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Rapid and ultrasensitive electromechanical detection of ions, biomolecules and SARS-CoV-2 RNA in unamplified samples

Abstract

The detection of samples at ultralow concentrations (one to ten copies in 100 μl) in biofluids is hampered by the orders-of-magnitude higher amounts of ‘background’ biomolecules. Here we report a molecular system, immobilized on a liquid-gated graphene field-effect transistor and consisting of an aptamer probe bound to a flexible single-stranded DNA cantilever linked to a self-assembled stiff tetrahedral double-stranded DNA structure, for the rapid and ultrasensitive electromechanical detection (down to one to two copies in 100 μl) of unamplified nucleic acids in biofluids, and also of ions, small molecules and proteins, as we show for Hg2+, adenosine 5′-triphosphate and thrombin. We implemented an electromechanical biosensor for the detection of SARS-CoV-2 into an integrated and portable prototype device, and show that it detected SARS-CoV-2 RNA in less than four minutes in all nasopharyngeal samples from 33 patients with COVID-19 (with cycle threshold values of 24.9–41.3) and in none of the 54 COVID-19-negative controls, without the need for RNA extraction or nucleic acid amplification.

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Fig. 1: MolEMS and MolEMS g-FET.
Fig. 2: Ultrasensitive biodetection and long-term stability.
Fig. 3: Universality, specificity and structural design.
Fig. 4: SARS-CoV-2 nucleic acid testing.

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Data availability

The main data supporting the results in this study are available within the paper and its Supplementary Information. The raw and analysed datasets generated during the study are too large to be shared publicly, yet they are available for research purposes from the corresponding authors on reasonable request.

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Acknowledgements

We thank K. Vesterager Gothelf from Aarhus University for the valuable discussion on this research. This work was supported by the National Key R&D Program of China (2021YFE0201400), the National Natural Science Foundation of China (51773041, 61890940, 21603038), the Shanghai Committee of Science and Technology in China (18ZR1404900), the Chongqing Bayu Scholar Program (DP2020036), the Strategic Priority Research Program of the Chinese Academy of Sciences (XDB30000000), the China Postdoctoral Science Foundation (2019M661338, 2016LH00046, 2019M661353), the National Postdoctoral Program for Innovative Talents (BX20190072), the Major Project of MOST in China (2018ZX10714002-001-005) and biosafety level 3 laboratory of Fudan University.

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Contributions

D.W. supervised the project. D.W. conceived the original idea and designed all aspects of the experiments. L.W. and Y.G.W. prepared MolEMS. X.W., Y.G.W. and D.K. fabricated devices. L.W. did AFM, transmission electron microscopy, Raman, scanning electron microscopy and gel electrophoresis. X.W., C.Z., C.D. and L.W. did fluorescence measurements. X.W. measured FRET. C.G., Y.W., D.Q. and Y.X. prepared SARS-CoV-2 virus cDNA samples. M.G. and Z.Z. provided clinical samples. C.G., Y.X., M.G. and Z.Z. measured qRT–PCR. X.W., Y.G.W., C.D., D.K. and D.W. measured devices. D.W., L.W., X.W., Y.G.W., Y.L. and C.F. analysed the data and prepared the manuscript. All authors commented on the manuscript.

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Correspondence to Zhaoqin Zhu or Dacheng Wei.

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Extended data

Extended Data Fig. 1 Antifouling performance against BSA.

a, b, ∆Ids/Ids0 responses of a bare g-FET upon addition of BSA with concentrations from 2.5 × 10−13 M to 5 × 10−11 M in 1×TM buffer. c, d, ∆Ids/Ids0 responses of a g-FET modified with a BSA antifouling layer upon addition of BSA with concentrations from 2.5 × 10−13 M to 5 × 10−11 M in 1×TM buffer. To modify the graphene surface with the BSA layer, we added 50 μL 1×TM buffer solution with 1 × 10−3 M BSA in the PDMS well of the device. After 12-hours incubation, the g-FET was washed using 1×TM buffer by three times. e, f, ∆Ids/Ids0 responses of a MolEMS g-FET upon addition of BSA with concentrations from 2.5 × 10−13 M to 5 × 10−11 M in 1×TM buffer. The MolEMS g-FET exhibits an antifouling ability against unspecific adsorption of BSA. All samples were technical replicates.

