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Article

Nano-Selenium Reduces Concentrations of Fecal Minerals by Altering Bacteria Composition in Feedlot Goats

by
Hu Liu
1,
Kaiyu Mao
1,2,
Weishi Peng
1,
Allan Degen
3,
Gang Zuo
4,
Yuanting Yang
1,
Jiancheng Han
1,*,
Qun Wu
1,
Ke Wang
1,
Qinyang Jiang
2 and
Hanlin Zhou
1,2,5,*
1
Zhanjiang Experimental Station, Chinese Academy of Tropical Agricultural Sciences, Zhanjiang 524013, China
2
College of Animal Science and Technology, Guangxi University, Nanning 530004, China
3
Desert Animal Adaptations and Husbandry, Wyler Department of Dryland Agriculture, Blaustein Institutes for Desert Research, Ben-Gurion University of Negev, Beer Sheva 8410500, Israel
4
Beijing Deyuanshun Biotechnology Co., Ltd., Beijing 102206, China
5
Sanya Research Institute, Chinese Academy of Tropical Agricultural Sciences, Sanya 572025, China
*
Authors to whom correspondence should be addressed.
Agriculture 2024, 14(12), 2233; https://doi.org/10.3390/agriculture14122233
Submission received: 23 October 2024 / Revised: 27 November 2024 / Accepted: 3 December 2024 / Published: 6 December 2024
(This article belongs to the Section Farm Animal Production)
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Abstract

:
This study examined the effect of dietary supplementation of nano-selenium (nano-Se) on the average daily gain (ADG), fecal bacteria community, and concentrations of fecal minerals and volatile fatty acids in feedlot Hainan black goats. Eighteen goats (18.6 ± 0.69 kg) were divided randomly into three groups, with each group receiving a different level of supplementary nano-Se (n = six goats per treatment) as follows: (1) 0.0 mg (CON); (2) 0.2 mg; and (3) 0.4 mg nano-Se/kg dry matter intake (DMI). The final body weight (p = 0.012) and ADG increased linearly (p < 0.01), whereas the ratio of DMI to ADG decreased linearly (p < 0.01) with increasing dietary nano-Se levels. Fecal concentrations of Se increased linearly (p < 0.001), whereas Cu (p < 0.01), Zn (p = 0.020), and Fe (p = 0.010) decreased linearly with increasing dietary nano-Se levels. The relative abundances of Treponema (p = 0.046), norank_f__norank_o__Clostridia_UCG-014 (p < 0.01), norank_ f_norank_o__RF39 (p < 0.01), Eubacterium_siraeum_group (p < 0.001), and Family_XIII_AD3011_group (p = 0.040) increased linearly, and unclassified_f__Lachnospiraceae (p < 0.001), Rikenellaceae_RC9_gut_group (p < 0.01), Eubacterium_ruminantium_group (p = 0.021), and Prevotella (p < 0.001) decreased linearly with increasing dietary nano-Se levels. It was concluded that supplementary nano-Se could improve ADG and reduce the DMI to ADG ratio and fecal heavy metals by altering the bacterial community in feedlot goats. We recommend a dietary supplementation of approximately 0.4 mg nano-Se/kg DM for feedlot Hainan black goats, but further research is warranted to determine the precise dose and the possible contamination risks of Se.

1. Introduction

Livestock provide food, fiber, manure, and transport for people [1,2]. It is estimated that they contribute approximately 18% of the caloric and at least 25% of the protein intake of people globally [3]. With the demand for animal products predicted to grow, an increase and improvement in animal products would be beneficial for future food security. However, heat stress can become a potential widespread risk to animals, as it is predicted that the average global temperature will increase by at least 1.5 °C by the mid-2030s [4]. An increase in temperature can affect reproduction and growth rate of livestock, and, therefore, heat-adapted animals could be preferable in the future in many regions of the world [5,6].
Hainan black goats, raised in southern China, are tolerant of high temperature and high humidity, as are many goat breeds [7], and the quality of their meat is very good. However, these goats are small and their growth rate is considered only moderate [8]. Improving the average daily gain (ADG) of these goats would improve the livelihood of the goat farmers and food security in the region.
It was reported that supplementary dietary selenium (Se), an essential mineral, improved the ADG of growing male goats [9]. In addition, Se possesses anti-inflammatory properties and is reputed to prevent cardiovascular diseases, infections, and cancer [10,11], and to alleviate heat stress in livestock [12]. There are several Se sources offered to animals, and it was concluded that organic sources are more effective than inorganic sources [2]. Currently, with the fast development in nanotechnology, nano-selenium (nano-Se) is available and is relatively cheap [13], but its impact on goats has not been examined. One of the aims of this experiment was to fill this important gap and examine the effect of nano-Se on the ADG of Hainan black goats.
Microorganisms, especially bacteria, play crucial roles in the physiology, health, and ADG of the host [14,15,16]. The composition and dynamic diversity of microorganisms are impacted by multiple factors, including diet, environment, gender, age, and breed of the host [17,18]. Microorganisms ferment dietary carbohydrates and produce microbial metabolites, in particular, volatile fatty acids (VFAs), which provide approximately 70% of the total energy needs of ruminants [19,20,21] while also affecting ADG. Therefore, it is likely that the composition of the microorganisms would be altered if the ADG of the animal is affected. Moreover, it was reported that dietary Se supplementation affected the concentrations of minerals in rumen fluid and feces in ruminants [14]. Fecal minerals can pollute the environment, but there is little information on the effect of Se on fecal minerals and bacterial communities. Additional aims of this study were to fill these gaps. We hypothesized that supplementary nano-Se would (1) improve ADG and reduce the DMI to ADG ratio; (2) alter the composition of fecal bacteria; (3) affect concentrations of minerals in the rumen and serum; and (4) affect minerals and VFAs concentrations in feces in goats. We tested these hypotheses by offering feedlot Hainan black goats different levels of supplementary nano-Se.

