Electronic energy migration in microtubules
Open accessAbstract
The repeating arrangement of tubulin dimers confers great mechanical strength to microtubules, which are used as scaffolds for intracellular macromolecular transport in cells and exploited in biohybrid devices. The crystalline order in a microtubule, with lattice constants short enough to allow energy transfer between amino acid chromophores, is similar to synthetic structures designed for light harvesting. After photoexcitation, can these amino acid chromophores transfer excitation energy along the microtubule like a natural or artificial light-harvesting system? Here, we use tryptophan autofluorescence lifetimes to probe energy hopping between aromatic residues in tubulin and microtubules. By studying how the quencher concentration alters tryptophan autofluorescence lifetimes, we demonstrate that electronic energy can diffuse over 6.6 nm in microtubules. We discover that while diffusion lengths are influenced by tubulin polymerization state (free tubulin versus tubulin in the microtubule lattice), they are not significantly altered by the average number of protofilaments (13 versus 14). We also demonstrate that the presence of the anesthetics etomidate and isoflurane reduce exciton diffusion. Energy transport as explained by conventional Förster theory (accommodating for interactions between tryptophan and tyrosine residues) does not sufficiently explain our observations. Our studies indicate that microtubules are, unexpectedly, effective light harvesters.
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Written from the paper’s full text.
TL;DR
Tryptophan autofluorescence lifetimes show that electronic excitation energy can migrate over 6.64 ± 0.1 nm in microtubules, far beyond conventional Förster-theory predictions. The diffusion length depends on tubulin polymerization state and is reduced by etomidate and isoflurane, suggesting microtubules act as unexpectedly effective light harvesters.
Key findings
- Microtubules showed a 2D tryptophan photoexcitation diffusion coefficient of 3.15 ± 0.1 × 10–5 cm2·s–1 and diffusion length of 6.64 ± 0.1 nm, compared with 4 ± 0.1 nm in free GTP-tubulin.
- Tryptophan quenching constants were 23.84 ± 0.8 ns–1 for 13-protofilament GTP microtubules versus 7.46 ± 0.4 ns–1 for free GTP-tubulin; 14-protofilament GMPCPP microtubules gave a similar diffusion length of 6.1 ± 0.1 nm.
- Etomidate and isoflurane (50 μM) reduced microtubule diffusion lengths to 5.6 ± 0.1 nm and 5.8 ± 0.2 nm, respectively, with quenching constants of 17.47 ± 0.5 ns–1 and 18.43 ± 1.2 ns–1.
- Conventional Förster theory simulations over 3000 trajectories predicted only 1.11 nm for intertyrosine interactions and 1.54 nm including tyrosine–tryptophan interactions, much lower than experiment.
Methods
- Tryptophan autofluorescence lifetimes were measured by time-correlated single photon counting using 305 nm excitation and 335 nm emission, with AMCA as an externally conjugated quencher at varying concentrations; Stern–Volmer static quenching analysis yielded quenching rates, diffusion coefficients, and diffusion lengths.
- Tubulin states included free GTP-tubulin, 13-protofilament GTP microtubules, 14-protofilament GMPCPP microtubules, vinblastine-induced oligomers, and microtubules with etomidate or isoflurane; negative stain electron microscopy confirmed polymorphs, and experiments were repeated n = 3 to 5 times.
- Computational work used a microtubule model of 31 stacked tubulin rings, dipole-approximation coupling calculations, kinetic Monte Carlo simulations of 3000 trajectories, and docking simulations for anesthetic binding to tubulin.
Limitations
- The paper states that the diffusion length is “not definite but should be a reliable order of magnitude estimate” because tryptophan has multiexponential fluorescence decays and the analysis uses average weighted lifetimes.
- The paper states that vinblastine produced overlapping fluorescence, making it difficult to quantify tryptophan signal from tubulin oligomers, and that dipole-approximation/Förster theory may be inaccurate for closely spaced chromophores; short-range charge-transfer integrals up to 419 cm–1 suggest additional coupling not captured.
- Evident from the text: experiments use purified porcine brain tubulin in vitro with paclitaxel stabilization and without MAPs or bundling drugs, so the biological relevance of the observed energy migration and anesthetic effects remains to be established in cellular contexts.
Model-written summary. Check it against the paper before relying on it.
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Claims the paper makes
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- Findingown data
The 2D diffusion length for microtubules is 6.64 ± 0.1 nm.
“Our data yielded a 2D diffusion coefficient of 3.15 ± 0.1 × 10–5 cm2·s–1 and a corresponding diffusion length of 6.64 ± 0.1 nm for microtubules (Table 1, Figure 5B,C).”
