Biochimica et Biophysica Acta-Bioenergetics最新文献

{"title":"Increase in spillover and excitation energy dissipation during wet–dry transitions in the desert green alga Chlorella ohadii","authors":"Soma Kawamura ,&nbsp;Makio Yokono ,&nbsp;Chiyo Noda ,&nbsp;Jun Minagawa","doi":"10.1016/j.bbabio.2025.149573","DOIUrl":"10.1016/j.bbabio.2025.149573","url":null,"abstract":"<div><div><ul><li><span>•</span><span><div>Under drought, lack of an electron source (water) reduces the capacity of oxygen-evolving photosynthesis.</div></span></li><li><span>•</span><span><div>Consequently, even under low light, excess excitation energy may be generated, which is harmful as it leads to generation of reactive oxygen species.</div></span></li><li><span>•</span><span><div>When the desert green alga <em>Chlorella ohadii</em> undergoes desiccation, first photosystem II binds to photosystem I via LHCII to establish energy transfer pathways, and then excitation energy dissipation induced by a quencher is initiated.</div></span></li><li><span>•</span><span><div>This strategy may provide efficient protection of the entire photosynthetic apparatus during early stages of desiccation, when the available quencher may be insufficient.</div></span></li></ul></div></div>","PeriodicalId":50731,"journal":{"name":"Biochimica et Biophysica Acta-Bioenergetics","volume":"1867 1","pages":"Article 149573"},"PeriodicalIF":2.7,"publicationDate":"2025-09-17","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145092999","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}

{"title":"Mechanism of Na+ ions contribution to the generation and maintenance of a high inner membrane potential in mitochondria","authors":"Victor V. Lemeshko","doi":"10.1016/j.bbabio.2025.149571","DOIUrl":"10.1016/j.bbabio.2025.149571","url":null,"abstract":"<div><div>A recent revision of the chemiosmotic theory was reported by Hernansanz-Agustín and coauthors as a discovery that a Na⁺ gradient across the mitochondrial inner membrane equates with the H⁺ gradient and contributes up to half of the inner membrane potential, without an explanation of the possible underlying mechanism. Based on the experimental data of these and other authors, and performed biophysical estimations, I propose a mechanism by which both the reported fast-acting Na⁺/H⁺ exchanger, associated with the complex I of the respiratory chain, and Na⁺ electrodiffusion in the intracristae space and the matrix allow maintenance of a high membrane potential.</div></div>","PeriodicalId":50731,"journal":{"name":"Biochimica et Biophysica Acta-Bioenergetics","volume":"1867 1","pages":"Article 149571"},"PeriodicalIF":2.7,"publicationDate":"2025-09-04","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145007521","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}

{"title":"Vibrational cooling of monomeric bacteriochlorophylls in reaction centers of purple bacteria studied by time-resolved fluorescence spectroscopy","authors":"Andrei G. Yakovlev ,&nbsp;Alexandra S. Taisova","doi":"10.1016/j.bbabio.2025.149570","DOIUrl":"10.1016/j.bbabio.2025.149570","url":null,"abstract":"<div><div>Photosynthesis in bacteria, algae, and plants begins with the absorption of light energy by (bacterio)chlorophyll molecules, part of which is then converted into heat, leading to a transient change in molecular temperature. We investigated this phenomenon in reaction centers (RCs) of the purple bacterium <em>Rhodobacter</em> (<em>Rba</em>.) <em>sphaeroides</em> using picosecond fluorescence spectroscopy. Exclusion of charge separation processes using the VR(L157) mutation allowed us to record the spectral dynamics of fluorescence of monomeric BChl <em>a</em> molecules. We found that excitation of RCs into the Soret band results in significant heating of BChl <em>a</em> by ~160 K with subsequent vibrational cooling, which manifests itself in a dynamic narrowing of the BChl <em>a</em> fluorescence spectrum with two characteristic times of 5 and 16 ps. The weaker heating by ~65 K and cooling with a characteristic time of 7.5 ps are observed upon excitation of RCs into the Q_x band. Excitation into the Q_у band does not result in any noticeable heating of BChl <em>a</em>. Difference absorption spectroscopy of tryptophan in the 280 nm region showed that the observed dynamics of the BChl <em>a</em> fluorescence spectrum are not associated with the dielectric rearrangement of the RCs protein matrix. Analysis of the obtained data using the phenomenological model of vibrational cooling led to the conclusion that during heat diffusion from excited BChl <em>a</em>, several amino acid residues from the immediate environment of BChl <em>a</em> act as the first solvation shell (FSS). At the first, faster stage, heat is transferred from BChl <em>a</em> to FSS, and at the second stage, FSS transfers heat to the protein matrix of RCs. Our work has shown the importance of taking into account vibrational cooling when studying the primary processes of photosynthesis.</div></div>","PeriodicalId":50731,"journal":{"name":"Biochimica et Biophysica Acta-Bioenergetics","volume":"1866 4","pages":"Article 149570"},"PeriodicalIF":2.7,"publicationDate":"2025-08-25","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144904589","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}