2. Materials and Methods

This study was carried out at the Zhanjiang Experimental Station, Zhanjiang, Guangdong Province, P.R., China, from June to August 2023. All procedures on the Hainan black goats were approved by the Animal Care Committee of Zhanjiang Experimental Station, Chinese Academy of Tropical Agricultural Sciences (protocol number: CATAS-20230601ZES).

2.1. Goats, Diets, and Experimental Design

Eighteen growing Hainan black goats (initial body weight: 18.6 ± 0.69 kg), 8 months of age, were held in individual cages (80 cm × 120 cm) equipped with feeders and automatic waterers. The goats were offered an ad libitum pelleted diet (Table 1) that was formulated for growing goats [22]. The goats were assigned randomly into one of 3 groups (n = 6), each receiving a different level of supplementary nano-Se mixed in the diet: 0.0 (control), 0.2, and 0.4 mg nano-Se/kg DM. The nano-Se was in powder form and 40–60 nm in size (Beijing Deyuanshun Biotechnology Co., Ltd., Beijing, China). Weighed feed was offered the goats twice daily, at 08:00 and 17:00, and the feed remains were collected and weighed daily before 08:00. The experiment lasted for 8 weeks, in which the first 2 weeks allowed the goats to adapt to the conditions, and measurements were taken over the next 6 weeks. Water was freely available.

2.2. Experimental Procedures and Collection of Samples

At the beginning and the end of the experiment, the goats were fasted for 12 h and then weighed before morning feed. The ADG was calculated over the 42-day period. A dry and wet bulb thermometer (Kimo Industry Co., Biarritz, France) was set at 1.0 m above the ground in the center of the goat cages. Temperature and humidity were recorded at 08:00, 10:00, 12:00, 14:00, 16:00, and 18:00 daily and averaged. The temperature humidity index (THI) was calculated using the following equation [23]:
THI = (1.8 × Tdb + 32) − [(0.55 − 0.0055 × RH) × (1.8 × Tdb − 26.8)]
where Tdb = ambient temperature and RH = the relative humidity/100. A THI ≥ 72 is considered to heat-stress the animal [24].
Before morning feedings on days 55 and 56, rectal temperatures were measured using a digital rectal thermometer (SAT-1, Shangnong Electronic Technology Co., Ltd., Linyi, China), and fecal samples were collected manually following the method described by Lourenco et al. [25] and stored at −80 °C for determination of VFAs and the bacterial community. In addition, fecal samples were collected 8 times during days 55 and 56 at 0:00, 06:00, 12:00, and 18:00 and then mixed and stored at −20 °C for measurements of mineral concentrations.
On day 56 before 08:00, 10 mL of jugular blood and 25 mL of rumen content were collected from each goat, and serum and rumen fluid samples were prepared following the method of Liu et al. [18].

2.3. Sample Analyses

The 3 feed and 18 fecal samples were dried at 65 °C for 96 h in a forced-air oven (DHG-9123A, Jiecheng Experimental Apparatus, Shanghai, China), air-equilibrated for 12 h at night, ground to pass through a 1 mm sieve, and stored in self-sealing plastic bags. The dry matter (method 925.45), ether extract (method 920.2), organic matter (method 942.05), and nitrogen (method 942.05) contents were determined as described by the Association of Official Analytical Chemists [26]. The crude protein of the feed was calculated as 6.25 × N, and neutral and acid detergent fibers were measured by a fiber analyzer (Ankom Technology, Fairport, NY, USA) following Van Soest et al. [27] and Robertson and Van Soest [28], respectively.
Measurement of Se, iron (Fe), copper (Cu), manganese (Mn), zinc (Zn), calcium (Ca), and phosphorus (P) concentrations in the feed, rumen fluid, serum, and feces followed the method of Yang et al. [29]. Briefly, 1 g (1 ± 0.05 g) of dried feces or feed, or 1.00 mL of rumen fluid or serum, was mixed with 15 mL digesting solution (perchloric acid nitric acid, v:v = 1:3) in triplicate and kept at room temperature overnight. The mixture was heated to 80 °C, then to 120 °C, 180 °C, and 220 °C for 1 h each, and then combusted completely at 500 °C (Multiwave 3000, Anton Paar, Buchs Aargau, Switzerland). The ash was suspended in 15 mL 1% nitric acid and filtered, and then Fe, Cu, Mn, Zn, Ca, and P concentrations were measured by inductively coupled plasma-optical emission spectroscopy (ICP-MS 7900; Agilent, Palo Alto, CA, USA). The Se concentration was measured by hydride-atomic fluorescence spectrometry (iCE 3300 AAS, Thermo Fisher Scientific, Rockford, IL, USA) coupled with a standard reference of Se (GBW8551, National Sharing Platform for Reference Materials, Beijing, China).