Quote in the paperSubstantial claim- The authors state this as an assumption: The sum of the tryptophan and AMCA radii is 1 nm.
- Findingown data
Stern-Volmer analysis revealed quenching constants of 23.8 ± 0.8 ns-1 for microtubules and 7.5 ± 0.4 ps-1 for free GTP-tubulin.
“Our analysis for microtubules and free GTP-tubulin in solution revealed quenching constants of 23.8 ± 0.8 ns–1 and 7.5 ± 0.4 ps–1, respectively (Figure 4A, Table 1).”
Quote in the paperSubstantial claim - Findingown data
The simulated diffusion lengths (1.11 and 1.54 nm) are appreciably lower than the experimental diffusion lengths.
“In both simulations, the obtained diffusion lengths (1.11 and 1.54 nm, respectively) are appreciably lower than the diffusion lengths obtained experimentally.”
Quote in the paperSubstantial claim- The authors state this as an assumption: The sum of the tryptophan and AMCA radii is 1 nm.
- The authors state this as an assumption: The refractive index of the medium surrounding the microtubule is 1.4.
- Findingown data
AMCA fluorescence emission was observed on tryptophan photoexcitation in steady-state experiments.
“also observed AMCA fluorescence emission on tryptophan photoexcitation in steady-state experiments (Figure 2E,F)”
Quote in the paperSubstantial claim - Findingown data
Tryptophan fluorescence lifetimes in microtubules shortened on increasing AMCA concentration.
“We found that tryptophan fluorescence lifetimes in microtubules shortened on increasing AMCA concentration (Figure 4A)”
Quote in the paperSubstantial claim
- Findingown data
The presence of isoflurane decreased the 2D diffusion length from 6.6 ± 0.1 nm to 5.8 ± 0.2 nm.
“The presence of etomidate and isoflurane decreased the 2D diffusion lengths from 6.6 ± 0.1 nm to 5.6 ± 0.1 nm and 5.8 ± 0.2 nm, respectively (Figure 5C).”
Quote in the paperSubstantial claim- The authors state this as an assumption: The sum of the tryptophan and AMCA radii is 1 nm.
- Findingown data
The 2D diffusion coefficient for microtubules is 3.15 ± 0.1 × 10-5 cm2·s-1.
“Our data yielded a 2D diffusion coefficient of 3.15 ± 0.1 × 10–5 cm2·s–1 and a corresponding diffusion length of 6.64 ± 0.1 nm for microtubules (Table 1, Figure 5B,C).”
Quote in the paperSubstantial claim- The authors state this as an assumption: The sum of the tryptophan and AMCA radii is 1 nm.
- Findingown data
The presence of etomidate decreased the 2D diffusion length from 6.6 ± 0.1 nm to 5.6 ± 0.1 nm.
“The presence of etomidate and isoflurane decreased the 2D diffusion lengths from 6.6 ± 0.1 nm to 5.6 ± 0.1 nm and 5.8 ± 0.2 nm, respectively (Figure 5C).”
Quote in the paperSubstantial claim- The authors state this as an assumption: The sum of the tryptophan and AMCA radii is 1 nm.
- Findingown data
Introducing 50 μM etomidate and isoflurane significantly lowered tryptophan quenching by AMCA in GTP-polymerized microtubules.
“Introducing 50 μM etomidate and isoflurane significantly lowered tryptophan quenching by AMCA in GTP-polymerized microtubules (Figure 4C; Figure S16).”
Quote in the paperSubstantial claim - Findingown data
Changing the number of protofilaments from 13 to 14 has a negligible effect on the 2D photoexcitation diffusion length.
“Changing the number of protofilaments from 13 to 14 has a negligible effect on the 2D photoexcitation diffusion length.”
- Also stated in: § Abstract · plain
“they are not significantly altered by the average number of protofilaments (13 versus 14).”
Quote in the paperNot a substantial claim- The authors state this as an assumption: The sum of the tryptophan and AMCA radii is 1 nm.
- Also stated in: § Abstract · plain
- Findingown data
Polymerizing into microtubules enhances diffusion lengths from 4 ± 0.1 nm in free GTP tubulin to 6.64 ± 0.1 nm in microtubules.
“Polymerizing into microtubules enhances diffusion lengths from 4 ± 0.1 nm in free GTP tubulin to 6.64 ± 0.1 nm in microtubules.”
Quote in the paperSubstantial claim- The authors state this as an assumption: The sum of the tryptophan and AMCA radii is 1 nm.
