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. 2022 Jul 14;3(5):334–338. doi: 10.3168/jdsc.2022-0238

Effect of zinc source (zinc sulfate or zinc hydroxychloride) on relative abundance of fecal Treponema spp. in lactating dairy cows

BA Wenner 1,*,†, T Park 2, K Mitchell 1, SK Kvidera 3,*, KE Griswold 3, EA Horst 4, LH Baumgard 4
PMCID: PMC9623701  PMID: 36340900

Graphical Abstract

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Summary: The present study describes the difference in fecal microbiome between cows fed supplemental zinc either in a sulfate or hydroxychloride form. Supplemental zinc hydroxychloride under ad libitum feeding conditions decreased Treponema spp., particularly those sequences within Treponema 2, by 67% compared with a similar diet with zinc sulfate, whereas other changes in the fecal microbiome were minimal. The shift in Treponema spp. from zinc source could reflect a fecal microbiome response to zinc availability, but it is unknown if that shift reflects a pathogenic risk to the ruminant.

Highlights

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    Cows (n = 24) were fed typical lactating diets that only differed in zinc source inclusion.

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    Fecal samples collected from cows were extracted for prokaryotic 16S gene DNA.

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    Feeding zinc hydroxychloride decreased the Treponema spp. recovered from fecal samples compared with cows fed zinc sulfate.

Abstract

Previous research revealed a potential effect of dietary trace mineral source on both ruminal and fecal microbiota. However, the effect of Zn source, specifically, has not previously been considered. Based on reported postruminal solubility, we hypothesized that Zn hydroxychloride would decrease Treponema spp. fecal excretion relative to cows fed Zn sulfate. To test this hypothesis, lactating Holstein cows (n = 24; 685 ± 9 kg of body weight; 159 ± 8 d in milk; parity 3 ± 0.2) were randomly assigned to 1 of 2 dietary treatments: control (75 mg/kg Zn from ZnSO4) or Zn hydroxychloride (HYD; 75 mg/kg IntelliBond Z; Micronutrients USA LLC). Single fecal grab samples were collected on d 1 before dietary treatments and on d 27 after dietary treatments were applied. Fecal microbial DNA was extracted and sequenced to establish taxonomy using a universal primer for the 16S rRNA gene. Supplementation of HYD decreased the relative abundance of Treponema 2 by 3-fold (14.7% vs. 4.9%). Poor sequencing resolution at the species level limited inference of Treponema spp. toward management or gut health implications of HYD supplementation. However, the inclusion of pathogenic species among Treponema spp. indicates a potential implication of HYD feeding to reduce environmental exposure of the dairy cow to Treponema spp.

Since the 1960s, Zn has been recognized as an essential micromineral in dairy cattle nutrition. More recently, the Zn source has been shown to have broader effects on animal health and metabolism beyond variation in bioavailability or cost (Weiss, 2017). Ionic salts such as ZnSO4 are highly soluble and dissociate into elemental zinc (Zn2+) and sulfate (SO42−) ions quickly in an aqueous environment such as the rumen. In contrast, trace mineral sources with strong covalent bonds such as hydroxychloride trace minerals may prevent the metal from being released early and rapidly in the digestive tract (Goff, 2018).

Zinc-amino acid chelates have specifically been shown to shift rumen microbiomes compared with ZnSO4 (Ishaq et al., 2019), whereas hydroxychloride trace minerals have been shown to positively affect fiber digestibility in both cows (Faulkner and Weiss, 2017; Miller et al., 2020) and sheep (VanValin et al., 2018). Both Zn-AA chelates and Zn hydroxychloride can have improved intestinal bioavailability compared with inorganic sources (Schlegel and Windisch, 2006; Shaeffer et al., 2017); this improved bioavailability may be due to the ability of covalently bonded Zn to avoid antagonistic reactions, resulting in less mineral binding to digesta contrasting with sulfate trace minerals (Caldera et al., 2019). More mineral availability throughout the lower digestive tract (Klasing and Naziripour, 2010) may positively or negatively affect microbial populations within the lower gut of cattle but remains to be fully investigated.

Given the role of Zn in Treponema metabolism (Hazlett et al., 2003) and the potential implication of Treponema spp. in bovine digital dermatitis (Klitgaard et al., 2014; Moreira et al., 2018), our objective in the present study was to evaluate the effect of Zn source on fecal microbiota relative abundance. Based on a single study comparing glycinate mineral sources versus sulfates and their effect on fecal Treponema (Faulkner et al., 2017), we hypothesized that Zn hydroxychloride would shift the fecal microbiome away from Treponema spp. when replacing supplemental ZnSO4.