Extended Data Fig. 2 Long-term stability of the MolEMS g-FETs.

a, b, ∆Ids/Ids0 responses of a MolEMS g-FET with DH25.42 aptamer probes upon addition of 5 × 10−15 M and 5 × 10−14 M ATP in full serum. c, d, ∆Ids/Ids0 responses of the same MolEMS g-FET device upon addition of 5 × 10−15 M and 5 × 10−14 M ATP in full serum, after continuous exposure in full serum for 15 days at 4 °C. The response maintains ~56% in full serum after 15 days. All samples were technical replicates.

Extended Data Fig. 3 Real-time detection of Hg2+, ATP and ss-DNA.

∆Ids/Ids0 responses of MolEMS g-FETs with corresponding probes upon addition of (a) Hg2+ (1×TM), (b) ATP (full serum) and (c) ss-DNA-T (full serum) with concentrations from 5 × 10−20 M to 2.5 × 10−10 or 5 × 10−10 M under an electrostatic actuation. All samples were technical replicates.

Extended Data Fig. 4 Selectivity of the MolEMS g-FET sensors.

Real-time ∆Ids responses of MolEMS g-FETs carrying different probes upon targeted (5 × 10−16 M) and non-targeted (5 × 10−15 M) analytes. a, The targeted analyte is thrombin, and non-targeted analytes are Casein and BSA. b, The targeted analyte is ATP, and non-targeted analytes are CTP and GTP. c, The targeted analyte is Hg2+, and non-targeted analytes are Fe3+, Cd2+, Zn2+, Ca2+ and Cu2+. All samples were technical replicates.

Extended Data Fig. 5 Specificity towards mixture samples.

|∆Ids/Ids0| responses of MolEMS g-FETs upon non-targeted (5 × 10−15 M) analytes and upon mixture samples with the targeted analytes (5 × 10−16 M) and non-targeted analysts (5 × 10−15 M). The mixed samples are a mixture of 5 × 10−16 M Thrombin, 5 × 10−15 M Casein, 5 × 10−15 M BSA; a mixture of 5 × 10−16 M ATP, 5 × 10−15 M CTP, 5 × 10−15 M GTP; a mixture of 5 × 10−16 M Hg2+, 5 × 10−15 M Fe3+, 5 × 10−15 M Cd2+, 5 × 10−15 M Zn2+, 5 × 10−15 M Ca2+, 5 × 10−15 M Cu2+; and a mixture of 5 × 10−16 M ss-DNA-T, 5 × 10−15 M ss-DNA-mis-3’, 5 × 10−15 M ss-DNA-mis-m, 5 × 10−15 M ss-DNA-mis-5’. All samples were technical replicates.

Extended Data Fig. 6 Calculation of the LoD.

The LoD values were obtained from the interception of the noise level and the linear standard curve of |∆Ids/Ids0| versus concentration for the SARS-CoV-2 viral cDNA (a) and the SARS-CoV-2 IVT RNA (b) detection. The error bars are defined by the standard deviation of the results from 3 parallel experiments. In high concentration region, the larger error bars are probably attributed to the difference of the probe density on each device. All samples were technical replicates.

Extended Data Fig. 7 Real-time detection of clinical samples from COVID-19 patients.

|∆Ids/Ids0| versus t curves upon addition of clinical samples (a) P4, (b) 50% and 100% P7, (c) P18 and (d) P21. All samples were biological replicates.

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Wang, L., Wang, X., Wu, Y. et al. Rapid and ultrasensitive electromechanical detection of ions, biomolecules and SARS-CoV-2 RNA in unamplified samples. Nat. Biomed. Eng 6, 276–285 (2022). https://doi.org/10.1038/s41551-021-00833-7

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