- Findingown data
The 2D photoexcitation diffusion length in microtubules (6.6 ± 0.1 nm) is substantially higher than that predicted by conventional Förster theory (1.11 nm for intertyrosine interactions and 1.54 nm including tyrosine-tryptophan interactions).
“Here, we exploit tryptophan autofluorescence to show that the 2D photoexcitation diffusion length in microtubules (6.6 ± 0.1 nm) is substantially higher than that predicted by conventional Förster theory (1.11 nm for intertyrosine interactions and 1.54 nm including tyrosine-tryptophan interactions).”
Quote in the paperSubstantial claim- The authors state this as an assumption: The sum of the tryptophan and AMCA radii is 1 nm.
- The authors state this as an assumption: The refractive index of the medium surrounding the microtubule is 1.4.
- Findingown data
Diffusion lengths are influenced by tubulin polymerization state (free tubulin versus tubulin in the microtubule lattice).
“while diffusion lengths are influenced by tubulin polymerization state (free tubulin versus tubulin in the microtubule lattice)”
- Also stated in: § Discussion and Conclusion · hedged
“Our observations suggest that photoexcitation diffusion takes place in a manner that is dependent on the tubulin polymorph type (tubulin dimers versus oligomers versus microtubules).”
Quote in the paperSubstantial claim- The authors state this as an assumption: The sum of the tryptophan and AMCA radii is 1 nm.
- Also stated in: § Discussion and Conclusion · hedged
- Findingown data
AMCA itself contributed a negligible signal over the relevant wavelength range.
“AMCA itself contributed a negligible signal over the relevant wavelength range (Figure S6).”
Quote in the paperSubstantial claim - Findingown data
The lifetime trend in the presence of AMCA in GMPCPP-microtubules resembled that of GTP-microtubules (p > 0.005).
“the lifetime trend in the presence of AMCA in GMPCPP-microtubules resembled that of GTP-microtubules (p-values > 0.005; Figure 4B).”
Quote in the paperSubstantial claim - Findingown data
Introducing 50 μM picrotoxin decreased tryptophan quenching by AMCA.
“It is also worth noting that introducing a convulsant (50 μM picrotoxin) also decreased tryptophan quenching by AMCA.”
Quote in the paperNot a substantial claim- Rests on an assumption: AMCA labeling at random surface lysines does not perturb tubulin structure or photoexcitation energy migration.
- Findingown data
Unlabeled tryptophan fluorescence lifetimes in GMPCPP-microtubules were significantly lower than those in GTP-microtubules (p < 0.005).
“Our results showed that while unlabeled tryptophan fluorescence lifetimes in GMPCPP-microtubules were significantly lower than those in GTP-microtubules (p-values < 0.005; Figure S10B)”
Quote in the paperSubstantial claim - Findingown data
Photoexcitation diffusion lengths decrease in tubulin oligomers formed in the presence of vinblastine.
“our data also suggest that photoexcitation diffusion lengths decrease in tubulin oligomers (formed in the presence of vinblastine)”
Quote in the paperNot a substantial claim- The authors state this as an assumption: The sum of the tryptophan and AMCA radii is 1 nm.
- Findingown data
The diffusion length obtained for tubulin oligomers is 4.6 ± 0.1 nm.
“the diffusion length obtained from such analysis (4.6 ± 0.1 nm) indicates long-range electronic energy transport in oligomers.”
Quote in the paperSubstantial claim- The authors state this as an assumption: The sum of the tryptophan and AMCA radii is 1 nm.
- Findingown data
Tryptophan autofluorescence can distinguish between polymerized and unpolymerized tubulin.
“We showed that tryptophan autofluorescence can distinguish between polymerized and unpolymerized tubulin.”
Quote in the paperSubstantial claim - Findingown data
Photoexcitation diffusion cannot be explained via conventional Förster theory, which accounts for only dipole-dipole interactions between tryptophan and tyrosine residues.
“A key finding of our study is that photoexcitation diffusion cannot be explained via conventional Förster theory, which accounts for only dipole–dipole interactions between tryptophan and tyrosine residues.”
Quote in the paperSubstantial claim- Rests on an assumption: Tryptophan quenching by AMCA is a valid measure of photoexcitation diffusion in microtubules.
- Rests on an assumption: AMCA labeling at random surface lysines does not perturb tubulin structure or photoexcitation energy migration.
- Findingown data
The tuning of photoexcitation diffusion length through biochemical parameters of microtubules (tubulin polymerization, introduction of anesthetics) was observed.
“The tuning of photoexcitation diffusion length through biochemical parameters of microtubules (tubulin polymerization, introduction of anesthetics) was a further intriguing observation.”