All animal procedures were approved by the Iowa State University Institutional Animal Care and Use Committee as described previously in a companion study (Horst et al., 2020). Briefly, lactating Holstein cows (n = 24; 685 ± 9 kg of BW; 159 ± 8 DIM; parity 3 ± 0.2) were fed in an experiment consisting of 2 replications (n = 12/replicate). Cows were randomly assigned to 1 of 2 dietary treatments: (1) control (CON; 75 mg/kg Zn from ZnSO4; n = 12) or (2) Zn hydroxychloride (HYD; 75 mg/kg IntelliBond Z; Micronutrients USA LLC; n = 12). At the start of the study (d 0) cows were fed their respective treatment diets for 21 d. After the initial feeding phase, cows were moved to individual box stalls (4.57 × 4.57 m) for metabolic measurements relevant to the previous study (Horst et al., 2020). Cows were allowed 3 d to acclimate to housing conditions, then maintained in box stalls on their present diet ad libitum.

Throughout the experiment, all cows were fed a TMR formulated to meet or exceed the predicted requirements for energy, protein, minerals, and vitamins (NRC, 2001). While the diet is described in greater detail in Horst et al. (2020), it consisted of 30.3% corn silage, 23.5% alfalfa hay, 18.8% ground corn, 10.3% corn gluten pellets, 6.0% soybean meal (treated and untreated), 3.4% whole cottonseed, and 7.7% premix. Analysis of TMR and diet details are also available in the previously published study (Horst et al., 2020). Briefly, the control diet was 32.5% NDF, 16.2% CP, 24.6% starch, and 53.8% forage. Dietary Zn was 92.4 and 92.5 mg/kg, including 17.4 and 17.5 mg/kg baseline Zn within the diet for CON and HYD, respectively. Feed was provided once daily for all cows (0800 h) and feed intake averaged 26.5 kg/d (Horst et al., 2020).

On d 1 (pre-treatment) and d 27, a single fecal grab sample was obtained directly from each cow following the morning milking (0600 h) and before feeding. Individual grab samples were subsampled into 15-mL RNAase- and DNase-free conical tubes, then stored at −80°C within 1 h of sample collection until being shipped for analysis. Fecal DNA was extracted using the repeated bead beating and column method (Yu and Morrison, 2004) and DNA purified using Qiagen (Thermo Fisher Scientific Inc.) mini-stool kits. Researchers performing extractions were blind to treatment at the time of extraction and taxonomy assignation. Samples were compared with a 1 kb ladder for quality control and to assess DNA fragment length.

Amplicon libraries were prepared targeting the V4–V5 hypervariable region of the 16S rRNA gene using 515F (5′-GAGTGCCAGCMGCCGCGGTAA-3′) and 806R (5′-ACGGACTACHVGGGTWTCTAAT-3′) universal primers (Caporaso et al., 2011) with each library having a unique barcode for multiplexing at the Molecular and Cellular Imaging Center (The Ohio State University). Amplicon libraries were pooled and sequenced (2 × 300 bp paired-end sequencing) using the MiSeq platform (Illumina Inc.). Quality control (denoising, merging, removal of chimeras) was applied through QIIME2 (version 2019.10; Bolyen et al., 2019), similarly to Lee et al. (2021). The final quantity of quality amplicon sequencing variants (ASV) used in this analysis numbered 3,855,702 and were clustered into taxonomy based on 99% similarity using the Silva 16S reference database (NR 132 version; Quast et al., 2013).

Phyla, families, and genera present in at least 5 samples at a relative abundance of ASV greater than or equal to 0.5% were included in analysis. Alpha diversity indices were derived from rarified ASV (21,069 ASV per sample) including richness, Chao1, Shannon's index, Pielou's evenness, Good's coverage, and Faith's phylogenetic diversity. Phylogenetic investigation of communities by the reconstruction of unobserved studies (PICRUSt2; Douglas et al., 2020) was used to predict microbial metabolic functions from 16S ASV. Kyoto Encyclopedia of Genes and Genomes (KEGG) modules were reconstructed from predicted KEGG ortholog profiles in PICRUSt2 and represent microbial metabolic functions.

Microbial relative abundance data were analyzed using samples taken on d 1 as a covariate. The relative abundance data were not transformed because previous transformations of relative abundance were not effective in improving distribution normality (Faulkner et al., 2017). Using R project, relative abundances and predicted KEGG ortholog pathways were compared using the model where Yij is the dependent variable, µ is the overall population mean, Ni is the fixed effect of ith mineral treatment (i = CON, HYD), b represents the covariate of baseline relative abundance during the adaptation period, and εij is the residual error, assumed independent and normal. Sequencing data are available upon request from the corresponding author. A Kenward-Roger degrees of freedom correction was applied to protect against type 1 error. Alpha diversity measures were compared using the same model except without the covariate adjustment for the pre-treatment sampling. Beta diversity was visualized using principal coordinate analysis based on comparisons using Bray-Curtis distance matrices via the emperor plugin (Vázquez-Baeza et al., 2013) implemented within QIIME2. The microbial community differences were statistically analyzed using PERMANOVA test implemented in QIIME2.