2.4. Measurement of Fecal Volatile Fatty Acids (VFAs)

One g of frozen feces was vortexed with 4 mL ultrapure water, shaken at 4 °C for 3 h, and centrifuged at 15,000× g for 15 min. Then, 1.0 mL of the supernatant was transferred into a 2 mL centrifuge tube containing 200 μL of 25% (w/v) metaphosphoric acid. The mixture was hand-shaken for 60 s and then kept at −20 °C for 12 h, centrifuged at 15,000× g for 15 min, and 1.0 mL was pipetted into a new centrifuge tube and passed through a 0.22 μm filter membrane. The individual VFA concentrations of the feces were measured by gas chromatography (GC, Agilent 7890A, and Agilent Inc., Santa Clara, CA, USA) following Liu et al. [18], and are presented as mM/fresh weight of feces.

2.5. DNA Extraction of Feces, 16S rRNA Gene Amplification, and Sequencing

Total genomic DNA from 200 mg of goat feces was extracted using an E.Z.N.A® kit (Omega Bio-tek, Norcross, GA, USA), and following the standard protocol. The yield and purity of the extracted DNA were determined by using an ND 2000 UV–Vis spectrophotometer (NanoDrop Technologies, Wilmington, DE, USA) at a 260/280 nm ratio (1.8 to 2.2), and the integrity of the extracted DNA was tested using 1% agarose gel electrophoresis (Axygen Biosciences, Union City, CA, USA). All the extracted DNA was frozen and stored at −80 °C for later analysis.
The conventional polymerase chain reaction (PCR) amplification and the bioinformatic analysis were performed by Shanghai Majorbio Bio-Pharm Technology Co., Ltd. (Shanghai, China). The V3–V4 of bacterial 16S ribosomal ribonucleic acid (rRNA) gene was amplified with the specific primers 338F (5′-barcode-ACTCCTACGGGAGGCAGCAG-3′) and 806R (5′-barcode-GGACTACHVGGGTWTCTAAT-3′). The reactions for PCR were conducted 3 times as follows: initial denaturation at 95 °C for 3 min, followed by 30 cycles of denaturing at 95 °C for 30 s, annealing at 55 °C for 30 s, elongation at 72 °C for 45 s, and a final single elongation at 72 °C for 10 min. The 20 μL PCR mixtures consisted of 4 μL of TransStart FastPfu buffer (5×), 2 μL of dNTPs (2.5 mM), 0.8 μL of forward primer (5 μM), 0.8 μL of reverse primer (5 μM), 0.4 μL of TransStart FastPfu DNA Polymerase, 10 ng of template DNA, and double-distilled H2O (ddH2O) up to 20 μL. The products of PCR were tested by agarose gel electrophoresis (concentration 2%), purified using the AxyPrep DNA Gel Extraction Kit (Axygen Biosciences, Union City, CA, USA) following the instructions of the manufacturer, and then quantified using Quantus™ Fluorometer (Promega, Madison, WI, USA).
The purified amplicons were combined in equimolar quantities and paired-end sequenced on an Illumina MiSeq PE 300 platform (Illumina, Inc., San Diego, CA, USA) by Majorbio Bio-Pharm Technology Co. Ltd. (Shanghai, China) following standard protocols. All the data from fecal bacteria communities were analyzed at the free online resource https://www.majorbio.com/ (accessed 18 February 2024), developed by Majorbio Cloud Platform (Shanghai, China). The raw 16S rRNA gene sequencing reads were demultiplexed, quality-filtered by fastp (version 0.19.6) [30], and merged by FLASH (version 1.2.11) with the following criteria: (i) the 300 bp reads were truncated at any position receiving an average quality score of <20 over a 50 bp sliding window, and truncated reads shorter than 50 bp, and those reads containing ambiguous characters were discarded; (ii) only overlapping sequences >10 bp longer were assembled according to their overlapped sequence. The maximum mismatch ratio of overlap region was 0.2. Reads that could not be assembled were removed; and (iii) samples were distinguished according to the barcode and primers, and the sequence direction was adjusted, with exact barcode matching and 2 nucleotide mismatch in primer matching.
Operational taxonomic units (OTUs) were clustered with a similarity of 97% using UPARSE (version 11.0), and chimeric sequences were identified and excluded. The taxonomy of each OTU representative sequence was analyzed by RDP Classifier version 2.13 [31] against the 16S rRNA database (Silva v138) using a confidence threshold of 70%.

2.6. Calculations and Statistical Analysis

Data of DMI, ADG, rectal temperature, and concentrations of minerals in rumen fluid, serum, and feces, and fecal VFAs were analyzed using the SAS statistical package (version 9.4, SAS Inst. Inc., Cary, NC, USA). The model was: Yi = μ + SLj + eij, where Y = dependent variable, μ = treatment mean value, SLj = effect of Se level, and eij = residual error. Selenium levels were fixed effects. Significant differences among treatments were tested by one-way ANOVA using Duncan’s multiple comparisons test with each goat as an experimental unit. A p value < 0.05 was considered significant.
Pearson’s rank correlations tested the relationships between the relative abundances of fecal bacteria (at genus level > 0.05%) and concentrations of fecal VFAs and minerals using the “corrplot” package in R (Version 3.5.0).

3. Results

3.1. Dry Matter Intake, Average Daily Gain, and Rectal Temperature

The THI was above 72 between 12:00 and 16:00 (Table 2). Initial body weight, DMI, and rectal temperature did not differ (p > 0.05) among the three groups (Table 3). The final body weight (p = 0.012) and ADG (p < 0.01) increased linearly, whereas the DMI:ADG ratio decreased linearly (p < 0.01) with increasing dietary nano-Se levels. Linear regressions of FBW, ADG, and the ratio of DMI:ADG on supplemental nano-Se took the following forms:
FBW (kg) = 4.98 × nano-Se (mg/kg DM) + 22.2 (r2 = 0.16)
ADG (g/d) = 112.6 × nano-Se (mg/kg DM) + 88.9 (r2 = 0.66)
DMI: ADG = −10.9 × nano-Se (mg/kg DM) + 11.4 (r2 = 0.64).