Quote in the paperNot a substantial claim- Rests on an assumption: Tryptophan quenching by AMCA is a valid measure of photoexcitation diffusion in microtubules.
- Rests on an assumption: AMCA labeling at random surface lysines does not perturb tubulin structure or photoexcitation energy migration.
- Interpretationreasoning
A diffusion length of 6.64 nm suggests that energy transfer between tryptophan residues across a single tubulin dimer can occur in a microtubule.
“Given that a single tubulin dimer occupies the same volume as a sphere of diameter 7.4 nm (from its dimensions of 4 nm × 6.5 nm × 8 nm), a diffusion length of 6.64 nm suggests that energy transfer between tryptophan residues across a single tubulin dimer can occur in a microtubule.”
Quote in the paperSubstantial claim- The authors state this as an assumption: The sum of the tryptophan and AMCA radii is 1 nm.
- Interpretationreasoning
Depending on initial photoexcitation location, energy could reasonably migrate to the adjacent tubulin dimer within the microtubule lattice.
“Depending on the locations of the residue where the initial photoexcitation occurred, it could reasonably migrate to the adjacent tubulin dimer within the microtubule lattice.”
Quote in the paperSubstantial claim- The authors state this as an assumption: The sum of the tryptophan and AMCA radii is 1 nm.
- Interpretationown data
Intermolecular orbital overlap mediated interactions could increase the electronic coupling and therefore the predicted exciton diffusion length.
“which suggests that the intermolecular orbital overlap mediated interactions could increase the electronic coupling and therefore the predicted exciton diffusion length.”
Quote in the paperSubstantial claim- The authors state this as an assumption: The refractive index of the medium surrounding the microtubule is 1.4.
- Interpretationreasoning
Etomidate and isoflurane dampen energy transfer between tryptophan and AMCA due to changes in dielectric screening of electronic couplings.
“Taken together, these findings suggest that etomidate and isoflurane “dampen” energy transfer between tryptophan and AMCA due to changes in the dielectric screening of electronic couplings.”
Quote in the paperSubstantial claim - Interpretationreasoning
The higher quenching rate in microtubules can be explained by sensitization of AMCA quenching sites remote from the photoexcited tubulin dimer via multiple energy transfer steps.
“The higher quenching rate in microtubules can be explained by sensitization of AMCA quenching sites remote from the photoexcited tubulin dimer, which can occur by multiple energy transfer steps (as energy migrates from tryptophan to other aromatic residues in its vicinity).”
Quote in the paperSubstantial claim - Interpretationown data
Microtubules are effective light harvesters.
“Our studies indicate that microtubules are, unexpectedly, effective light harvesters.”
- Also stated in: § Discussion and Conclusion · plain
“In this work, we find that microtubules are more effective light-harvesters than anticipated for a protein devoid of bound chromophores.”
Quote in the paperSubstantial claim- The authors state this as an assumption: The sum of the tryptophan and AMCA radii is 1 nm.
- The authors state this as an assumption: The refractive index of the medium surrounding the microtubule is 1.4.
- Also stated in: § Discussion and Conclusion · plain
- Interpretationown data
The diffusion lengths observed in GMPCPP microtubules support the notion that a repeating arrangement of tubulin dimers is sufficient to allow long-range photoexcitation energy transfer.
“The diffusion lengths observed in GMPCPP microtubules also support the notion that a repeating arrangement of tubulin dimers is sufficient to allow long-range photoexcitation energy transfer.”
Quote in the paperSubstantial claim - Interpretationown data
Photoexcitation may migrate more effectively along protofilaments, as opposed to rings.
“indicating that photoexcitation may migrate more effectively along protofilaments, as opposed to rings.”
Quote in the paperNot a substantial claim - Interpretationown data
The 2D diffusion length in microtubules is comparable to that observed in some photosynthetic complexes and organic photovoltaic devices.
“Stern–Volmer analysis revealed that the 2D diffusion length of tryptophan photoexcitation in microtubules is comparable to that observed in some photosynthetic complexes23−25 and organic photovoltaic devices.45−47”
Quote in the paperSubstantial claim0 of 6 sources checked- cites [23] source
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- cites [45] source
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- cites [46] source
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- cites [47] source
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- The authors state this as an assumption: The sum of the tryptophan and AMCA radii is 1 nm.
- Premisecitation
Tryptophan absorbs light poorly compared to chlorophyll a.
“Because tryptophan absorbs light poorly (molar extinction coefficient of ∼5600 M–1 cm–160) compared to chlorophyll a (molar extinction coefficient of ∼110,000 M–1 cm–161) photoexcitation diffusion on a lengths scale of several nanometers was not expected.”