A general description of the community recovered from the fecal samples at the phyla level is summarized in Figure 1. The top 97.2% of ASV relative abundance on average was dominated by Firmicutes (48.4%), Bacteroidetes (37.7%), Spirochaetes (7.7%), and Actinobacteria (3.3%). Whereas Firmicutes and Bacteroidetes dominated the microbial community, Bacteroidetes were proportionally lower than expected from previous work (Faulkner et al., 2017), where they were reported at 45.8% and 42.1%, respectively, but is more in line with the greater ratio of Firmicutes:Bacteroidetes recently seen in other cow studies (Huang et al., 2020; Li et al., 2020) evaluating fecal microbiota. Recovery of sequences within Spirochaetes was nearly 6-fold greater in the present study than previously reported (Faulkner et al., 2017; Huang et al., 2020); thus, it may be reasonable to scale inferred expected changes in Spirochaetes. There were no differences in α-diversity measures between CON and HYD (P ≥ 0.11, Table 1) nor in β-diversity assessed by Bray-Curtis (P = 0.11).

Figure 1.

Figure 1

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Average (across treatments) fecal microbial phyla relative abundance for all phyla in excess of 0.5% relative abundance from lactating dairy cows fed either 75 mg/kg supplemental ZnSO4 or 75 mg/kg supplemental Zn hydroxychloride.

Table 1.

Relative abundance of 16S rRNA gene sequences for recovered Treponema spp. and diversity indices for fecal microbiome sequences of cows fed either Zn sulfate or Zn hydroxychloride

Amplicon sequencing variant CON1 HYD SE P-value2
Treponema 14.7 4.9 3.1 0.05
Treponema 2 14.1 4.6 3.0 0.05
Treponema porcinum 0.354 0.043 0.103 0.06
Uncultured Treponema 0.185 0.312 0.056 0.13
Gut metagenome Treponema 0.009 0.017 0.005 0.24
Diversity metric
 Richness 567 700 66 0.16
 Chao1 573 714 67 0.16
 Shannon's diversity 7.50 7.96 0.21 0.13
 Inverse Simpson 16.3 19.5 1.3 0.11
 Pielou's evenness 0.826 0.848 0.016 0.33
 Good's coverage 0.999 0.999 0.0004 0.25
 Faith's phylogenetic diversity 30.8 34.7 1.7 0.12
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1

Treatments consisted of either 75 mg/kg supplemental ZnSO4 (CON) or 75 mg/kg supplemental Zn hydroxychloride (HYD).

2

P-values reported for the effects of HYD.

The only genus within Spirochaetes with relative abundance greater than 0.5% was Treponema 2. With the exception of uncultured Barnesiellaceae (average 0.45% relative abundance, P = 0.03, data not shown), Treponema 2 was the only genus significantly affected by Zn source. Relative abundance of Treponema 2 was decreased 3-fold in cows fed HYD (P = 0.05; Table 1). Although most other prokaryotic genera remained static, the dramatic shift in Treponema 2 supports our hypothesis that a shift in Zn source would decrease Treponema spp. within the fecal microbiome. The only other previous study to quantify a fecal microbial response to mineral source, Faulkner et al. (2017) found that a shift from sulfate to glycinate-based Cu, Mn, and Zn did not significantly decrease Treponema recovered from feces. However, a shift in Zn source only from sulfate to glycinate source did decrease Treponema spp. by 4-fold.

In vitro dosing of ZnSO4 by Martinez and Church (1970), as well as Eryavuz and Dehority (2009), demonstrated that rumen microbes are sensitive to high concentrations of Zn, whereas Zinicola et al. (2015) reported the rumen as a downstream contributor of Treponema to the lower digestive tract of cows and ultimately to the fecal slurry. Given the demonstrated effect of mineral source on NDF digestibility (Faulkner and Weiss, 2017), it is possible that the fecal microbiome response measured in our current study could be a response to a shift in nutrient outflow exiting the rumen, especially as Treponema spp. are known fiber degraders. A less soluble Zn source within the rumen could have increased ruminal fiber digestibility and therefore decreased opportunity for a niche fiber degrader such as Treponema spp. (Bekele et al., 2011) within the lower digestive tract. However, ruminal digestibility of NDF was not reported in Horst et al. (2020). Further, a recent study found most microbiome effects within the rumen were undetectable within the fecal microbiome (Noel et al., 2019); thus, we expect the effect of Zn source to be localized to conditions within the lower digestive tract rather than a result of microbial flow from the rumen. We consider a rumen outflow effect unlikely due to the lack of variation among 47 other leading genera recovered from the fecal samples, including other cellulolytics.