{"title":"Photodamage and excitation energy quenching in PSII: A time-resolved fluorescence study in Arabidopsis","authors":"Cleo Bagchus ,&nbsp;Herbert van Amerongen ,&nbsp;Emilie Wientjes","doi":"10.1016/j.bbabio.2025.149569","DOIUrl":"10.1016/j.bbabio.2025.149569","url":null,"abstract":"<div><div>Photosynthesis is driven by light absorbed in photosystem (PS) I and II. Paradoxically, light can also inactivate photosynthesis, mainly by damage to PSII. The light-dependent decrease in functional PSII, referred to as photoinhibition, is initially accompanied by an increase of excitation quenching, energy dissipation characterized by a decline in the lifetime and yield of chlorophyll fluorescence. In plants, research has not yet been performed on the effect of photoinhibition on the fluorescence lifetime of PSII in conditions where the PSII reaction centers are closed or remain open (capable of performing photochemistry).</div><div>In this work, we studied the effect of photoinhibition on the fluorescence lifetime of PSII in <em>Arabidopsis thaliana</em> using time-resolved fluorescence measurements with a streak-camera setup in both closing (F_m) and non-closing (F_o) conditions. Measurements under F_m conditions in the <em>chlorina</em> mutant, lacking peripheral antenna, demonstrate formation of a photoinhibitory quencher in the PSII core complex. In F_o_, the average fluorescence lifetime of PSII increases upon induction of photoinhibition. This could be due to the degradation of quenched PSII core reaction center protein by FtsH proteases, which leads to unquenched and dysfunctional PSII. We tested this hypothesis by comparing WT plants with the FtsH2 lacking mutant. Based on the similar behavior, we conclude that degradation by FtsH proteases is not the main cause of the increase. Instead this increase is caused by the larger antenna size of still functional PSII. These findings provide new insights into the impact of photoinhibition on the PSII fluorescence lifetime in <em>A. thaliana</em>.</div></div>","PeriodicalId":50731,"journal":{"name":"Biochimica et Biophysica Acta-Bioenergetics","volume":"1866 4","pages":"Article 149569"},"PeriodicalIF":2.7,"publicationDate":"2025-08-11","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144849506","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}