Quote in the paperSubstantial claim0 of 2 sources checked- cites [60] Fasman G. D., 2018
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- cites [61] source
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- Interpretationown data
The different tryptophan quenching rates in GMPCPP-microtubules are ascribed to differences in tryptophan fluorescence lifetime in the absence of AMCA.
“Stern–Volmer analysis revealed different tryptophan quenching rates in GMPCPP-microtubules, which we ascribe to differences in tryptophan fluorescence lifetime in the absence of AMCA.”
Quote in the paperNot a substantial claim - Interpretationown data
Long-range electronic energy transport occurs in tubulin oligomers.
“the diffusion length obtained from such analysis (4.6 ± 0.1 nm) indicates long-range electronic energy transport in oligomers.”
Quote in the paperSubstantial claim- The authors state this as an assumption: The sum of the tryptophan and AMCA radii is 1 nm.
- Interpretationown data
Electronic energy migration is surprisingly efficient in microtubules.
“our results demonstrate that electronic energy migration is surprisingly efficient in microtubules.”
Quote in the paperSubstantial claim- The authors state this as an assumption: The sum of the tryptophan and AMCA radii is 1 nm.
- The authors state this as an assumption: The refractive index of the medium surrounding the microtubule is 1.4.
- Study design and conductreasoning
Intermicrotubule separation distances were large enough in solution for electronic energy transfer to be insignificant.
“Due to MAPs and drugs that induce microtubule bundling being absent in our solutions and the highly charged C-termini tail of tubulin (expected to cause intermicrotubule repulsion), intermicrotubule separation distances were large enough in solution for electronic energy transfer to be insignificant.”
Quote in the paperSubstantial claim - Interpretationown data
Anesthetics are not the only macromolecules that decrease photoexcitation diffusion in microtubules.
“These additional experiments that we do not report here suggest that anesthetics are not the only macromolecules that decrease photoexcitation diffusion in microtubules.”
Quote in the paperSubstantial claim- Rests on an assumption: Tryptophan quenching by AMCA is a valid measure of photoexcitation diffusion in microtubules.
- Interpretationreasoning
Protein polymers may be suitable for active materials in biologically sourced electronic devices where UV photoexcitation is desired.
“Our work shows that protein polymers may be suitable for active materials in biologically sourced electronic devices where UV photoexcitation is desired.”
Quote in the paperNot a substantial claim - Interpretationreasoning
Conformational changes in the tubulin structure within the microtubule lattice in the presence of paclitaxel are not expected.
“Consequently, conformational changes in the tubulin structure within the microtubule lattice in the presence of paclitaxel are not expected.”
Quote in the paperNot a substantial claim
- May combine two claims. 12
- The quote only partly states this claim. 2
- Classified as probably not a substantial claim. 8
May combine two claims.
Findingown dataIn simulations, heteromolecular coupling between tyrosine and tryptophan residues shows the highest contribution to VCoul, followed by tyrosine-tyrosine coupling, with tryptophan-tryptophan coupling lowest due to longer intermolecular distances.
“The heteromolecular coupling between tyrosine and tryptophan residues shows the highest contribution to the VCoul, followed by tyrosine-tyrosine coupling strengths. Tryptophan-tryptophan coupling strengths are the lowest, as a result of longer intermolecular distances between them (Figure 6B,C).”
Quote in the paperNot a substantial claim- The authors state this as an assumption: The refractive index of the medium surrounding the microtubule is 1.4.
May combine two claims.
Findingown dataEtomidate and isoflurane did not contribute to overall solution fluorescence nor the fluorescence spectra of free GTP-tubulin or AMCA.
“Notably, these anesthetics did not contribute to overall solution fluorescence nor the fluorescence spectra of free GTP-tubulin or AMCA (Figure S6), demonstrating that they did not chemically interfere with either tryptophan or AMCA lifetime.”
Quote in the paperSubstantial claimMay combine two claims.
Findingown dataDocking simulations showed both etomidate and isoflurane exhibited affinities to 16 distinct binding sites, including vinca, taxol, and colchicine sites, with low predicted binding energies, indicating weak to moderate interactions and no distinct preference.
“Our results showed that both macromolecules exhibited affinities to 16 distinct binding sites (including the vinca, taxol, and colchicine sites), but with low predicted binding energies, which indicates weak to moderate interactions with tubulin, with no distinct preference for any of these sites.”
Quote in the paperSubstantial claimThe quote only partly states this claim.