3.2. Concentrations of Minerals in Rumen Fluid, Serum, and Feces

Rumen fluid concentrations of Se (p < 0.001) and Cu (p < 0.01) increased linearly, whereas of Ca (p = 0.028) decreased linearly with increasing dietary nano-Se levels (Table 4). Ruminal concentrations of P, Zn, Mn, and Fe did not differ (p > 0.05) among the three groups. Serum concentrations of Se (p < 0.001) and Fe (p = 0.019) increased linearly with increasing dietary nano-Se levels, whereas P, Cu, and Mn did not differ (p > 0.05) among the three groups. Fecal concentrations of Se (p < 0.001) increased linearly and of Cu (p < 0.01), Zn (p = 0.020), and Fe (p = 0.010) decreased linearly, whereas of P, Ca, and Mn did not differ (p > 0.05) among the three groups with increasing dietary levels of nano-Se. The linear regressions of Se in rumen fluid, serum, and feces on supplemental nano-Se took the following forms:
Se in rumen fluid (μg/L) = 80.7 × nano-Se (mg/kg DM) + 6.8 (r2 = 0.84)
Se in serum (μg/L) = 20.3 × nano-Se (mg/kg DM) + 70.6 (r2 = 0.19)
Se in feces (mg/kg) = 1.18 × nano-Se (mg/kg DM) + 0.42 (r2 = 0.87).

3.3. Concentrations of Fecal Volatile Fatty Acids

Concentrations of fecal total VFAs (p = 0.007), acetate (p = 0.011), propionate (p = 0.008), and butyrate (p = 0.001) decreased linearly, while the ratio of acetate:propionate increased linearly (p = 0.011) with increasing dietary nano-Se levels (Table 5). A linear regression of supplemental nano-Se on total VFAs took the following form:
total VFAs (mM) = 6.5 × nano-Se (mg/kg DM) + 21.2 (r2 = 0.42).

3.4. Summary of Collective Sequencing Data

There were 1,277,687 raw reads generated from the fecal samples, and 1,220,062 high quality sequences remained after quality–filtering and removal of chimeric sequences. There were 4494 OTUs based on 97% nucleotide sequence identity analysis among reads. Of these, 1710 OTUs were shared among the three treatment groups, which accounted for 59.7%, 58.9%, and 58.7% of the total OTUs in the 0.0, 0.2 and 0.4 mg nano-Se/kg DM groups, respectively (Figure 1), while the specific number of OTUs in these groups were 654, 673, and 690, respectively. The ACE, Chao, Shannon, Simpson, and Sobs indices of fecal bacteria did not differ among the three groups (Table 6).

3.5. Microbial Community Composition in Feces of Hainan Black Goats

There were 17 bacteria phyla identified in the feces of the Hainan black goats. The dominant phylum was Firmicutes, with relative abundances of 65.6%, 71.0%, and 71.7%, followed by Bacteroidetes, with 22.5%, 20.2%, and 16.7%, in the 0.0, 0.2, and 0.4 mg nano-Se/kg DM groups, respectively (Figure 2; Supplementary Table S1). The relative abundances of Firmicutes (p = 0.048) and Patescibacteria (p = 0.027) increased linearly, whereas of Bacteroidetes (p = 0.012), Fibrobacterota (p < 0.001) and Proteobacteria (p < 0.001) decreased linearly with increasing dietary nano-Se levels.
A total of 266 bacterial genera were identified in the feces of the 3 groups of goats. The dominant genus was unclassified_f_Lachnospiraceae, with 14.5%, 11.2%, and 10.0%, and the second most abundant genus was Ruminococcus, with 8.52%, 8.52%, and 8.73%, in the 0.0, 0.2, and 0.4 mg nano-Se/kg DM groups, respectively (Figure 3; Supplementary Table S2). The relative abundances of Treponema (p = 0.046), norank_f__norank_o__Clostridia_UCG-014 (p < 0.01), norank_ f_norank_o__RF39 (p < 0.01), Eubacterium_siraeum_group (p < 0.001), and Family_XIII_AD3011_group (p = 0.040) increased linearly, whereas of unclassified_f__Lachnospiraceae (p < 0.001), Rikenellaceae_RC9_gut_group (p < 0.01), Eubacterium_ruminantium_group (p = 0.021), and Prevotella (p < 0.001) decreased linearly with increasing dietary nano-Se levels. The relative abundance of norank_f__Eubacterium_coprostanoligenes_group was lesser (p = 0.014) in the 0.4 mg nano-Se/kg DM group than the other two groups.

3.6. Correlations Between Fecal Bacteria Abundances and Fecal Mineral Concentrations or Volatile Fatty Acids

There were 12 positive (p < 0.05) and 19 negative (p < 0.05) correlations between the relative abundances of bacterial genera and concentrations of fecal VFAs and minerals (Figure 4). Eubacterium_ruminantium_group was correlated negatively with the concentration of fecal Se, but positively with the concentrations of fecal acetate, propionate, butyrate, and Ca. Eubacterium_siraeum_group was correlated negatively with fecal concentrations of total VFAs, acetate, butyrate, Ca, and Zn, but positively with the fecal concentration of Se. Rikenellaceae_RC9_gut_group was correlated negatively with the fecal concentration of Se, but positively with fecal concentrations of butyrate, Cu, and Zn. Norank_f__norank_o__Clostridia_UCG-014 was correlated negatively with fecal concentrations of total VFAs, acetate, propionate, and butyrate, but positively with the fecal concentration of Se.