{"title":"Chamber oxygen concentration impacts mitochondrial function and hydrogen peroxide appearance in permeabilized human skeletal muscle fibers","authors":"Bradley A. Ruple ,&nbsp;Soung Hun Park ,&nbsp;Jesse C. Craig ,&nbsp;Matthew T. Lewis ,&nbsp;Joel D. Trinity ,&nbsp;Russell S. Richardson ,&nbsp;Ryan M. Broxterman","doi":"10.1016/j.bbabio.2025.149568","DOIUrl":"10.1016/j.bbabio.2025.149568","url":null,"abstract":"<div><div>Skeletal muscle mitochondrial respiration is commonly assessed ex vivo using permeabilized fibers in media with high oxygen (O₂) concentrations to ensure that O₂ availability does not limit respiration. However, high O₂ concentrations also increase the production of reactive O₂ species that can negatively affect respiration. In this study, we tested the hypotheses that permeabilized fiber mitochondria in a high, compared to low, O₂ concentration would (i) not be different at maximal state 3 respiration rate (V_max), (ii) have lower submaximal respiration rates at submaximal O₂ concentrations, and (iii) have greater total cumulative hydrogen peroxide (H₂O₂) appearance. We continuously monitored mitochondrial state 3 respiration and H₂O₂ appearance rates using high-resolution respirometry in permeabilized skeletal muscle fibers (12 untrained participants; 22 ± 4 yrs) with either control (~127 mmHg; CON) or high (~327 mmHg; HIGH) partial pressures of O₂ (PO₂). V_max was not different between conditions (HIGH: 80.7 ± 16.7 vs. CON: 82.3 ± 18.7 pmol/s/mg, <em>p</em> = 0.695). The PO₂ at 80 % V_max (P₈₀) was greater in HIGH (73.9 ± 25.5 vs. 28.0 ± 7.1 mmHg, <em>p</em> &lt; 0.001) and respiration rates at 5–60 mmHg PO₂ were lower for HIGH than CON (all <em>p</em> &lt; 0.001). Additionally, the total cumulative H₂O₂ appearance was greater in HIGH than CON (<em>n</em> = 11; 51.5 ± 23.2 vs. 18.3 ± 10.3 pmol/mg, <em>p</em> &lt; 0.001), and this difference was directly correlated with the difference in P₈₀ (<em>r</em> = 0.655, <em>p</em> = 0.029). The current findings support that a high O₂ concentration, by itself, does not appear to affect V_max in the permeabilized skeletal muscle fiber preparation, but the corollary increase in H₂O₂ exposure may diminish mitochondrial state 3 respiratory function.</div></div>","PeriodicalId":50731,"journal":{"name":"Biochimica et Biophysica Acta-Bioenergetics","volume":"1866 4","pages":"Article 149568"},"PeriodicalIF":2.7,"publicationDate":"2025-08-11","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144842126","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}

{"title":"Deletion of AC8 in glioma cells elevates oxidative phosphorylation by system-wide remodeling of the mitochondrial proteome","authors":"Emil Jakobsen ,&nbsp;Jacob M. Bech ,&nbsp;Jens V. Andersen ,&nbsp;Emil W. Westi ,&nbsp;Martin R. Larsen ,&nbsp;Niels H. Skotte ,&nbsp;José M.A. Moreira ,&nbsp;Blanca I. Aldana ,&nbsp;Lasse K. Bak","doi":"10.1016/j.bbabio.2025.149567","DOIUrl":"10.1016/j.bbabio.2025.149567","url":null,"abstract":"<div><div>The Warburg effect is the reprogramming of cancer cells towards glycolytic metabolism, likely producing and releasing lactate into the tumor microenvironment. This lactate has been suggested to partly drive tumor growth by signaling through the lactate receptor, GPR81. Thus, reprogramming cancer cells away from glycolytic activity may be beneficial for cancer treatment. Here, we show that deletion of <em>ADCY8</em> (coding for adenylyl cyclase 8; AC8) employing the CRISPR-Cas9 technology in U87MG glioma cells, changes the proteome of these cells through a system-wide transformation in expression of mitochondrial proteins. These changes shift the metabolic balance towards oxidative phosphorylation, as shown by an increase in oxygen consumption, an elevation in tricarboxylic acid cycle flux, and a concomitant decrease in glycolytic flux. This metabolic shift is likely driven by the absence of AC8-mediated transcriptional regulation and may suggest that inhibition of AC8 activity could hold therapeutic potential in the treatment of cancer.</div></div>","PeriodicalId":50731,"journal":{"name":"Biochimica et Biophysica Acta-Bioenergetics","volume":"1866 4","pages":"Article 149567"},"PeriodicalIF":3.4,"publicationDate":"2025-07-14","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144651137","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}