Findingown dataCharge transfer integral magnitudes for five representative TYR dimers with interaromatic distance < 6.3 Å range up to 419 cm-1.
“We observed charge transfer integral magnitudes ranging up to 419 cm–1”
Quote in the paperSubstantial claimMay combine two claims.
Findingown dataSimulated diffusion lengths considering only intertyrosine interactions and considering tyrosine-tryptophan interactions are 1.11 and 1.54 nm, respectively.
“In both simulations, the obtained diffusion lengths (1.11 and 1.54 nm, respectively) are appreciably lower than the diffusion lengths obtained experimentally.”
Quote in the paperSubstantial claim- The authors state this as an assumption: The refractive index of the medium surrounding the microtubule is 1.4.
The quote only partly states this claim.
Findingown dataStern-Volmer analysis revealed different tryptophan quenching rates in GMPCPP-microtubules compared to GTP-microtubules.
“Stern–Volmer analysis revealed different tryptophan quenching rates in GMPCPP-microtubules, which we ascribe to differences in tryptophan fluorescence lifetime in the absence of AMCA.”
Quote in the paperNot a substantial claimMay combine two claims.
Findingown dataLong-range electronic energy transfer was observed in GMPCPP-microtubules, with diffusion lengths of 6.1 ± 0.1 nm.
“Consequently, long-range electronic energy transfer was observed in GMPCPP-microtubules (diffusion lengths of 6.1 ± 0.1 nm; Figure 5B,C), consistent with multiple step hopping.”
Quote in the paperSubstantial claim- The authors state this as an assumption: The sum of the tryptophan and AMCA radii is 1 nm.
Classified as probably not a substantial claim. May combine two claims.
Findingnone givenLabeling efficiency was 1-2 AMCA molecules per tubulin dimer, attached at random surface lysines.
“Labeling efficiency was 1–2 AMCA molecules per tubulin dimer, attached at random surface lysines.”
Quote in the paperSubstantial claimMay combine two claims.
Interpretationown dataEtomidate and isoflurane did not chemically interfere with either tryptophan or AMCA lifetime.
“Notably, these anesthetics did not contribute to overall solution fluorescence nor the fluorescence spectra of free GTP-tubulin or AMCA (Figure S6), demonstrating that they did not chemically interfere with either tryptophan or AMCA lifetime.”
Quote in the paperSubstantial claimMay combine two claims.
Interpretationown dataThe 2D tryptophan photoexcitation diffusion length of 6.64 nm is surprisingly high in microtubules given their structural roles and the chlorophyll a equivalent value of 20-80 nm.
“The two-dimensional tryptophan photoexcitation diffusion length of 6.64 nm is surprisingly high in microtubules, given that they are optimized to play structural roles in the cell and that the equivalent value for chlorophyll a, which is optimized for electronic energy transfer, is only 20–80 nm.”
Quote in the paperSubstantial claim0 of 4 sources checked- cites [23] source
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- cites [24] source
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- cites [59] source
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- The authors state this as an assumption: The sum of the tryptophan and AMCA radii is 1 nm.
May combine two claims.
Interpretationown dataPhotoexcitation energy migration likely takes place preferentially along a protofilament or along the tubulin ring along a helical path.
“It is likely that photoexcitation energy migration takes place preferentially along a protofilament or along the tubulin ring along a helical path (Figure S13).”
Quote in the paperSubstantial claimMay combine two claims.
Study design and conductreasoningThe diffusion length calculated using the method employed in this work is not definite but should be a reliable order of magnitude estimate.
“Therefore, the diffusion length calculated using the method employed in this work is not definite but should be a reliable order of magnitude estimate.”
Quote in the paperSubstantial claimProbably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.
Study design and conductown dataAverage weighted values were estimated by finding the weighted lifetime of tryptophan fluorescence lifetime and then determining the average over n = 3 to 5 experiments.
“Average weighted values were estimated by finding the weighted lifetime of tryptophan fluorescence lifetime (the parameters T1, T2, and T3 were weighted using amplitudes A1, A2, and A3) and then determining the average of this value over n = 3 to 5 experiments.”
Quote in the paperNot a substantial claimClassified as probably not a substantial claim.
Study design and conductnone givenThe time-resolved spectra were corrected for instrument response function (IRF) using an aqueous Ludox colloidal silica solution.
“The time-resolved spectra were corrected for instrument response function (IRF) using an aqueous Ludox colloidal silica solution (Figure S3a).”
Quote in the paperSubstantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
Study design and conductnone givenMeasurements on free tubulin in solution were performed in the presence of 10 mM CaCl2 to ensure that free tubulin remained in solution.