4. Discussion

4.1. Effect of Dietary Nano-Selenium Levels on Dry Matter Intake, Average Daily Gain, and Rectal Temperature

Over the past decades, climate has become a vital factor affecting animal husbandry. Numerous studies reported that growth performance and production efficiency declined in livestock in summer, but that supplementary Se improved ADG and the ratio of ADG to DMI in both heat and non-heat-stressed livestock [32,33,34]. In the current study, ADG increased with supplementary Se in the goats, which is in agreement with previous studies in goats [9] and chickens [33], and the ratio of DMI to ADG decreased. This occurred even though the DMI was similar among the three groups of goats, which would indicate that the Se either improved the digestibility of the diet and/or improved the efficiency of utilization of energy for growth [35].
The THI in the present study was above 72 at 12:00 and 16:00. A value greater than 72 was reported to heat-stress livestock, which would suggest that the goats were heat-stressed for 4 to 8 h each day [36]. Rectal temperature has been used as an indicator of heat stress and health of an animal [37]. In the present study, the rectal temperature did not differ among treatments and ranged between 38.9 and 39.3 °C, which is within the normal range of 38.3 to 40.0 °C reported for goats [38], suggesting that the goats were not heat-stressed. Hainan black goats are raised in southern China and are tolerant of heat [7,39], which could explain their normal rectal temperature under the climatic conditions of the study. In contrast, rectal temperature declined with supplementary Se in rabbit bucks [40]; differences between studies could be due to different responses among animal species, different environmental conditions, and/or different dietary compositions [12,37,40].

4.2. Effect of Dietary Nano-Selenium Levels on Concentrations of Minerals in Rumen Fluid, Serum, and Feces

The serum concentration of Se in the current study ranged between 69.6 and 77.7 μg/L, which was well below the toxic level of 1340 μg/L in goats [41]. The fecal concentration of Se in the 0.4 mg nano-Se/kg DM group was 0.89 mg/kg, which was two times greater than the concentration in the CON group. This high concentration could potentially pollute the environment and the soil; consequently, it is suggested to monitor fecal Se in livestock offered supplementary Se [42]. The accumulations of Se in serum and feces in the current study were consistent with data reported for piglets [43] and laying hens [29,44]; we are unaware of such measurements in other ruminants.
Serum concentrations of Ca, Zn, and Fe increased linearly with increasing nano-Se level, which is in agreement with Jin et al., who reported that the serum concentrations of Ca and Zn displayed an increasing trend, and Fe rose sharply in sheep receiving supplementary Se [45]. This would indicate that Se enhanced the ruminal absorption of these minerals [46]. Serum concentrations of Ca, P, Zn, and Cu were reported to range from 20 to 28 mg/L, 13 to 22 mg/L, 5.4 to 9.9 mg/L, and 7.9 to 9.3 mg/L, respectively, in small East African goats in a semiarid area of Tanzania [42]. None of the values in the present study fell within these ranges, which would suggest differences in mineral intakes or metabolism between breeds.
The annual manure production from livestock in China totals approximately 3.8 × 109 tons. Goat manure is high in nutrient and organic contents, and could improve soil fertility [47]. However, the heavy metals, including Cu, Fe, and Zn, are the main limiting factors in the use of goat manure for fertilization, as they could pose a threat to human health by contaminating agricultural products, and have attracted increasing concern for food safety and health issues [48,49]. In the present study, fecal concentrations of Cu, Zn, and Fe decreased with increasing supplementary Se intake, which was in agreement with previous studies [50,51]. The decrease in mineral excretion in feces was likely a result of their increased ruminal absorption due to supplementary nano-Se, as discussed above.

4.3. Effect of Dietary Nano-Selenium Levels on Volatile Fatty Acids (VFAs) Concentrations

VFAs are the main products of bacterial degradation of carbohydrates and proteins in the gut and are either absorbed by the gut epithelium or excreted in feces. In the present study, concentrations of total fecal VFAs, acetate, propionate, and butyrate decreased with increasing dietary Se intake, whereas, in poultry, concentrations of fecal VFAs did not differ with different Se dietary intakes [52]. This difference between studies could be due to response differences among animal species. In addition, Sun et al. reported that Se improved the yield and absorption of VFAs in lactating dairy cows, which would indicate a decrease in fecal VFAs [53].

