IMPORTANCE Accumulating evidence is pointing to an important association between gut microbiota-derived metabolites and metabolic disorders in humans and animals; however, this association in dairy cows from late gestation to early lactation is poorly understood. To address this gap, we integrated longitudinal gut microbial (feces) and metabolic (feces and plasma) profiles to characterize the phenotypic differences between healthy and hyperketonemic dairy cows from late gestation to early lactation. Our results demonstrate that cows underwent excessive lipid mobilization and insulin insensitivity before hyperketonemia was evident. The bile acids are functional readouts that link gut microbiota and host phenotypes in the development of hyperketonemia. Thus, this work provides new insight into the mechanisms involved in metabolic adaptation during the transition period to adjust to the high energy and metabolic demands after calving and during lactation, which can offer new strategies for livestock management involving intervention of the gut microbiome to facilitate metabolic adaptation.

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Section: Discussionmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Alterations in the gut microbiota and its metabolites contribute to metabolic maladaptation in dairy cows during the development of hyperketonemia

Luo,

Du,

Huang

et al. 2024

mSystems

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“…UHPLC-Q-TOF MS was performed at Shanghai Applied Protein Technology Co., Ltd. The sample pretreatment, equipment parameters, and metabolite identification methods were the same as those used in our previous report ( Luo et al, 2022 ).…”

Section: Methodsmentioning

confidence: 99%

Screening for potential warning biomarkers in cows with ketosis based on host–microbiota co-metabolism analysis

Du,

Luo,

Huang

et al. 2024

Front. Microbiol.

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IntroductionThe risk of ketosis is assessed by monitoring changes in plasma metabolites and cow behavior during the peripartum period. However, little is known about changes in the fecal bile acid and microbiota of cows before parturition. Therefore, this study clarified the bile acid profile and screened potential warning biomarkers in heifers 7 days before calving.MethodsNinety healthy cows were tracked in the transition period, and plasma and feces were collected 7 days before calving, on calving day, and 7 days after calving. The cows were divided into ketosis and healthy groups based on the blood β-hydroxybutyric acid levels from day 7 after calving. The levels of serum biochemical indices were measured at three time points using commercial kits. Ten cows in the ketosis group (KET-7) and 10 healthy cows (HEA-7) were randomly selected 7 days before calving for metabolome and 16S rRNA amplicon sequencing.ResultsNo significant differences in serum energy-related indices were observed 7 days before calving. The major bile acids in the feces of the KET-7 group were non-conjugated secondary bile acids (UnconSBA). Differential bile acids were primarily derived from UnconSBA. The potential ketosis warning metabolite in feces for 7 days before delivery was isodeoxycholic acid. The abundance of Rikenellaaceae-RC9-gut-group in the KET-7 group increased, whereas the abundance of Oscillospiraceae UCG-010 bacteria significantly decreased. Lactobacillus and Prevotella-9 in feces were potential warning biomarkers for ketosis in dairy cows 7 days before calving. The variation in differential bile acids in the plasma, consistent with the feces, was mainly derived from UnconSBA. Lithocholic acid in the plasma was a potential ketosis warning metabolite 7 days before delivery.ConclusionKetotic cows experienced bile acid metabolism disorders 7 days before calving, and the gut microbiota was closely related to bile acid metabolism disorders. Future studies should investigate the relationship between secondary bile acids and the development of ketosis.

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“…Furthermore, the amount of dietary nutrients in the digesta might also play a pivotal role in nutrient supply not only for the host but also for the microbiota community thus shaping the microbial composition. A recent study demonstrated that gastrointestinal microbiota dysbiosis is linked to the development of feed intake-related diseases such as left displaced abomasum (LDA) in dairy cows (17).…”

Section: Introductionmentioning

confidence: 99%

“…Moreover, Luo et al (2022) hypothesized that in the context of LDA, the microbiota dysbiosis is associated with higher serum NEFA and BHB in dairy cows (17). Increased plasma NEFA concentrations induced by intravenous lipid infusion reduced the relative abundances of genera belonging to Succinivibrio, Ruminococcaceae, and Ruminiclostridium, and greater relative Bacteroidetes genus abundances in the rumen of dairy cows (18), suggesting that besides dietary effects changes in the concentration of circulatory metabolites exert an in uence on the digestal and eventually the epimural microbiome.…”

Section: Introductionmentioning

confidence: 99%

Heat stress and feeding effects on the mucosa-associated and digesta microbiome and their relationship to plasma and digesta fluid metabolites in the jejunum of dairy cows

Koch,

Reyer,

Görs

et al. 2023

Preprint

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The intestinal microbiota plays a pivotal role in digestive processes and maintains gut health and intestinal homeostasis. These functions may be compromised by increased environmental heat which in turn reduces feed intake and gut integrity, while activating the intestinal immune system. However, it is not known whether high ambient temperatures, causing heat stress (HS) to dairy cows, disturb the eubiosis of the microbial community and if so, to which extent the reduction in feed intake and the impairment of circulating and intestinal metabolites induced by HS account for the alterations of the jejunal microbiota. To address these questions, jejunal digesta, mucosa, and plasma samples from cows exposed to heat stress (HS: 28°C, temperature-humidity-index (THI) = 76, n = 10), or control conditions (CON: 16°C, THI = 60, n = 10), or pair-feeding (PF: 16°C, THI = 60, n = 10) for 7 days were collected. Digesta fluids were examined for pH, acetate, non-esterified fatty acids (NEFA), glucose, and lactate, whilst plasma metabolites were analyzed for glucose, lactate, beta-hydroxybutyrate (BHB), triglycerides, NEFA, creatinine and urea. The microbiota composition of digesta and mucosa samples were analyzed by 16S rRNA sequencing. The alpha diversity was higher in mucosa than digesta, but not affected by high ambient temperatures. However, the mucosa-associated microbiota appears more prone to ambient heat than the digesta microbiome. Furthermore, HS cows showed a greater mucosal abundance of Bifidobacteriaceae, Succinivibrionaceae UCG-001, Clostridia and a trend for Lactobacillus compared to CON cows. In the digesta, lower abundance of Colidextribacter and a trend for lower Lachnospiraceae UCG-008 were found in HS than CON cows. Several correlations between plasma or intestinal metabolites and microbiota were elucidated, including Methanobacteriaceae correlating positively with plasma BHB and digesta glucose concentrations. The shifts in the microbial profile of the small intestine give some implications for the adaptive responses under HS conditions. Moreover, the reduction in feed intake during HS had non-negligible effects on microbial diversity and the abundance of certain taxa, underpinning the importance of nutrient supply on maintaining intestinal homeostasis.

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Altered Fecal Microbiome and Correlations of the Metabolome with Plasma Metabolites in Dairy Cows with Left Displaced Abomasum

Cited by 6 publications

References 59 publications

Alterations in the gut microbiota and its metabolites contribute to metabolic maladaptation in dairy cows during the development of hyperketonemia

Alterations in the gut microbiota and its metabolites contribute to metabolic maladaptation in dairy cows during the development of hyperketonemia

Screening for potential warning biomarkers in cows with ketosis based on host–microbiota co-metabolism analysis

Heat stress and feeding effects on the mucosa-associated and digesta microbiome and their relationship to plasma and digesta fluid metabolites in the jejunum of dairy cows

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