Abstract
Male fertility is extremely important in dairy animals because semen from a single bull is used to inseminate several thousand females. Asthenozoospermia (reduced sperm motility) and oligozoospermia (reduced sperm concentration) are the two important reasons cited for idiopathic infertility in crossbred bulls; however, the etiology remains elusive. In this study, using a non-targeted liquid chromatography with tandem mass spectrometry-based approach, we carried out a deep metabolomic analysis of spermatozoa and seminal plasma derived from normozoospermic and astheno-oligozoospermic bulls. Using bioinformatics tools, alterations in metabolites and metabolic pathways between normozoospermia and astheno-oligozoospermia were elucidated. A total of 299 and 167 metabolites in spermatozoa and 183 and 147 metabolites in seminal plasma were detected in astheno-oligozoospermic and normozoospermic bulls, respectively. Among the mapped metabolites, 75 sperm metabolites were common to both the groups, whereas 166 and 50 sperm metabolites were unique to astheno-oligozoospermic and normozoospermic bulls, respectively. Similarly, 86 metabolites were common to both the groups, whereas 45 and 37 seminal plasma metabolites were unique to astheno-oligozoospermic and normozoospermic bulls, respectively. Among the differentially expressed metabolites, 62 sperm metabolites and 56 seminal plasma metabolites were significantly dysregulated in astheno-oligozoospermic bulls. In spermatozoa, selenocysteine, deoxyuridine triphosphate, and nitroprusside showed significant enrichment in astheno-oligozoospermic bulls. In seminal plasma, malonic acid, 5-diphosphoinositol pentakisphosphate, D-cysteine, and nicotinamide adenine dinucleotide phosphate were significantly upregulated, whereas tetradecanoyl-CoA was significantly downregulated in the astheno-oligozoospermia. Spermatozoa from astheno-oligozoospermic bulls showed alterations in the metabolism of fatty acid and fatty acid elongation in mitochondria pathways, whereas seminal plasma from astheno-oligozoospermic bulls showed alterations in synthesis and degradation of ketone bodies, pyruvate metabolism, and inositol phosphate metabolism pathways. The present study revealed vital information related to semen metabolomic differences between astheno-oligozoospermic and normospermic crossbred breeding bulls. It is inferred that fatty acid synthesis and ketone body degradations are altered in the spermatozoa and seminal plasma of astheno-oligozoospermic crossbred bulls. These results open up new avenues for further research, and current findings can be applied for the modulation of identified pathways to restore sperm motility and concentration in astheno-oligozoospermic bulls.
Highlights
Infertility is a multifactorial problem; a majority of infertility cases are idiopathic and molecular exploration on spermatozoa, and seminal plasma revealed that 50% of such problems were associated with a male partner [1]
After sorting out the metabolite IDs, the majority of the identified endogenous metabolites are categorized into lipid, phospholipid, glycerophospholipid, amines, common amino acid, fats, and common fatty acid based on functional enrichment of chemical compound in MBrole 2.0
LC/MS-MS chromatogram of some important peaks of endogenous metabolites of spermatozoa and seminal plasma of both the groups are represented in Supplementary Figures 2A,B as documentation of stable and reliable analytical method
Summary
Infertility is a multifactorial problem; a majority of infertility cases are idiopathic and molecular exploration on spermatozoa, and seminal plasma revealed that 50% of such problems were associated with a male partner [1]. Immature spermatocytes in astheno-oligozoospermia patients appear as a good source of reactive oxygen species (ROS) production, which alters mitochondrial DNA, membrane potential, depletes adenosine triphosphate, and triggers extensive damage to the lipid-rich membrane of spermatid and mature spermatozoa [10]. All these could lead to DNA damage in the normal sperm population and reduced fertility because semen with higher fragmented DNA is associated with male infertility [11]
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