4.4. Effect of Dietary Nano-Selenium Levels on Fecal Microbial Composition in the Feces

Firmicutes and Bacteroidetes were the dominant bacteria phyla, which is in agreement with previous studies in goats [54], sheep [55], and cattle [19]. In the present study, the relative abundance of Firmicutes increased and that of Bacteroidetes decreased with supplementary Se. Firmicutes degrade cellulose, hemicellulose, starch, and oligosaccharides, while Bacteroidetes degrade carbohydrates and are involved in protein hydrolysis and immune regulation [5]. Fecal fiber concentrations were greater in the CON group than the groups with supplementary Se, which could be explained by the increased relative abundance of Firmicutes and decreased relative abundance of Bacteroidetes with an increase in dietary Se. In addition, Fibrobacteres, an important cellulose-degrading phylum [56], decreased with an increase in dietary Se, which could explain the decreased fecal concentrations of NDF (45.4% vs. 43.9% vs. 44.7%) and ADF (14.9% vs. 14.4% vs. 12.3% in 0.0, 0.2, and 0.4 mg nano-Se/kg DM, respectively; unpublished data) with an increase in dietary Se intake. The relative abundance of fecal Proteobacteria, bacteria that degrade mainly proteins [57], decreased in the Hainan black goats with an increase in supplementary Se. Proteobacteria was reported to be associated with dysbiosis in hosts with metabolic or inflammatory disorders [58], which would suggest fewer metabolic or inflammatory disorders in goats with supplementary Se.
At the genus level, the most dominant fecal bacteria was unclassified_f__Lachnospiraceae, followed by Ruminococcus and Treponema. However, previous studies reported that the most abundant genera were Ruminococcaceae UCG-005 and Christensenellaceae R-7 group in goats [59,60]. These differences among studies could have resulted from differences due to goat breeds, diet, and/or environmental conditions [61,62]. In addition, it was reported that the relative abundance of Lachnospiraceae, which synthesizes VFAs, especially butyrate, and alleviates stress, was high in the gut in the rat [63]. In the present study, the relative abundance of unclassified_f__Lachnospiraceae decreased with supplementary Se and correlated positively with the concentration of fecal butyrate and negatively with the concentration of fecal Se.
Fecal fibrolytic bacteria, such as unclassified_f__Lachnospiraceae [64], Rikenellaceae_RC9_gut_group [18], and Eubacterium_ruminantium_group [61,62], decreased with supplementary nano-Se. A previous study reported that Se increased the digestibility of fibers in the total tract, that is, it reduced the fiber content in feces [65]. Hence, the relative abundances of fibrolytic bacteria were lesser in nano-Se groups than in the CON group. Prevotella is a vital enterotype associated with high production of total VFAs. In the present study, the relative abundance of Prevotella was greatest in the CON group and lowest in the 0.4 mg nano-Se/kg DM group, which is in accordance with the total concentration of fecal VFAs. Treponema contains both pathogenic and nonpathogenic bacteria species and has disclosed a strict growth dependence on Se [66]. In the present study, fecal Se concentration increased linearly with an increase in dietary Se, which resulted in a linear increase in the relative abundance of Treponema. Eubacterium_siraeum_group is considered beneficial to the health of their host [67], and in the current study, their relative abundance increased linearly with increasing dietary Se. A previous study reported that norank_f__norank_o__RF39 can influence the host’s immune system and increase the body’s immune defense function [68]. The relative abundance of norank_f__norank_o__RF39 increased linearly with increasing Se intake n the present study, indicating that Se improved the immune system of the goats.

4.5. Effect of Dietary Nano-Selenium Levels on Correlations Between Fecal Bacteria and Concentrations of Fecal Minerals and Short-Chain Fatty Acids

It was reported that Se and air temperature affect gastrointestinal bacteria [51,69]. We are unaware of studies that have examined the correlation between fecal bacteria and fecal mineral concentrations in goats. Eubacterium_ruminantium_group, a fibrolytic bacteria, was correlated positively with acetate in the present study, which is in agreement with a previous study [61]. Ruminococcus_2 was reported to be correlated positively with the digestibility of dietary P in the goat jejunum [32], which could explain the lower fecal P output with a greater relative abundance of Rumincoccus 2 and the negative correlation between Ruminococcus and fecal P concentration. It was reported that bacterial communities in the gastrointestinal tract could affect the total absorption of Ca in goats [70,71]. In the present study, norank_f_norank_o_RF39 and Enbacterium_siraeum_group were correlated negatively, whereas Enbacterium_ruminantium_group was correlated positively with fecal Ca concentrations. Christensenellaceae R-7 plays a role in fiber digestion; however, the relative abundance of this genus did not change with supplementary Se in goats [72]. In addition, there was no correlation between Christensenellaceae R-7 and the concentrations of fecal VFAs and minerals in the present study.

5. Conclusions

The ADG increased and the DMI:ADG ratio decreased, whereas the fecal concentrations of total VFAs, acetate, propionate, butyrate, Cu, Zn, and Fe decreased with supplementary nano-Se. In addition, fecal bacteria were altered with supplementary Se. We concluded that nano-Se altered the bacterial community in feedlot Hainan black goats, which affected growth performance and concentrations of serum and fecal minerals and fecal VFAs. We recommend a dietary supplementation of approximately 0.4 mg nano-Se/kg DM for feedlot Hainan black goats, but further research is warranted to determine the precise dose and the possible contamination risks of Se.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/agriculture14122233/s1, Table S1: Effect of dietary supplementation of different levels of nano-selenium on fecal bacteria (at phylum level, >0.1% of total reads) in Hainan black goats; Table S2: Effect of dietary supplementation of different levels of nano-selenium on fecal bacteria (at genus level, >0.05% total reads) in Hainan Black goats.

Author Contributions

Conceptualization, H.L. and G.Z.; methodology, K.M., W.P., Y.Y., Q.W. and G.Z.; software, H.L. and G.Z.; validation, H.Z., J.H., and Q.J.; formal analysis, H.L.; investigation, K.M., W.P., Y.Y., Q.W., G.Z., Q.J. and K.W.; resources, G.Z. and J.H.; data curation, H.L.; writing—original draft preparation, H.L.; writing—review and editing, A.D. and H.Z.; visualization, H.L. and K.M.; supervision, J.H.; project administration, H.Z.; funding acquisition, H.L., Y.Y., W.P. and H.Z. All authors have read and agreed to the published version of the manuscript.

