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Control of intracellular pH and bicarbonate by CO₂ diffusion into human sperm.

ABSTRACT: The reaction of CO₂ with H₂O to form bicarbonate (HCO₃^-) and H⁺ controls sperm motility and fertilization via HCO₃^--stimulated cAMP synthesis. A complex network of signaling proteins participates in this reaction. Here, we identify key players that regulate intracellular pH (pH_i) and HCO₃^- in human sperm by quantitative mass spectrometry (MS) and kinetic patch-clamp fluorometry. The resting pH_i is set by amiloride-sensitive Na⁺/H⁺ exchange. The sperm-specific putative Na⁺/H⁺ exchanger SLC9C1, unlike its sea urchin homologue, is not gated by voltage or cAMP. Transporters and channels implied in HCO₃^- transport are not detected, and may be present at copy numbers < 10 molecules/sperm cell. Instead, HCO₃^- is produced by diffusion of CO₂ into cells and readjustment of the CO₂/HCO₃^-/H⁺ equilibrium. The proton channel H_v1 may serve as a unidirectional valve that blunts the acidification ensuing from HCO₃^- synthesis. This work provides a new framework for the study of male infertility.

SUBMITTER: Grahn E

PROVIDER: S-EPMC10480191 | biostudies-literature | 2023 Sep

REPOSITORIES: biostudies-literature

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Control of intracellular pH and bicarbonate by CO2 diffusion into human sperm.

Grahn Elena E Kaufmann Svenja V SV Askarova Malika M Ninov Momchil M Welp Luisa M LM Berger Thomas K TK Urlaub Henning H Kaupp U Benjamin UB

Nature communications 20230905 1

The reaction of CO2 with H2O to form bicarbonate (HCO3-) and H+ controls sperm motility and fertilization via HCO3--stimulated cAMP synthesis. A complex network of signaling proteins participates in this reaction. Here, we identify key players that regulate intracellular pH (pHi) and HCO3- in human sperm by quantitative mass spectrometry (MS) and kinetic patch-clamp fluorometry. The rest ...[more]

PMID: 37669933

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Project description:CO2 and bicarbonate are required for carboxylation reactions, which are essential in most bacteria. To provide the cells with sufficient CO2, there exist two dissolved inorganic carbon supply (DICS) systems: the membrane potential-generating system (MpsAB) and the carbonic anhydrase (CA). Recently, it has been shown that MpsAB is a bicarbonate transporter that is present not only in photo- and autotrophic bacteria, but also in a diverse range of nonautotrophic microorganisms. Since the two systems rarely coexist in a species but are interchangeable, we investigated what advantages the one system might have over the other. Using the genus Staphylococcus as a model, we deleted the CA gene can in Staphylococcus carnosus and mpsABC genes in Staphylococcus aureus. Deletion of the respective gene in one or the other species led to growth inhibition that could only be reversed by CO2 supplementation. While the S. carnosus Δcan mutant could be fully complemented with mpsABC, the S. aureus ΔmpsABC mutant was only partially complemented by can, suggesting that MpsAB outperforms CA. Interestingly, we provide evidence that mucus biofilm formation such as that involving polysaccharide intercellular adhesin (PIA) impedes the diffusion of CO2 into cells, making MpsAB more advantageous in biofilm-producing strains or species. Coexpression of MpsAB and CA does not confer any growth benefits, even under stress conditions. In conclusion, the distribution of MpsAB or CA in bacteria does not appear to be random as expression of bicarbonate transporters provides an advantage where diffusion of CO2 is impeded. IMPORTANCE CO2 and bicarbonate are required for carboxylation reactions in central metabolism and biosynthesis of small molecules in all bacteria. This is achieved by two different systems for dissolved inorganic carbon supply (DICS): these are the membrane potential-generating system (MpsAB) and the carbonic anhydrase (CA), but both rarely coexist in a given species. Here, we compared both systems and demonstrate that the distribution of MpsAB and/or CA within the phylum Firmicutes is apparently not random. The bicarbonate transporter MpsAB has an advantage in species where CO2 diffusion is hampered-for instance, in mucus- and biofilm-forming bacteria. However, coexpression of MpsAB and CA does not confer any growth benefits, even under stress conditions. Given the clinical relevance of Staphylococcus in the medical environment, such findings contribute to the understanding of bacterial metabolism and thus are crucial for exploration of potential targets for antimicrobials. The knowledge gained here as exemplified by staphylococcal species could be extended to other pathogenic bacteria.

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Control of intracellular pH and bicarbonate by CO₂ diffusion into human sperm.

Publications

Control of intracellular pH and bicarbonate by CO<sub>2</sub> diffusion into human sperm.

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