{"title":"Dynamic binding of acetogenin-type inhibitors to mitochondrial complex I revealed by photoaffinity labeling","authors":"Misaki Nishida ,&nbsp;Cristina Pecorilla ,&nbsp;Takahiro Masuya ,&nbsp;Keitaro Hirano ,&nbsp;Masato Abe ,&nbsp;Oleksii Zdorevskyi ,&nbsp;Vivek Sharma ,&nbsp;Hideto Miyoshi ,&nbsp;Masatoshi Murai","doi":"10.1016/j.bbabio.2025.149566","DOIUrl":"10.1016/j.bbabio.2025.149566","url":null,"abstract":"<div><div>Acetogenins isolated from the <em>Annonaceae</em> plant family are potent inhibitors of mitochondrial NADH-ubiquinone (UQ) oxidoreductase (complex I). Since acetogenins have a markedly different chemical framework from other complex I inhibitors, studying their inhibitory action offers valuable insights into the mechanism of complex I inhibition. A cryo-EM structure of mouse complex I with a bound ~35 Å-long acetogenin derivative suggested that acetogenins bind along the full length of the predicted UQ-accessing tunnel, with their γ-lactone ring orientating toward the iron‑sulfur cluster N2. However, this binding mode does not fully explain the structure–activity relationships of various acetogenin derivatives. To further elucidate their inhibition mechanism, we conducted photoaffinity labeling experiments in bovine heart SMPs using a photoreactive acetogenin derivative DLA-1, containing a small photolabile diazirine near the γ-lactone ring. DLA-1 labeled both the complex I subunits 49-kDa and ND1, which define the architecture of “top” and “bottom” regions of the canonical UQ-accessing tunnel, respectively. Proteomic analysis revealed that the labeled sites in ND1 are not within the tunnel's interior, whereas in the case of 49-kDa subunit, part of the tunnel's inner region is labeled. To investigate the molecular basis of acetogenin binding, we performed atomistic molecular dynamics simulations of DLA-1 and a natural-type acetogenin analog in the UQ-accessing tunnel. The simulation data indicate that DLA-1 is relatively rigid yet adopts multiple conformations and interacts with several regions in the tunnel including the residues identified by photoaffinity labeling. Based on these results, we discuss the binding modes of acetogenin analogs to complex I.</div></div>","PeriodicalId":50731,"journal":{"name":"Biochimica et Biophysica Acta-Bioenergetics","volume":"1866 4","pages":"Article 149566"},"PeriodicalIF":3.4,"publicationDate":"2025-06-29","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144545921","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}

{"title":"Human VDAC3 as a sensor of the intracellular redox state: contribution to cytoprotection mechanisms in oxidative stress","authors":"Martyna Baranek-Grabińska ,&nbsp;Tomasz Skrzypczak ,&nbsp;Hanna Kmita ,&nbsp;Andonis Karachitos","doi":"10.1016/j.bbabio.2025.149565","DOIUrl":"10.1016/j.bbabio.2025.149565","url":null,"abstract":"<div><div>Voltage-dependent anion channels (VDACs) are essential for mitochondrial function, facilitating the exchange of metabolites between the cytosol and mitochondria. This study investigated the role of human VDAC paralogs, hVDAC1, hVDAC2, and hVDAC3, in maintaining mitochondrial function under oxidative stress in <em>Saccharomyces cerevisiae</em> strains lacking endogenous VDACs (encoded by <em>POR1</em> and <em>POR2</em>) and antioxidant enzymes, i.e., superoxide dismutases (encoded by <em>SOD1</em> and <em>SOD2</em>). The yeast cells expressing hVDAC3 showed stable growth under oxidative stress, maintained mitochondrial membrane potential and morphology, exhibited reduced superoxide anion levels, and achieved efficient ATP synthesis with minimal proton leak. In contrast, the cells expressing hVDAC1 or hVDAC2 presented impaired mitochondrial function which was supported by differences in bioenergetic profiles including ATP synthesis and proton leak but also FCCP uncoupling capacity and spare respiratory capacity. The cysteine-depleted variant of hVDAC3 (hVDAC3ΔCys) showed impaired cell growth under stress conditions, indicating that the cysteine residues in hVDAC3 are essential for its protective role. These findings highlight the unique protective function of hVDAC3 under oxidative stress, which is attributed to efficient metabolite transport and regulation via cysteine oxidation.</div></div>","PeriodicalId":50731,"journal":{"name":"Biochimica et Biophysica Acta-Bioenergetics","volume":"1866 4","pages":"Article 149565"},"PeriodicalIF":3.4,"publicationDate":"2025-06-28","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144517673","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}