Funding

The present work was jointly supported by the Central Public-interest Scientific Institution Basal Research Fund (no. 1630102024014), Special Research Project of Zhanjiang Experimental Station, Chinese Academy of Tropical Agricultural Sciences (no. ZJSYZ2024002) Hainan Provincial Natural Science Foundation of China (no. 324QN301), National Natural Science Foundation of China (U23A20228), and Special Fund for Agricultural Product Quality and Safety of Ministry of Agriculture and Rural Affairs of China: “Evaluation and Analysis of Quality and Safety of Tropical and Subtropical New Feed Resources” (08240054; 16230077).

Institutional Review Board Statement

The animal study protocol was approved by the Animal Care Committee of Zhanjiang Experimental Station, Chinese Academy of Tropical Agricultural Sciences (protocol number: CATAS-20230601ZES).

Data Availability Statement

The data used are confidential and will be made available on request.

Conflicts of Interest

No conflicts of interest exist in the submission of this manuscript, and the manuscript has been approved by all authors for publication. Author Gang Zuo is/was employed by Beijing Deyuanshun Biotechnology 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 potential conflicts of interest.

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Figure 1. Different and similar OTUs in feces of Hainan black goats offered different levels of supplementary nano-selenium (nano-Se).
Figure 1. Different and similar OTUs in feces of Hainan black goats offered different levels of supplementary nano-selenium (nano-Se).
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Figure 2. Relative abundances of bacterial phyla (>0.1% of total reads) in feces of Hainan black goats offered different dietary nano-selenium levels.
Figure 2. Relative abundances of bacterial phyla (>0.1% of total reads) in feces of Hainan black goats offered different dietary nano-selenium levels.
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Figure 3. Bacterial composition at genus level (>0.05% total reads) in feces in Hainan black goats offered diets with different nano-selenium levels.
Figure 3. Bacterial composition at genus level (>0.05% total reads) in feces in Hainan black goats offered diets with different nano-selenium levels.
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Figure 4. Correlations between relative abundances of fecal bacteria at genus level and fecal concentrations of minerals or volatile fatty acids. Se = selenium; P = phosphorus; Ca = calcium; Cu = copper; Zn = zinc; Mn = manganese; Fe = iron. * p < 0.05; ** p < 0.01.
Figure 4. Correlations between relative abundances of fecal bacteria at genus level and fecal concentrations of minerals or volatile fatty acids. Se = selenium; P = phosphorus; Ca = calcium; Cu = copper; Zn = zinc; Mn = manganese; Fe = iron. * p < 0.05; ** p < 0.01.
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Table 1. Ingredients and chemical composition of the diet offered to the Hainan black goats.
Table 1. Ingredients and chemical composition of the diet offered to the Hainan black goats.
ItemsContent
Ingredients, g/kg of DM
Corn stalk500
Corn grain, ground150
Wheat bran50.0
Soybean meal130
DDGS41.5
Barley grain80.0
NaHCO310.0
Limestone12.0
CaHPO49.50
NaCl5.00
Urea2.00
Premix 110.0
Chemical composition
Dry matter, g/kg920
Crude protein, g/kg140
Neutral detergent fiber, g/kg398
Acid detergent fiber, g/kg202
Ether extract, g/kg50.0
Calcium, g/kg7.58
Phosphorus, g/kg3.19
Selenium, mg/kg0.37
Zinc, mg/kg109
Copper, mg/kg37.9
Manganese, mg/kg349
Iron, g/kg4.71
ME, MJ/kg7.60
DDGS = distillers dried grains with solubles; ME = metabolizable energy. 1 The premix provided the following items per kg: vitamin A 12,000 IU, vitamin E 30 IU, vitamin D 2000 IU, Cu 12.0 mg, Fe 64.0 mg, Mn 56.0 mg, Zn 60.0 mg, I 1.20 mg, Se 0.35 mg, Co 0.40 mg.
Table 2. The average temperature humidity index (THI) in the experimental period.
Table 2. The average temperature humidity index (THI) in the experimental period.
Time08:0010:0012:0014:0016:0018:00
Average THI70.2271.7472.6072.7072.1171.28
Table 3. Effect of dietary supplementation of different levels of nano-selenium (nano-Se) on feed intake, average daily gain, and rectal temperature in Hainan black goats.
Table 3. Effect of dietary supplementation of different levels of nano-selenium (nano-Se) on feed intake, average daily gain, and rectal temperature in Hainan black goats.
ItemsNano-Se, mg/kg DMISEMp-Values
0.00.20.4Nano-SeL
Initial body weight, kg18.618.418.70.690.9730.881
Final body weight, kg22.3 a23.1 a,b24.3 b0.750.0250.012
Dry matter intake, kg/d1.001.051.000.1130.8650.954
Average daily gain, g/d88.1 a113 b132 c7.390.013<0.01
DMI: ADG11.4 c9.26 b7.54 a0.7520.012<0.01
Rectal temperatures, °C39.039.138.90.0110.4440.464
DMI: ADG = ratio of dry matter intake to average daily gain; SEM = standard error of the means among 3 groups; Se = selenium; L = linear regression of variable measured on nano-Se level. Means within a row with different superscripts differ from each other (p < 0.05).
Table 4. Effect of dietary supplementation of different levels of nano-selenium (nano-Se) on mineral concentrations in rumen fluid, serum, and feces in Hainan black goats.
Table 4. Effect of dietary supplementation of different levels of nano-selenium (nano-Se) on mineral concentrations in rumen fluid, serum, and feces in Hainan black goats.
ItemsNano-Se, mg/kgSEMp-Values
0.00.20.4Nano-SeL
Rumen fluidP, g/L1.801.941.750.1220.4620.830
Se, μg/L9.31 a17.9 b41.6 c0.31<0.001<0.001
Ca, mg/L1418 b1241 a1295 a33.90.0120.028
Cu, mg/L2.74 a2.75 a3.39 b0.123<0.01<0.01
Zn, mg/L11.611.711.40.510.9180.766
Mn, mg/L24.022.422.80.720.3140.252
Fe, mg/L25623324411.50.3980.469
SerumP, mg/L1251181263.60.2840.840
Se, μg/L69.6 a76.6 b77.7 b2.790.0400.025
Ca, mg/L812 a968 b820 a38.9<0.010.083
Cu, mg/L2.682.993.050.1220.0770.074
Zn, mg/L7.38 a8.87 c7.95 b0.251<0.010.076
Mn, mg/L0.270.320.290.0150.0750.210
Fe, mg/L32.2 a32.7 a37.8 b1.390.0310.019
FecesP, g/kg5.645.405.650.4470.9050.982
Se, mg/kg0.42 a0.66 b0.89 c0.037<0.001<0.001
Ca, g/kg33.532.931.70.7800.1900.079
Cu, mg/kg76.8 c70.0 a68.1 a1.66<0.01<0.01
Zn, mg/kg241 b227 a220 a5.900.0450.020
Mn, mg/kg73174371519.70.6190.572
Fe, g/kg11.4 b11.1 b10.9 a0.1350.0300.010
SEM = standard error of the means; Se = selenium; P = phosphorus; Ca = calcium; Cu = copper; Zn = zinc; Mn = manganese; Fe = iron. L = linear regression of variable measured on nano-Se level. Means within a row with different superscripts differ from each other (p < 0.05).
Table 5. Effect of dietary supplementation of different levels of nano-selenium (nano-Se) on fecal concentrations of volatile fatty acids in Hainan black goats.
Table 5. Effect of dietary supplementation of different levels of nano-selenium (nano-Se) on fecal concentrations of volatile fatty acids in Hainan black goats.
ItemsNano-Se, mg/kgSEMp-Values
0.00.20.4Nano-SeL
Total VFAs, mM21.0 b20.1 b18.4 a0.550.0200.007
Acetate, mM15.0 b14.8 b13.8 a0.270.0210.011
Propionate, mM2.96 b2.73 b2.41 a0.1390.0250.008
Butyrate, mM2.32 c1.83 b1.44 a0.1310.0020.001
Iso-VFA, mM0.770.710.780.0460.4110.797
Acetate: propionate5.08 a5.42 b5.73 c0.1370.0330.011
SEM = standard error of the means; Se = selenium; SCFA = short-chain fatty acids. L = linear regression of variable measured on nano-Se level. Means within a row with different superscripts differ from each other (p < 0.05).
Table 6. The alpha diversity of fecal bacteria in response to different supplementary dietary nano-selenium (nano-Se) levels in Hainan black goats.
Table 6. The alpha diversity of fecal bacteria in response to different supplementary dietary nano-selenium (nano-Se) levels in Hainan black goats.
ItemsNano-Se, mg/kg DMSEMp-Values
0.00.20.4Nano-SeL
Ace14851546148455.80.6740.994
Chao14341483143852.50.7680.954
Shannon5.055.145.140.0700.5920.393
Simpson0.020.020.020.0030.4810.302
Sobs12741305127447.90.8690.996
SEM = standard error of the means; Se = selenium. L = linear regression of variable measured on nano-Se level.
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MDPI and ACS Style