“Measurements on free tubulin in solution were performed in the presence of 10 mM CaCl2 (BRB80Ca) to ensure that free tubulin remained in solution.”
Quote in the paperNot a substantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
Study design and conductnone givenA long pass dielectric filter with a transition wavelength of 325 nm was placed after the solution and before the detector to reduce scatter signal.
“A long pass dielectric filter with a transition wavelength of 325 nm was placed after the solution and before the detector to reduce scatter signal.”
Quote in the paperNot a substantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationThe binding of paclitaxel counters the conformational effect of GTP-hydrolysis on microtubules, stabilizing microtubules against depolymerization.
“The binding of paclitaxel counters the conformational effect of GTP-hydrolysis on microtubules, stabilizing microtubules against depolymerization.69,70”
Quote in the paperNot a substantial claim0 of 2 sources checkedClassified as probably not a substantial claim. May combine two claims.
InterpretationreasoningBiochemically tuned electronic energy migration would allow microtubule architectures to be used as targets for photobiomodulation and to transduce photonic energy in biohybrid devices.
“Biochemically tuned electronic energy migration would allow microtubule architectures to be used as targets for photobiomodulation9,63 and to transduce photonic energy in biohybrid devices.64”
Quote in the paperSubstantial claim0 of 3 sources checked- cites [9] source
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- cites [63] source
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- Rests on an assumption: Tryptophan quenching by AMCA is a valid measure of photoexcitation diffusion in microtubules.
Probably not a substantial claim: may not pass S4 (based).
Study design and conductnone givenThe usage of 305 nm light ensured that tyrosine and phenylalanine were not photoexcited.
“The usage of 305 nm light ensured that tyrosine and phenylalanine were not photoexcited.”
- Also stated in: § Time-Correlated Single Photon Counting (TCPSC) · plain
“These excitation and detection wavelengths were selected to ensure that tyrosine and phenylalanine were not photoexcited.”
Quote in the paperNot a substantial claim- Also stated in: § Time-Correlated Single Photon Counting (TCPSC) · plain
The authors state this as an assumption.
The sum of the tryptophan and AMCA radii is 1 nm.
“r is the sum of the tryptophan and AMCA radii (assumed here to be 1 nm).”
The authors state this as an assumption.
The refractive index of the medium surrounding the microtubule is 1.4.
“n is the refractive index of the medium surrounding the microtubule (assumed to be n = 1.4).”
The paper relies on this without support.
Tryptophan quenching by AMCA is a valid measure of photoexcitation diffusion in microtubules.
“introducing a convulsant (50 μM picrotoxin) also decreased tryptophan quenching by AMCA.”
“The tuning of photoexcitation diffusion length through biochemical parameters of microtubules (tubulin polymerization, introduction of anesthetics) was a further intriguing observation.”
The paper relies on this without support.
AMCA labeling at random surface lysines does not perturb tubulin structure or photoexcitation energy migration.
“Labeling efficiency was 1–2 AMCA molecules per tubulin dimer, attached at random surface lysines.”
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Functionally relevant quantum effects occur in microtubules at room temperature.
“I also review experimental evidence that functionally relevant quantum effects occur in microtubules at room temperature”
From A quantum microtubule substrate of consciousness is experimentally supported and solves the binding and epiphenomenalism problems (2025) · cites this paper as Kalra et al. 2023
The Results report electronic energy migration in microtubules, and Methods > Steady-State Measurements says those measurements were performed at room temperature. But the paper does not establish that this effect has a biological function: the Discussion and Conclusion says it is unlikely that biological systems use tubulin’s light-harvesting properties. It also does not demonstrate functionally relevant quantum coherence. (LLM, conf=0.88)
Experimental — accuracy not yet measuredQuantum optical effects in MTs were shown to be dampened by inhalational anesthetics.
“Moreover, quantum optical effects in MTs were shown to be dampened by inhalational anesthetics (Kalra et al. 2023), supporting the view of anesthesia I outlined in the previous section.”
From A quantum microtubule substrate of consciousness is experimentally supported and solves the binding and epiphenomenalism problems (2025) · cites this paper as Kalra et al. 2023
The Results section, “Electronic Energy Migration Is Dampened by Anesthetics Etomidate and Isoflurane” (page not specified), reports reduced photoexcitation diffusion in microtubules with both anesthetics. It does not establish that quantum optical effects or long-range dipole switching were dampened; it explicitly says the latter had not been experimentally evaluated. The copy also does not characterize both tested anesthetics as inhalational. (LLM, conf=0.86)
Experimental — accuracy not yet measuredRecent experimental studies have demonstrated that microtubules can capture and transfer energy over distances of approximately 6.6 nm, surpassing classical predictions.