{"title":"ATP requirements for growth reveal the bioenergetic impact of mitochondrial symbiosis","authors":"William F. Martin","doi":"10.1016/j.bbabio.2025.149564","DOIUrl":"10.1016/j.bbabio.2025.149564","url":null,"abstract":"<div><div>Studies by microbiologists in the 1970s provided robust estimates for the energy supply and demand of a prokaryotic cell. The amount of ATP needed to support growth was calculated from the chemical composition of the cell and known enzymatic pathways that synthesize its constituents from known substrates in culture. Starting in 2015, geneticists and evolutionary biologists began investigating the bioenergetic role of mitochondria at eukaryote origin and energy in metazoan evolution using their own, widely trusted—but hitherto unvetted—model for the costs of growth in terms of ATP per cell. The more recent model contains, however, a severe and previously unrecognized error that systematically overestimates the ATP cost of amino acid synthesis up to 200-fold. The error applies to all organisms studied by such models and leads to conspicuously false inferences, for example that the synthesis of an average amino acid in humans requires 30 ATP, which no biochemistry textbook will confirm. Their ATP ‘cost’ calculations would require that <em>E. coli</em> obtains ~100 ATP per glucose and that mammals obtain ~240 ATP per glucose, untenable propositions that invalidate and void all evolutionary inferences so based. By contrast, established methods for estimating the ATP cost of microbial growth show that the first mitochondrial endosymbionts could have easily doubled the host's available ATP pool, provided (i) that genes for growth on environmental amino acids were transferred from the mitochondrial symbiont to the archaeal host, and (ii) that the host for mitochondrial origin was an autotroph using the acetyl-CoA pathway. Stated in simple terms, the significance of these findings are this: Life is a chemical reaction. It requires energy release in order to proceed. The currency of energy in cells is adenosine triphosphate, ATP. Five decades ago, microbiologists were able to measure and understand the amount of ATP that cells require to grow. New studies by evolutionary biologists have appeared in the meantime that brush aside the older microbiological findings, using their own methods to calculate the ATP cost of growth instead. Science is, however, an imperfect undertaking. The new studies contain a major error, similar to conflating centimeters with yards. The error affects many publications and their conclusions. Using the old methods, we can still meaningfully study the role of energy in evolution, including the origin of complex, nucleus-bearing cells.</div></div>","PeriodicalId":50731,"journal":{"name":"Biochimica et Biophysica Acta-Bioenergetics","volume":"1866 4","pages":"Article 149564"},"PeriodicalIF":3.4,"publicationDate":"2025-06-23","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144499075","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}

{"title":"Conformational dynamics of a histidine molecular switch in a cation/proton antiporter","authors":"Cristina Pecorilla ,&nbsp;Anton Altmeyer ,&nbsp;Outi Haapanen ,&nbsp;Yongchan Lee ,&nbsp;Volker Zickermann ,&nbsp;Vivek Sharma","doi":"10.1016/j.bbabio.2025.149563","DOIUrl":"10.1016/j.bbabio.2025.149563","url":null,"abstract":"<div><div>Multisubunit Mrp (<u>m</u>ultiple <u>r</u>esistance and <u>p</u>H adaptation) type sodium proton antiporters are indispensable for the growth of alkali and salt tolerant bacteria and archaea. They share sequence and structural similarity with the membrane domain of respiratory complex I, a key mitochondrial enzyme. The molecular mechanism of complex I and Mrp antiporters has remained largely unknown and is the subject of intense debate. Here, by combining site-directed mutagenesis with large-scale molecular dynamics simulations, we explore the conformational dynamics of a key histidine residue in the MrpA subunit of the antiporter. We show that point mutations perturbing the conformational mobility of the histidine sidechain directly affect the transport activity of the antiporter. We identify that protonation state variations in conserved lysine residues around the histidine drive hydrogen bonding rearrangements and hydration changes coupled to sidechain and backbone conformational dynamics. Finally, we develop detailed and testable mechanistic models of proton transfer in Mrp antiporter and complex I, in which the histidine switch functions as a unique gating element.</div></div>","PeriodicalId":50731,"journal":{"name":"Biochimica et Biophysica Acta-Bioenergetics","volume":"1866 4","pages":"Article 149563"},"PeriodicalIF":3.4,"publicationDate":"2025-06-17","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144481769","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}