Liu, H.; Mao, K.; Peng, W.; Degen, A.; Zuo, G.; Yang, Y.; Han, J.; Wu, Q.; Wang, K.; Jiang, Q.; et al. Nano-Selenium Reduces Concentrations of Fecal Minerals by Altering Bacteria Composition in Feedlot Goats. Agriculture 2024, 14, 2233. https://doi.org/10.3390/agriculture14122233

AMA Style

Liu H, Mao K, Peng W, Degen A, Zuo G, Yang Y, Han J, Wu Q, Wang K, Jiang Q, et al. Nano-Selenium Reduces Concentrations of Fecal Minerals by Altering Bacteria Composition in Feedlot Goats. Agriculture. 2024; 14(12):2233. https://doi.org/10.3390/agriculture14122233

Chicago/Turabian Style

Liu, Hu, Kaiyu Mao, Weishi Peng, Allan Degen, Gang Zuo, Yuanting Yang, Jiancheng Han, Qun Wu, Ke Wang, Qinyang Jiang, and et al. 2024. "Nano-Selenium Reduces Concentrations of Fecal Minerals by Altering Bacteria Composition in Feedlot Goats" Agriculture 14, no. 12: 2233. https://doi.org/10.3390/agriculture14122233

APA Style

Liu, H., Mao, K., Peng, W., Degen, A., Zuo, G., Yang, Y., Han, J., Wu, Q., Wang, K., Jiang, Q., & Zhou, H. (2024). Nano-Selenium Reduces Concentrations of Fecal Minerals by Altering Bacteria Composition in Feedlot Goats. Agriculture, 14(12), 2233. https://doi.org/10.3390/agriculture14122233

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