Little is known about microbial sensitivity to mineral source within the lower gastrointestinal tract, particularly in ruminants where rumen interactions can confound mineral availability in the lower digestive tract. Given the difference in source between the current study (Zn hydroxychloride) and previous work using glycinate minerals (Faulkner et al., 2017), it is also possible that a competitive response of Treponema to sulfate sources—a common control in both studies—or their insoluble mineral complexes postabomasum, or both, better describes the similarities with 2 alternative mineral sources decreasing Treponema spp. relative abundance compared with compared with sulfate mineral sources. It has been known for some time that Zn is required by Treponema spp. (Hazlett et al., 2003) and other pathogenic members of Spirochaetes, such as Borellia burgdorferi (Boylan et al., 2003). Although it could be argued that a more intestinally bioavailable Zn source would also favor the microbes inhabiting the lower digestive tract, it is more likely that Treponema spp. hold a competitive advantage within the lower digestive tract where insoluble Zn complexes are poorly available except to those microbes capable of scavenging mineral complexes. However, in the present study, data on absorption of Zn are unavailable and it is possible that both diets passed enough Zn to the lower digestive tract that solubility was a moot issue. We propose that when a greater proportion of Zn within digesta is bound in insoluble complexes, less is absorbed within the small intestine, and a greater opportunity exists for Treponema spp. to uptake Zn to meet their requirement within the large intestine.

Radolf et al. (2016) note heavy reliance on Fe within Treponema pallidum, a known human pathogen, that correlates to PICRUSt2 data in the present study, indicating a 50% reduction in Fe(III) transport pathway predictions (KEGG M00190, P = 0.04, data not shown). A decrease in relative abundance of iron transport systems in HYD might alter the gut microbial composition toward less pathogenic bacterial populations residing in the gut (Lee et al., 2008; Zimmermann et al., 2010). Additionally, the inhibition of Borrelia burgdorferi (a spirochete implicated in Lyme disease) by high Mn that was experimentally countered with increasing Zn dosage (Troxell et al., 2013) is further evidence toward a hypothesis that mineral availability (either to the cow or lack thereof) could influence the prevalence of Treponema spp. within the lower intestinal tract. Genome studies in Treponema pallidum, a pathogenic Treponema known for syphilis, indicate a requirement for Zn (Hazlett et al., 2003; Houston et al., 2012; Radolf et al., 2016) linked to specific transporters and transcription activators. This requirement for related species makes it increasingly unlikely that Treponema spp. in the present study decreased in the lower digestive tract as a response to purported increased Zn availability from chelated or hydroxychloride mineral sources. Ultimately, whether or not the prevalence of Treponema spp. is responding to increased availability of a Zn source for absorption in the small intestine or responding to a decreased concentration of insoluble Zn was not directly addressed within this study.

High-throughput 16S sequencing approaches with a universal primer have limited resolution at the species level, including the present fecal microbiome data. In the present study, there were only 4 Treponema species-level ASV identified and their proportions relative to total Treponema spp. are presented in Table 1. The only significant decrease in Treponema was for those sequences within unresolved sequences of Treponema 2 (P = 0.05). Although no sequences were specifically identified that matched pathogenic strains of Treponema, more than 20 species are contained within Treponema 2 including potential pathogens (Edwards et al., 2020). Thus, although not a sole causative factor for bovine digital dermatitis (Klitgaard et al., 2017), the potential hoof health benefit of decreased Treponema spp. fecal excretion cannot be ruled out. Treponema spp. within manure slurry may pose a likely indictment for bovine digital dermatitis (Klitgaard et al., 2014; Zinicola et al., 2015) but more recent papers cast doubt on whether fecally excreted Treponema spp. are a causative agent for bovine digital dermatitis (Klitgaard et al., 2017; Moreira et al., 2018) or just guilty by association. The exposure of the foot to microbes within manure slurry and evidence of mineral-related response of the fecal microbiome leads to questions on the potential role of bacteria shed in feces toward foot lesion development.

Our data demonstrate a clear linkage between a supplemental Zn source with limited rumen availability and decreased fecal populations of Treponema spp. The lack of specific opportunistic pathogen sequence recovery within the current study limits inference on the impact these changes may play in development of bovine digital dermatitis. However, the reduction in Treponema highlights the systemic influence of a mineral source bioavailability on microbial populations in the lower digestive tract, regardless of animal health implications. More specific research needs to be conducted to consider the potential effect of sulfates on the fecal microbiome to isolate Zn bioavailability from other chemical mechanisms of influence on fecal populations.

Notes

This project was funded by Micronutrients USA LLC (Indianapolis, IN). We are additionally grateful to L. Moraes, formerly within the Department of Animal Sciences at The Ohio State University, for his advice on statistical analysis.

K. E. Griswold is an employee of the funding source for this work. The authors have not stated any other conflicts of interest.

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