“Recent experimental studies have demonstrated that microtubules can capture and transfer energy over distances of approximately 6.6 nm, surpassing classical predictions [48,49,50].”
From Quantum Models of Consciousness from a Quantum Information Science Perspective (2025) · cites this paper as [49]
Kalra et al. (2023) showed that tryptophan fluorescence lifetimes propagated and persisted due to quantum exciton mechanisms, and these were dampened by isoflurane and etomidate.
“Kalra et al. (2023) showed that tryptophan fluorescence lifetimes propagated and persisted due to quantum exciton mechanisms, and these were dampened by two types of anesthetic, isoflurane and etomidate.”
From Microtubule-stabilizer epothilone B delays anesthetic-induced unconsciousness in rats (2024) · cites this paper as Kalra et al., 2023
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
Each contradiction between two passages listed here was confirmed by an independent check.
Conflicting CaCl2 concentrations for free-tubulin measurements
MajorThe Tubulin Polymerization methods specify 10 mM CaCl2 for measurements on free tubulin, but the Steady-State Measurements methods define the free-tubulin background buffer as containing 1 mM CaCl2.
“Measurements on free tubulin in solution were performed in the presence of 10 mM CaCl2 (BRB80Ca) to ensure that free tubulin remained in solution.”
“BRB80Ca (BRB80 supplemented with 1 mM GTP or GMPCPP and 1 mM CaCl2) for free GTP-tubulin solutions.”
Free-tubulin quenching constant has conflicting units
MinorThe Results text gives the free GTP-tubulin quenching constant as 7.5 ps-1, while Table 1 gives essentially the same value in ns-1. These units differ by a factor of 1,000.
“Our analysis for microtubules and free GTP-tubulin in solution revealed quenching constants of 23.8 ± 0.8 ns–1 and 7.5 ± 0.4 ps–1, respectively (Figure 4A, Table 1).”
“| tubulin polymerization state | KQ (ns–1) | Adj R2 | | --- | --- | --- | | Free GTP-tubulin | 7.46 ± 0.4 | 0.96 |”
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Tuszyński, J. A. (2024) · Wiley eBooks · doi:10.1002/9781119865667.ch16
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Collapse and Evolution’s Solutions
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On the functional significance of quantum effects at subneuronal scales
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- Authors
- Kalra, A. P., Benny, A., Travis, S. M., Zizzi, E. A., Morales-Sanchez, A., Oblinsky, D. G., Craddock, T. J. A., Hameroff, S. R., MacIver, M. B., Tuszyński, J. A., Petry, S., Penrose, R., & Scholes, G. D.
- Affiliations
- Princeton University (US)
- Politecnico di Torino (IT)
- Nova Southeastern University (US)
- University of Arizona (US)
- Stanford Medicine (US)
- University of Alberta (CA)
- University of Oxford (GB)
- Corresponding author
- Scholes, Gregory D.
- ORCID
- Venue
- ACS Central Science
- Publisher
- American Chemical Society (ACS)
- Published
- 2023-01-12
- Volume
- 9
- Issue
- 3
- Pages
- 352-361
- ISSN
- 2374-7943 (ISSN-L)
- 2374-7951
- PMC
- PMC10037452
- OpenAlex
- W4315784035
- Cited by
- 80
- References
- 71
- Citations by year
- 2026: 32 · 2025: 16 · 2024: 23 · 2023: 9
- FWCI
- 11.96
- Type
- journal article
- Language
- en
- Open access
- diamond
- doi.org
- Licence
- Locations
- ACS Central Science (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- arXiv (Cornell University) (submittedVersion)
- PORTO@Iris (submittedVersion, cc-by)
- arXiv (Cornell University) (cc-by)
- Funders
- Nova Southeastern University (PFRDG334807)
- U.S. Department of Defense (W911NF-19-1-0373-(74884-PH))
- Templeton World Charity Foundation (TWCF0530)
- Topics
- Physical Sciences › Chemistry › Physical and Theoretical Chemistry › Photochemistry and Electron Transfer Studies
- Physical Sciences › Physics and Astronomy › Atomic and Molecular Physics, and Optics › Spectroscopy and Quantum Chemical Studies
- Health Sciences › Medicine › Physiology › Biofield Effects and Biophysics
- Keywords
- microtubules, tubulin, excitation energy transfer, exciton diffusion, light harvesting, microtubule assembly, protofilament number, etomidate, isoflurane, fluorescence resonance energy transfer, biohybrid devices
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Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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